Review ArticleDiversity of the DNA Replication System in the Archaea Domain

Felipe Sarmiento1 Feng Long1 Isaac Cann2 and William B Whitman1

1 Department of Microbiology University of Georgia 541 Biological Science Building Athens GA 30602-2605 USA2 3408 Institute for Genomic Biology University of Illinois 1206 W Gregory Drive Urbana IL 61801 USA

Correspondence should be addressed to William B Whitman whitmanugaedu

Received 21 October 2013 Accepted 16 February 2014 Published 26 March 2014

Academic Editor Yoshizumi Ishino

Copyright copy 2014 Felipe Sarmiento et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

The precise and timely duplication of the genome is essential for cellular life It is achieved by DNA replication a complex processthat is conserved among the three domains of life Even though the cellular structure of archaea closely resembles that of bacteriathe information processing machinery of archaea is evolutionarily more closely related to the eukaryotic system especially for theproteins involved in the DNA replication process While the general DNA replication mechanism is conserved among the differentdomains of life modifications in functionality and in some of the specialized replication proteins are observed Indeed Archaeapossess specific features unique to this domain Moreover even though the general pattern of the replicative system is the same inall archaea a great deal of variation exists between specific groups

1 Introduction

Archaea are a diverse group of prokaryotes which are unitedby a number of unique features Many of these microorgan-isms normally thrive under extreme conditions of tempera-ture salinity pH or pressure However some also coexist inmoderate environments with Bacteria and eukaryotes [1 2]Likewise a wide range of lifestyles including anaerobic andaerobic respiration fermentation photo- and chemoautotro-phy and heterotrophy are common among this group Inspite of this diversitymembers of theArchaeadomain possessspecific physiological characteristics that unite them suchas the composition and structure of their membrane lipids[3]

Archaea for the most part resemble Bacteria in sizeand shape but they possess important differences at geneticmolecular and metabolic levels Remarkable differences arepresent in the machinery and functionality of the infor-mation processing systems For example the histones insome Archaea [4] the similarity of proteins involved intranscription and translation and the structure of the ribo-some are more closely related to those of eukaryotes thanBacteria [5] The most striking similarities between Archaeaand eukaryotes are observed in DNA replication one of themost conserved processes in living organisms where the

components of the replicative apparatus and the overallprocess closely resemble a simplified version of the eukaryoticDNA replication system [6 7] However a few characteristicsof the archaeal information processing system are sharedonly with Bacteria such as the circular topology of thechromosome the small size of the genome and the pres-ence of polycistronic transcription units and Shine-Dalgarnosequences in the mRNA instead of Kozak sequences [8 9]These observations suggest that archaeal DNA replication isa process catalyzed by eukaryotic-like proteins in a bacterialcontext [10] In addition there are specific features whichbelong only to the domain Archaea such as the DNApolymerase D which add another level of complexity anduniqueness to these microorganisms While a number ofevolutionary hypotheses have been proposed to accountfor the mosaic nature of this process [11 12] comparativegenomics and ultrastructural studies support two alternativescenarios The archezoan scenario holds that an archaealancestor developed a nucleus and evolved into a primitivearchezoan which later acquired an 120572-proteobacterium toform the mitochondrion and evolved into the eukaryotesThe symbiogenesis scenario holds that an archaeal ancestorplus an 120572-proteobacterium formed a chimeric cell whichthen evolved into the eukaryotic cell [12] A major differ-ence between these hypotheses is the time when the first

Hindawi Publishing CorporationArchaeaVolume 2014 Article ID 675946 15 pageshttpdxdoiorg1011552014675946

2 Archaea

eukaryotes evolved In the archezoan scenario the ancestorsof the early eukaryotes are as ancient as the two prokaryoticlineages the Bacteria and Archaea In the symbiogenesisscenario the eukaryotes evolved relatively late after thediversification of the ancient archaeal and bacterial line-ages

The cultivated Archaea are taxonomically divided intofive phyla Crenarchaeota and Euryarchaeota are best char-acterized and this taxonomic division is strongly supportedby comparative genomics A number of genes with keyroles in chromosome structure and DNA replication arepresent in one phylum but absent in the other Crenar-chaeotes also exhibit a vast physiological diversity includingaerobes and anaerobes fermenters chemoheterotrophs andchemolithotrophs [2] The majority of the cultivated crenar-chaeotes are also thermophiles [13] Euryarchaeotes exhibitan even larger diversity with several different extremophilesamong their ranks in addition to large numbers ofmesophilicmicroorganisms Interestingly all the known methanogensbelong to this phylum Additionally environmental sequenc-ing 16S rRNA analysis and cultivation efforts provide strongevidence for three additional phylaThaumarchaeota Korar-chaeota and Aigarchaeota [14ndash16] A sixth phylum has alsobeen proposed previously the Nanoarchaeota This phy-lum includes the obligate symbiont Nanoarchaeum equitanswhich has a greatly reduced genome [17] However a morecomplete analysis of its genome suggests that N equitanscorresponds to a rapidly evolving euryarchaeal lineage andnot an early archaeal phylum [18]

2 General Overview ofthe DNA Replication Process

The general process of DNA replication is conserved amongthe three domains of life but each domain possesses somefunctional modifications and variations in key proteinsDNA replication may be divided into four main stepsStep 1 (Preinitiation) starts when specific proteins recognizeand bind the origin of replication forming a protein-DNAcomplex This complex recruits an ATP-dependent helicaseto unwind the double-stranded DNA (dsDNA) The single-stranded DNA (ssDNA) formed is then protected by ssDNA-binding proteins (SSB) Step 2 (Initiation) corresponds to therecruitment of the DNA primase and DNA polymerase Step3 (Elongation) corresponds to the duplication of both strandsof DNA at the same time by the same unidirectional replica-tion machine Because of the antiparallel nature of the DNAthe leading strand is copied continuously and the laggingstrand is copied discontinuously as Okazaki fragments [10]During replication a sliding-clamp protein surrounds theDNA and binds to the polymerase to increase processivityor the number of nucleotides added to the growing strandbefore disassociation of the polymerase from the templateStep 4 (Maturation) corresponds to the completion of thediscontinuous replication in the lagging strand by the actionsof RNase DNA ligase and Flap endonucleaseThe variabilityof the players involved in each of these processes between thethree domains of life andmore specifically within theArchaeadomain is discussed in further detail below

3 DNA Replication Components

31 Preinitiation (Origin of Replication and Origin Recogni-tion) The number of origins of replication in a genome iscorrelated with phylogeny and varies among the differentdomains [19] Members of the Bacteria domain usuallypossess only one replication origin but eukaryotic chromo-somes contain multiple replication origins This differencewas generally accepted as a clear divisor in DNA repli-cation of eukaryotes and prokaryotes However membersof the Archaea domain display either one or multiple ori-gins of replication The origins of replication in archaeaare commonly AT-rich regions which possess conservedsequences called origin of recognition boxes (ORB) and arewell conserved across many archaeal species Also smallerversions of the ORBs calledmini-ORBs have been identified[20] Members of the Crenarchaeota phylum display multipleorigins of replication For example species belonging to theSulfolobales order contain three origins of replication [20 21]Likewise two and four origins of replication have been foundin members of the Desulfurococcales (Aeropyrum pernix)and Thermoproteales (Pyrobaculum calidifontis) respectively[22 23] In addition to shortening the time required forreplication multiple origins may play a role in counteractingDNA damage during hyperthermophilic growth [24] Incontrast most members of the Euryarchaeota phylum seemto possess only one origin of replication For example speciesbelonging to the Thermococcales (Pyrococcus abyssi) andArchaeoglobales (Archaeoglobus fulgidus) orders contain onlyone origin of replication [25ndash27] However members ofthe order Halobacteriales (eg Halobacterium sp NRC-1Haloferax volcanii andHaloarcula hispanica) possess numer-ous origins of replication that may be part of an intricatereplication initiation system [28ndash30] In fact a recent reportdemonstrated that the different origins of replication inHaloarcula hispanica are controlled by diverse mechanismswhich suggest a high level of coordination between themultiple origins [31] In contrast the deletion of a singleorigin of replication in Haloferax volcanii affects replicationdynamics and growth but the simultaneous deletion of allfour origins of replication accelerated growth compared tothe wild type strain [32] These results suggest that initiationof replication in Haloferax volcanii may be dependent ofhomologous recombination as it is in some viruses andgenerate questions about the purpose of the replicationorigins [32] With the exception of Methanothermobacterthermautotrophicus the DNA replication origin has not beenexperimentally demonstrated in themethanogens [33] How-ever bioinformatics analysis by GC-skew in Methanosarcinaacetivorans [34] and119885-curve analysis forMethanocaldococcusjannaschii and Methanosarcina mazei suggest a single originof replication A similar analysis of M maripaludis S2 wasinconclusive [35] The fact that the order Halobacteriales isthe only euryarchaeote that displays multiple origin of repli-cation suggests that there may have been a lineage-specificduplication in this group Moreover the number of origins isnot highly conserved even within a single archaeal phylum

The origin of replication is recognized by specific proteinsthat bind and melt the dsDNA and assist in the loading of

Archaea 3

Order Phylum Number ofgenomes

Number of homologs for replication genesORCCDC6 GINS15 GINS23 RPA MCM RFCS PCNA PolB DP1 DP2

Nitrosopumilales Thaumarchaeota 2 1 0 or 1 0 or 1 1 1 1 1 1 1 1

Thermoproteales

Crenarchaeota

14 0 0 1 1 to 3 1 to 3 0 09 2 0 0 or 1 1 0 0Desulfurococcales

15 3 1 1 1 1 1 3 0 0SulfolobalesNot named Korarchaeota 1 2 0 0 0 1 1 1 2 1 1Nanoarchaeota 1 1 0 0 1 1 1 1 1 1 1Thermococcales 11 1 1 3 1 1 1

1Methanopyrales 1 0 0 0 0 1 1 1 1 11

Methanobacteriales 7 1 or 2 0 or 1 0 1 1 1 2 1 1

Methanococcales Euryarchaeota 15 0 0 0 2 to 4 2 to 8 1 1 1 1

Thermoplasmatales 4 0 1 1 1 1 1 1 1

Archaeoglobales 4 2 or 3 0 0 1 or 2 1 1 1 1

Halobacteriales 15 3 to 15 0 0 1 1 or 2 1 1 1

Methanomicrobiales 6 0 0 1 1 2 1 1 or 2 1 1

Methanocellales 1 2 0 0 1 1 1 1 3 1 1Methanosarcinales 9 0 0 3 1 1

0lowast

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Figure 1 Homologs for some key genes involved in archaeal DNA replication Archaeal orders are phylogenetically organized followinga rooted maximum likelihood tree of Archaea based on 53 concatenated ribosomal proteins [36] The homology search was performedby RAST v40 (Rapid Annotation using Subsystem Technology) and the annotated data was viewed through the SEED viewer(httpwwwtheseedorg) A total of 115 archaeal genome sequences were obtained from NCBI and uploaded into the RAST server RASTannotation was performed using default parameters with the genetic code for Bacteria and Archaea The replication proteins homologswere checked through the SEED subsystem DNA replication Homology results of Thermococcus kodakaraensis KOD1 Pyrococcus furiosusDSM 3638 and Thermofilum pendens Hrk 5 were searched for replication protein homologs using BLAST (blastx v2228+) Results withhomology coverage of gt80 and 119864-values less than 0001 were considered as real homologs The results were also supplemented withdata from literature reviews and BLAST searches When indicated in the figure zero (0) homologs means that no homolog was foundfor a specific gene by using the described methodology Asterisks indicate that one or two of the analyzed microorganisms possessan exception for that specific feature Exceptions noted are (featureorder) ORC1CDC6Thermoproteales Thermofilum pendens Hrk5 (3homologs) and Thermosphaera aggregans DSM11486 (2 homologs) ORC1CDC6Thermoplasmatales and Picrophilus torridus DSM 9790(1 homolog) ORC1CDC6Methanomicrobiales and Methanoplanus petrolearius DSM11571 (4 homologs) ORC1CDC6Methanosarcinalesand Methanosalsum zhilinae DSM4017 (4 homologs) GINS15Thermoplasmatales and Thermoplasma acidophilum DSM1728 (1 homolog)GINS23Desulfurococcales Staphylothermus hellenicus DSM12710 (no homolog) and Staphylothermus marinus F1 (no homolog)GINS23Thermococcales Pyrococcus horikoshii OT3 (2 homologs) RPAThermoproteales Thermofilum pendens Hrk5 (3 homologs)and Thermosphaera aggregans DSM11486 (1 homolog) RPAMethanobacteriales and Methanothermus fervidus DSM2088 (no homolog)RPAArchaeoglobales and Archaeoglobus fulgidus DSM4304 (1 homolog) MCMThermococcales and Thermococcus kodakaraensis KOD1(3 homologs) MCMMethanosarcinales and Methanosarcina acetivorans C2A (2 homologs) RFCSDesulfurococcales and Hyperthermusbutylicus DSM 5456 (2 homologs) RFCSHalobacteriales and Haloquadratum walsbyi DSM16790 (1 homolog) RFCSMethanosarcinalesMethanosaeta concilii CG6 (2 homologs) and Methanosaeta thermophila PT (2 homologs) PCNADesulfurococcales and Ignisphaeraaggregans DSM17230 (1 homolog) PCNASulfolobales and Metallosphaera cuprina Ar-4 (1 homolog) PCNAThermococcales Pyrococcushorikoshii OT3 (2 homologs) and Thermococcus kodakaraensis KOD1 (2 homologs) PCNAMethanococcales Methanococcus maripaludisS2 (2 homologs) and Methanotorris igneus Kol5 (2 homologs) PolBThermoproteales Caldivirga maquilingensis IC-167 (3 homologs)and Pyrobaculum calidifontis JCM 11548 (3 homologs) PolBDesulfurococcales Staphylothermus hellenicus DSM12710 (3 homologs) andStaphylothermus marinus F1 (3 homologs) PolBArchaeoglobales Archaeoglobus fulgidus DSM4304 (2 homologs) PolBHalobacterialesHalorhabdus utahensis DSM12940 (2 homologs) PolBMethanosarcinales Methanosaeta concilii GP6 (2 homologs) DP1MethanosarcinalesMethanococcoides burtonii DSM6242 (2 homologs)

the replicative helicases In Bacteria this protein is DnaAwhich binds to the DnaA boxes [37] In eukaryotes aprotein complex known asORC (origin recognition complex)composed of 6 different proteins (Orc1-6) binds at thereplication origin and recruits other proteins [38] InArchaeathe candidate for replication initiation is a protein that shareshomology with the eukaryotic Orc1 and Cdc6 (cell divisioncycle 6) proteins and is encoded by almost all archaealgenomes [39] Their genes are commonly located adjacent tothe origin of replication These proteins termed Orc1Cdc6homologs have been studied in detail in representatives of theEuryarchaeota (Pyrococcus) and Crenarchaeota (Sulfolobus)and have been shown to bind to the ORB region with highspecificity [20 26 40] In addition purified Orc1Cdc6 from

S solfataricus binds to ORB elements from other crenar-chaeotes and euryarchaeotes in vitro suggesting that theseproteins recognize sequences conserved across the archaealdomain [20] The crystal structures of these proteins fromPyrobaculum aerophilum [41] and Aeropyrum pernix [42]have been solved contributing to the overall understandingof their activity during the initiation of replication (reviewedin [43]) In general the number of Orc1Cdc6 homologsfound in archaeal genomes varies between one and three(Figure 1) However there are some interesting exceptionsMembers of the order Halobacteriales possess between 3 and15Orc1Cdc6 homologs which may reflect the large numberof origins of replication Interestingly like other members oftheMethanosarcinales the extremely halophilic methanogen

4 Archaea

Methanohalobium evestigatum Z-7303 only possesses twoOrc1Cdc6 homologs Thus the ability to grow at extremelyhigh concentrations of salt and to maintain high intracellularsalt concentrations does not necessarily require a largenumber of Orc1Cdc6 homologsAlthoughmost members ofthe orderMethanomicrobiales possess two copies of this geneMethanoplanus petroleariusDSM 11571 possesses four copiesThus the number of Orc1Cdc6 homologs varies consider-ably among the euryarchaeotes In an extreme case repre-sentatives of the ordersMethanococcales andMethanopyralesdo not possess any recognizable homologs for the Orc1Cdc6protein [7 44] and the mechanics of replication initiation inthese archaea remain an intriguing unknown of the archaealreplication process

32 Initiation (DNA Unwinding and Primer Synthesis) AfterOrc1Cdc6 proteins bind to the origin of replication ahelicase is recruited to unwind the dsDNA In Bacteria thereplicative helicase is the homohexamer DnaB In eukaryotesthe most likely candidate for the replicative DNA helicase isthe MCM (minichromosome maintenance) complex whichis a heterohexamer that is activated when associated withother replicative proteins forming the CMG (Cdc45-MCM-GINS) complex [45ndash48] As in eukaryotes in Archaea themost probable candidate for the replicative helicase is theMCM complex Intriguingly theMCM complexes in eukary-otes and archaea possess a 31015840-51015840 unwinding polarity but thebacterialDnaBhelicase unwinds duplexDNAon the oppositedirection with a distinct 51015840-31015840 polarity [49ndash51]

Most archaeal genomes studied so far encode one MCMhomolog Its helicase activity has been demonstrated invitro for several archaea including Methanothermobacterthermautotrophicus ΔH where the MCM protein forms adimer of hexamers [52 53] The in vivo interaction betweenthe MCM complex and the Orc1Cdc6 proteins has beendemonstrated in other Archaea [54ndash56] Indeed through anin vitro recruiting assay Orc1CDC6 from P furiosus has beendemonstrated as the possible recruiter of the MCM complexto the origin of replication [57] A recent study identifiedthirteen species of archaeawithmultiplemcm genes encodingthe MCM complexes (Figure 1 [58]) The number of mcmhomologs is especially high in the order Methanococcaleswhere different representatives possess from 2 to 8 copies[59 60] For instance Methanococcus maripaludis S2 pos-sesses four homologs of the MCM protein [44] Through ashotgun proteomic study peptides for three of them havebeen detected [61] suggesting that multiple MCMs areexpressed and functional However a genome-wide surveyof gene functionality in M maripaludis demonstrated thatonly one of these genes MMP0030 was likely to be essentialfor growth [62] In addition coexpression of recombinantMCMs from M maripaludis S2 allowed copurification ofall four proteins [59] suggesting that M maripaludis mayform a heterologous multimeric MCM complex Howeverbecause MMP0030 protein is the only mcm gene essentialfor growth a homologous multimeric complex may alsobe possible Similar results have been found in Thermo-coccus kodakaraensis in which three MCM homologs arepresent but only one is essential [63] The T kodakaraensis

MCM system is suggested to form homologous multimericcomplexes [64] A recent study proposed that two of theMCMhomologs that are conserved among representatives ofthe order Methanococcales are a consequence of an ancientduplication that occurred prior to the divergence of thisgroup [59] It has also been proposed that the large numberof MCM homologs in the order Methanococcales is a directconsequence of mobile elements which may have takenadvantage of the ancient duplication of the MCM genes totake over the replication system by forming cellular MCMheterocomplexes [58] In any case the large number of MCMhomologs in the order Methanococcales may be a product ofan intricate and complex evolutionary history Whether ornot it is related to the absence of the replication initiationprotein Orc1Cdc6 is an interesting possibility [58]

In eukaryotes the MCM complex is not active on itsown and requires the association of two accessory factorsthe heterotetrameric GINS complex (from the Japanese go-ishi-ni-san meaning 5-1-2-3 after the four subunits Sld5Psf1 Psf2 and Psf3) and the Cdc45 protein This complexcalled CMG (Cdc45-MCM-GINS) is thought to be the activereplicative helicase [47] Homologs for GINS subunits havebeen identified in Archaea by bioinformatics analysis Onehomolog is most similar to the eukaryotic proteins Psf2and Psf3 (GINS23) and is common in the crenarchaeotesAnother homolog is most similar to the eukaryotic pro-teins Psf1 and Sld5 (GINS15) and is found largely in theeuryarchaeotes [65] The GINS complex is expected to beessential for DNA replication but the distribution of thesetwo different GINS homologs suggests that the presence ofone of them is sufficient for archaeal DNA replication SomeCrenarchaeota (S solfataricus) and some Euryarchaeota (Pfuriosus and T kodakaraensis) possess both homologs andform heterotetramers similar to the ones found in eukaryoteswith a ratio 2 2 [66ndash68] To find homologs of GINS15 andGINS23 in Archaea two known GINS15 (from Sulfolobussolfataricus P2 and Thermococcus gammatolerans EJ3) andthree known GINS23 (from Sulfolobus solfataricus P2 Pyro-coccus yayanosii CH1 andThermococcus gammatolerans EJ3)were used for homology searches These analyses failed toidentifyGINShomologs in several archaeal groups (Figure 1)These results suggest that there are other unknown GINShomologs in archaea or that the sequences have divergedenough between genera not to be recognized by homologysearches In any case a more comprehensive analysis of GINSproteins is necessary to fully understand their function anddistribution in Archaea

The detailed interactions of the GINS andMCM proteinsin archaea appear to be highly variable Although the Ssolfataricus GINS and MCM proteins physically interactin vitro MCM helicase activity was not stimulated in thecomplex [66] In contrast the MCM helicase activity of Tkodakaraensis and P furiosus is clearly stimulated by theirGINS complexes [64 67] The crystal structure of the GINScomplex of T kodakaraensis was recently determined Thebackbone structure and the assembly are similar to thehuman complex with some notable differences [68] Interest-ingly many other euryarchaeotes possess only the homologto GINS15 One of those Thermoplasma acidophilum forms

Archaea 5

a homotetrameric complex [68 69] Moreover in vitro the Tacidophilum MCM helicase activity was not affected by theGINS complex [69] These results suggest that other proteinsmay be involved in the formation of a stable helicase in manyArchaea M maripaludis S2 possesses a hypothetical proteinwhich may correspond to the gene encoding for GINS15which is probably essential for growth [60 62] No homologsof GINS23 are present in the genome ofM maripaludis

The replication related Cdc45 protein is ubiquitous ineukaryotes but its exact role has not yet been elucidatedInterestingly homologs of the Cdc45 protein are not presentin Archaea However a bioinformatics analysis revealed thatthe eukaryotic Cdc45 and the prokaryotic RecJ which is aconserved 51015840-31015840exonuclease in most bacteria and archaeapossess a common ancestry and share a homologous DHHdomain [70] These results suggest that the archaeal RecJmay substitute for the eukaryotic Cdc45 during replicationCircumstantial evidence supports this conclusion In S solfa-taricus a homolog of the DNA binding domain of RecJ waspurified together with a GINS protein [66] Similarly in Tkodakaraensis the RecJ homolog (TK1252p) copurified withproteins of theGINS complex [71] and formed a stable in vitroassociation with the GINS complex [72] Two RecJ homologsare found inM jannaschii (MJ0977 and 0831) and they par-tially complement a recJ mutation in E coliThe recombinantMJ0977 also possesses high levels of thermostable single-stranded DNA degrading activity similar to RecJ [73] In Mmaripaludis S2 four proteins possess the DHH domain withsimilarity to the M jannaschii RecJ homologs (MMP16820547 1078 and 1314) However none of them was essentialfor growth suggesting that the activities were redundant [62]Alternatively another protein which has a low similaritywith M jannaschii RecJ homolog (MMP0285) but possessesthe DHH domain was possibly essential for growth [62]However this protein possesses other domains related totransport which make it an unlikely candidate for RecJThese results are not definitive and more experimental datais needed to assign a function to this protein

As soon as the DNA is unwound ssDNA is protectedfromnucleases chemicalmodification and other disruptionsby ssDNA binding proteins These proteins are present in allthree domains of life and are called SSB in Bacteria wherethey form homotetramers or homodimers [74 75] and RPA(replication protein A) in eukaryotes where they form astable heterotrimer composed of 70 32 and 14 kDa proteins[76] Although all ssDNA binding proteins contain dif-ferent combinations of the oligonucleotideoligosaccharide-binding fold or OB-fold [77] the sequence similarity is lowamong RPA and the bacterial SSBs [43] In Archaea differ-ent types of ssDNA binding proteins have been reportedIn crenarchaeotes an ssDNA binding protein is only wellcharacterized in S solfataricus The S solfataricus ssDNAbinding protein contains only one OB-fold and can adopt aheterotetramer conformation [78] However the protein alsoappears to exist as a monomer [79] This protein appears tobe more similar to the bacterial proteins in sequence but itsstructure is more similar to that of the eukaryotic RPAs [4380] While homologs are recognizable in other members ofthe Sulfolobales andmost otherArchaea they are absent from

the genomes of many members of the closely related orderThermoproteales with some few exceptions (Figure 1) [81]

RPAs have been studied from different representativesof the euryarchaeotes revealing additional diversity M jan-naschii andM thermautotrophicus possess a single RPA sub-unit which shares amino acid similarity with the eukaryoticRPA70 and possesses four and five OB-folds respectively [8283] P furiosus possesses three different RPA subunits whichform a stable heterotrimer that is involved in homologousrecombination in vitro [84] The P furiosus RPA thereforeis similar in subunit organization to the eukaryotic RPATheother members of the Thermococcales genera also possessthree RPA homologs which likely form the homotrimericcomplex described for P furiosus (Figure 1) Methanosarcinaacetivorans also possesses three different RPAproteins (RPA1-3) with four two and two OB-folds respectively Howeverthey do not interact with each other and appear to functionas homodimers [85] This arrangement is common amongthe Methanosarcinales but is not found in the closely relatedmethanogen orders such as the Methanocellales (Figure 1)Members of the order Methanococcales possess two to fourRPA homologs The genome of M maripaludis S2 containsthree possible RPA homologs (MMP0122 0616 and 1032)[60] Only MMP0616 and 1032 were likely to be essential forgrowth [62] suggesting a possible different complex configu-ration for RPA proteins in this archaeon It has been hypoth-esized that the diversity in OB-folds in the archaeal RPAs is adirect consequence of homologous recombination [86]

DNA synthesis starts with the production of a RNAprimer since the DNA polymerases that replicate genomesare incapable of de novo DNA synthesis The RNA primeris synthesized by a DNA-dependent RNA polymerase orprimase DnaG a single subunit protein is the primase inBacteria In eukaryotes a two-subunit primase consisting ofa small catalytic subunit (PriS) and a large subunit (PriL)is found in a complex with DNA polymerase 120572 and itsaccessory B subunit [87] In Archaea the first biochemicallycharacterized primase was the eukaryotic primase-like smallsubunit PriS in M jannaschii [88] Later homologs of thePriS and PriL subunits were described in several Pyrococ-cus species [89ndash93] The eukaryotic-like DNA primase hasalso been characterized in the crenarchaeote S solfataricus[94 95] where it has been shown to interact with MCMthrough GINS23 [66] A unique polymerization activityacross discontinuous DNA templates has been characterizedin the PriSL of S solfataricus suggesting that this primasemay be involved in double-stranded break repair in Archaea[96] So far the eukaryotic-like primases found in archaeaexhibit similar properties PriS functions as the catalyticsubunit and PriL modulate its activity [87] In additionthe archaeal eukaryotic-like primase has the unique abilityto synthesize both DNA and RNA in vitro Indeed theP furiosus PriS synthesizes long DNA fragments but theaddition of PriL regulates the process by decreasing theDNA polymerase activity increasing the RNA polymeraseactivity and decreasing the product length [90] Additionallystudies of the P abyssi enzyme suggest that DNA primasemay also be involved in DNA repair because of the DNApolymerase gap filling and strand displacement activities

6 Archaea

also present in vitro [93] Interestingly the archaeal primasesmall subunit resembles DNA polymerases from the Pol Xfamily in sequence and structure suggesting a similarity intheir catalytic mechanism [96]

Homologs of the bacterial DnaG primase are also foundin archaea However in vitro studies of the P furiosusenzyme failed to detect primer synthesis activity and the TkodakaraensisDnaG was copurified with proteins of the exo-some [71] Also in S solfataricus DnaG primase was found tobe a core exosome subunit involved in RNA degradation [9798] However recent studies demonstrated that the S solfa-taricus DnaG homolog has limited primer synthesis activityand a dual primase system with PriSL has been proposed tofunction during DNA replication [99] Hu et al hypothesizedan interesting theory which suggests that LUCA employed adual-primase system comprisingDnaG and PriSL which alsoserved roles in RNA degradation and the nonhomologousend joining (NHEJ) pathwayThe system was inherited by allthree domains In theArchaea domain it retained its originalfunctions However in the Bacteria domain DnaG becamethe major replicative primase and PriSL evolved into the Poldomain of LigD involved in the NHEJ pathway In contrastDnaG was lost in the Eukaryota domain and PriSL becamethe only replicative primase In addition it also evolved intothe DNA Pol X family involved in NHEJ [96]

Like other ArchaeaM maripaludis S2 possesses both theeukaryotic- and bacterial-like primases A new genome-widesurvey of this methanoarchaea revealed that genes encodingboth subunits of the eukaryotic like primase PriS and PriL(MMP0009 and MMP0071) were likely to be essential forgrowth which is consistent with a role in replication Similarobservations have been demonstrated in other Archaea suchas Halobacterium sp NRC-1and Haloferax volcanii [93 100]In contrast the DnaG primase (MMP1286) was nonessentialwhich would be consistent with a role in the exosome [62]These results suggest that in M maripaludis and probablyother euryarchaeotes a dual primase system is not pre-sent

33 Elongation (Replicative DNA Polymerase) The primersynthesized by the primase is further extended by a replicativeDNA polymerase DNA polymerases have been classifiedinto seven families based on their amino acid sequencesimilarity (A B C D E X and Y) [101ndash105] In Bacteria Ecoli possesses five DNA polymerases Pol IndashV where the firstthree belong to families A B and C respectively and the lasttwo belong to the Y family The major replicative DNA poly-merase in E coli is Pol III a member of the C family whichsynthesizes DNA with high processivity when functioningwithin the holoenzyme [106] In eukaryotes a great diversityof DNA polymerases is also found but DNA replicationrequires three replicative DNA polymerases which belongto family B (Pol120572 Pol120575 and Pol120576) [107] In Archaea fewertypes of DNA polymerases are present but they have aninteresting evolutionary division Representatives of theDNApolymerase B family are found in all Archaea The D familyDNA polymerase is present in every phyla studied so farwith the exception of the Crenarchaeota (Figure 1) Lastly amember of theY family has been identified andbiochemically

characterized in S solfataricus [108] and the Methanosarci-nales in which several species harbor two homologs [109]Even though the activity of DNA polymerases belongingto the Y family in archaea is not fully understood they aresuggested to play an important role in DNA repair [109]

Representatives of the DNA polymerase family B havebeen identified in all Archaea The crenarchaeotes possess atleast two family B DNA polymerases (PolB I and PolB IIand in some cases PolB III) [102 110 111] The recombinantS solfataricus Pyrodictium occultum and A pernix enzymeshave been characterized [102] In contrast euryarchaeotesonly contain PolB I The recombinant P furiosus enzymehas been characterized [112] The PolB I enzymes havesimilar amino acid sequence and overall structure and theypossess a potent 31015840-51015840exonuclease proofreading activity [102]A unique property of the archaeal family B DNA polymeraseis the ability to stall DNA polymerization in the presenceof uracil or hypoxanthine deaminated bases [113 114] thisproperty helps to prevent the copy of template-strand uraciland the transmission of fixed mutations to progeny [115]Commonly cytosine deamination converts GC base pairsinto the promutagenic GU mismatches which result in50 of the offspring containing an AT transition mutationafter replication [116] In addition when A-U base pairs areformed the loss of the 5-methyl moiety upon replacementof thymine can exert a detrimental effect on protein DNAinteractions Interestingly in some crenarchaeotes and eur-yarchaeotes one of the B family DNA polymerase paralogspossesses disrupted versions of the sequence motifs thatare essential for catalysis Possibly these enzymes possess astructural role [117]

DNA polymerase family D (PolD) is a novel enzyme thatwas originally discovered in P furiosus [118] It has sincethen been identified in all euryarchaeotes [119] For a longtime this enzyme was considered a euryarchaeote-specificpolymerase but the three newly discovered archaeal phylawere also found to possess genes for PolD [14ndash16] PolD isa heterodimer with a small subunit (DP1) and a large subunit(DP2) It has been proposed that the large subunit harborsthe polymerase activity although its sequence is very differentfrom other hitherto described DNA polymerases The smallsubunit possesses high similarity with the noncatalytic B-subunits of the eukaryoticDNApolymerases120572 120575 and 120576 [120]Studies of the M jannaschii enzyme demonstrated that thesmall subunit possesses a strong 31015840-51015840exonuclease activitysuggesting that it may be involved in proofreading activity[7 121] Efficient polymerase and proofreading activity havealso been detected from a purified PolD of P furiosus andthe residues Asp-1122 and Asp-1124 are essential for thepolymerization reaction in P horikoshii [122 123] Everyeuryarchaeote examined possessed one homolog for DP1 andDP2 except forMethanococcoides burtoniiDSM 6242 whichpossesses two homologs for DP1 (Figure 1)

Because the crenarchaeotes only possess family B DNApolymerases one of themmust be the replicative polymeraseHowever in euryarchaeotes it was not clear which enzymewas involved in replication Studies in Halobacterium spNRC-1 showed that both PolB and PolD were essential forviability and it was proposed that they could be working

Archaea 7

together at the replication fork synthesizing the leading andlagging strand respectively [100 124] However in otherEuryarchaeota PolB does not appear to be essential Forinstance a recent report demonstrated that both subunits ofPolDwere essential but PolB was nonessential for the growthof M maripaludis S2 [62] Likewise in T kodakaraensisPolD can be coisolated with different proteins of the archaealreplication fork but PolB wasmainly coisolated with proteinsof unknown function [71] A deletion of the PolB in Tkodakaraensis also had no detectable effect on cell viability[125] Interestingly T kodakaraensis PolB mutants haveincreased sensitivity to UV radiation These results togethersuggest that PolD is the essential replicative DNA polymerasein these euryarchaeotes and not a PolB family polymeraseIn this scenario PolB may have some other crucial functionin Halobacterium and possibly other closely related specieswhich it is not conserved throughout the phylum Finallyit has been demonstrated that purified PolD from P abyssiis able to perform strand displacement and RNA primerextension in vitro Purified PolB on its own cannot performthese activities in vitro but in the presence of PCNA stranddisplacement activity is stimulated [124 126] A recent in vitrostudy in P abyssi demonstrated that RNase HII is required toinitiate strand displacement DNA synthesis by PolB [127]

34 Elongation (Other Accessory Proteins) Purified DNApolymerases possess low processivity however the addi-tion of an accessory factor the sliding clamp gives DNApolymerases the required processivity to replicate genomesThis factor whose structure resembles a doughnut functionsas a molecular platform which recruits several replication-associated enzymes and act together with DNA and thepolymerase to stabilize their interactions during replication[128] The structure of sliding clamps is conserved in thethree domains of life In Bacteria the sliding clamp or 120573-subunit is a homodimeric ring [129] In eukaryotes thesliding clamp or proliferating cell nuclear antigen (PCNA)is a homotrimeric ring [128] In Archaea the majority ofcrenarchaeotes have multiple PCNA homologs which formheterotrimeric rings [130 131] (Figure 1) In contrast mosteuryarchaeotes possess a single PCNA homolog (Figure 1)Interactions of DNA polymerase with the sliding clampare mediated through a common motif called the PCNAInteracting Protein (PIP) box [132] The three dimensionalstructures of PCNA-PolB and the PolB-PCNA-DNA complexfrom P furiosus have been solved shedding light on theinteractions between these molecules [133 134] In additiona study demonstrated that the PolDPCNA and PolBPCNAinteractions require two and one PIP boxes respectively[135] Recently through a protein-interaction network of Pabyssi a previously unknown protein with nuclease activity(Pab0431) and a PIP canonical motif was discovered tointeract with PCNA suggesting a possible involvement inDNA replication [136] T kodakaraensis is the only well-documented example of an euryarchaeotewith twohomologsfor PCNA TK0535 (PCNA1) and TK0582 (PCNA2) Recentwork demonstrated both proteins form stable homotrimericrings that interact with T kodakaraensis PolB in vitro [137]A more detailed study of the two homologs of PCNA in T

kodakaraensis demonstrated that both homologs stimulate invitro the primer extension activity of PolB but only PCNA1and not PCNA2 stimulates the same activity of PolD [138]Also the same report showed that the pcna2 gene can bedisrupted without causing growth deficiencies but it was notpossible to isolate mutants of pcna1 These results suggestthat PCNA1 but not PCNA2 is essential for DNA replication[138] It has been proposed that one of the PCNA geneswas acquired by lateral gene transfer [139] Members of theorderMethanococcales possess one PCNA homolog with twoexceptionsMmaripaludis S2 possesses twoPCNAhomologs(MMP1126 and 1711) [60] Both genes appeared to be essentialfor growth suggesting that they both play an importantrole in replication [62] The gene MMP1711 possesses highsimilarity to both T kodakaraensis genes and is likely thetrue methanococcal PCNA In contrast MMP1126 possessesonly low similarity to the T kodakaraensis genes and alsocontains an S-adenosylmethionine-dependent methyltrans-ferases domain Thus it is likely to possess some alternativefunction Methanotorris igneus Kol 5 also possesses twoPCNA homologs

For PCNA to assemble around DNA a specific loadingfactor is required In Bacteria the loading factor is knownas 120574-complex and comprises three different subunits ina 1205743-120575-1205751015840 stoichiometry [140] In eukaryotes the loading

factor is known as Replication Factor C (RFC) and is aheteropentameric complex comprising one large subunit andfour different small subunits [141] In contrast inArchaea theRFC consists of two different proteins a small subunit RFCSand a large subunit RFCLThey also form a heteropentamericcomplex in a 4 1 ratio (RFCS RFCL) Interestingly manycrenarchaeotes possess one homolog of RFCL and two orthree homologs of RFCS Alternatively most euryarchaeotespossess only one RFCL and RFCS homolog The exceptionsare somemembers of the ordersHalobacteriales Methanomi-crobiales and Methanosarcinales which possess two RFCShomologs (Figure 1) Structural and biochemical studies ofRFC have been conducted in several euryarchaeotes such asArchaeoglobus fulgidus and Pyrococcus species [142ndash144] Aninteresting case is observed in Methanosarcina acetivoransThis RFC possesses three subunits (RFC1 2 L) found ina ratio 3 1 1 [145] Homologs for these three subunits arealso present in most of the genomes of the haloarchaea[145] It is inferred that this type of RFC complex representsan intermediary form transitional between the canonicalarchaeal RFC complex of one small and one large subunit andthe eukaryotic RFC complex of four different small and onelarge subunit [146] The organization and spatial distributionexhibit a similarity to the E coliminimal 120574-complex but thefunction of the subunits is probably not conserved [145]

35 Maturation During DNA replication the lagging strandis discontinuously synthesized by extending the RNAprimersor Okazaki fragments This discontinuously synthesizedDNA strand requires maturation to form a single covalentlyclosed strand to end the replication process In ArchaeaOkazaki fragments were first demonstrated during replica-tion in P abyssi and Sulfolobus acidocaldarius [147] Duringreplication these RNA primers are replaced with DNA The

8 Archaea

removal of the primers is performed by the enzyme RNase Hwhich is ubiquitous in the three domains of life Accordingto their sequence similarity in prokaryotes the RNase Hproteins are classified into three groups RNase HI HII andHIII In eukaryotes they are classified as RNase H1 and H2[148] However phylogenetic analyses suggest that the RNaseH proteins can also be classified into two different groupsType 1 (prokaryotic RNaseHI eukaryotic RNaseH1 and viralRNase H) and Type 2 (prokaryotic RNase HII and HIII andeukaryotic RNase H2) [149] These two types of RNase Hpossess different specific activities metal ion preferences andcleavage sites [150] Originally it was thought that Archaeaonly possess type 2 RNase H [149] but several type 1 archaealRNase H enzymes have since then been discovered [151 152]Interestingly in eukaryotes RNaseH1 andH2 tend to coexistand different combinations of the three prokaryotic RNasesH(I II and III) are found except for the combination of RNasesHI and HIII This mutually exclusive evolution of some ofthe prokaryotic RNases seems to be related to functionalredundancy [148]

Another enzyme involved in primer replacement inDNA replication is the Flap endonuclease I (FEN-1) whichrecognizes double-strandedDNAwith an unannealed 51015840-flapand cleaves it A eukaryotic homolog of FEN-1 is found inevery archaeal member analyzed and one member of theThermoproteales Thermofilum pendens Hrk5 possesses twohomologs

M maripaludis S2 possesses genes for the prokaryoticRNase HI and HII and for FEN-1 but none are essentialsuggesting that they may be redundant in their functions[44 62] Possibly both RNase H proteins persist and areevolutionary stable in the genome The gene products mayperform the same function but one is less efficient than theother [153]

After the Okazaki fragments are replaced by DNA inthe lagging strand the nick between the newly synthesizedand the elongated DNA is repaired by a DNA ligase Thisenzyme uses a nucleotide cofactor to catalyze the formationof the phosphodiester bond in three well-characterized steps[154]The enzyme is common to all three domains but can begrouped into two families based on cofactor specificity (ATPor NAD+) The DNA ligases from several crenarchaeotes andeuryarchaeotes have been further characterized (reviewedin [43]) Many archaeal DNA ligases possess dual cofactorspecificity (ATPNAD+ or ATPADP) but every archaealDNA ligase characterized so far uses ATP A thermophilicDNA ligase from M thermautotrophicus which uses ATP assole cofactor was characterized in vitro [155] A characterizedDNA ligase from the crenarchaeote Sulfophobococcus zilligiidisplayed specificity for three cofactors (ATPNAD+GTP)[156]Major structuralwork in this enzymehas been achievedin P furiosus and S solfataricus and the findings have beenreviewed in detail [43] InM maripaludis S2 the DNA ligaseis likely to be essential for growth [44 62]

Understanding the maturation process in archaea hasbecome a focus of increasing research in recent years An invitro study reconstituted the Okazaki fragment maturationusing proteins derived from the crenarchaeote S solfataricusThey demonstrated that only six proteins are necessary for

coupled DNA synthesis RNA primer removal and DNAligation In this model a single PCNA (heterotrimeric ring)coordinates the activities of PolBI FEN-1 and DNA ligaseinto an efficient maturation complex [157] A different invitro study in P abyssi has demonstrated two different modelsfor Okazaki fragments maturation which differ in the RNAprimer removal process In the first model RNA primerelimination is executed by continuous PolD strand displace-ment DNA synthesis and 51015840RNA flap cleavage by FEN-1The resulting nicks are closed by DNA ligase Alternativelythe second model proposes that RNase HII cleaves theRNA primer followed by the action of FEN-1 and stranddisplacement DNA synthesis by polB or polD The nick isthen sealed by DNA ligase [127] Testing these models invivo is of great interest to complete the picture of how theseprocesses behave in the cell In addition other factors that canmodulate these processesmay be required for coordination ofthe in vivomaturation process

4 Conclusions

DNA replication in archaea possesses a dual nature wherethe machinery is structurally and functionally similar to theeukaryotic replication system but it is executed within abacterial context [11 25] Additionally unique archaeal fea-tures demonstrate the complexity of this process and it doesnot appear to be just a simplified version of the eukary-otic system For example the archaeal specific DNA poly-merase D is conserved across the Archaea domain with theexception of the Crenarchaeota phylumThe recent discoverythat it is the essential replicative polymerase in two differenteuryarchaeotic species demonstrates an unanticipated vari-ability in archaeal DNA replication and a fundamental differ-ence in the replication mechanism between crenarchaeotesand euryarchaeotes Interestingly the absence of PolD increnarchaeotes is not the only difference in DNA repli-cation These differences include the absence of histonesin crenarchaeotes [4] the presence of multiple origins ofreplication in crenarchaeotes and a single origin of repli-cation in most euryarchaeotes the absence of GINS23 inmost euryarchaeotes the absence of RPA protein in manycrenarchaeotes the presence of multiple MCM homologs inMethanococcales and the presence of one homolog of PCNAin euryarchaeotes compared to the multiple homologs increnarchaeotes These distinctive characteristics between thephyla highlight the complexity of archaeal DNA replicationand suggest a complex evolutionary history (Table 1)

Among the Euryarchaeota the ordersHalobacteriales andMethanococcales possess differences in the DNA replicationsystem that make them unique For instance Halobac-teriales possess many more origin recognition proteins(Orc1Cdc6) compared to the rest of the archaea On theother hand Methanococcales and Methanopyrales lack rec-ognizable homologs for the Orc1Cdc6 proteins suggestingthe presence of a very different mechanism for initiation ofreplication In addition the Methanococcales possess a largenumber of MCM protein homologs It has been proposedthat these distinctive features are connected and because ofthe absence of the Orc1Cdc6 proteins MCM proteins may

Archaea 9

Table1DNAreplicationproteins

andfeatures

inthed

omains

BacteriaEukaryotaand

thetwomajor

phylao

fthe

Archaeado

main

Mod

ified

from

[43]

DNAreplicationstage

Process

Bacteria

Eukaryota

Archaea

Crenarchaeota

Euryarchaeota

Preinitia

tion

Orig

inof

replication

Sing

leMultip

leMultip

leSing

lea

Orig

inrecogn

ition

DnaA

ORC

complex

(ORC

1-6)

Orc1C

dc6

Orc1C

dc6b

Initiation

DNAun

winding

(Helicase)

DnaB

MCM

complex

(MCM

2-7)

MCM

complex

MCM

complex

DNAun

winding

(Accessory

proteins)

DnaC

Cdc6

GIN

S23GIN

S15

GIN

S15c

Cdt1

GIN

Scomplex

(Sld5Psf1-3)

RecJho

molog

RecJho

molog

Cdc45

Prim

ersynthesis

DnaG

Pol120572

prim

asec

omplex

DNAprim

ase

(PriS

L)D

naG

dDNAprim

ase(PriSL)

Elon

gatio

n

DNAsynthesis

(polym

erase)

PolIII(Fam

ilyCDNApo

lymerase)

Pol120575and

Pol120576(Fam

ilyBDNA

polymerase)

Family

BDNApo

lymerase

Family

DDNA

polymerasee

DNAsynthesis

(Processivity

factors)

120574-com

plex

(clamploader)

RFC(clamploader)

RFC(clamploader)

RFC(clamploader)

120573-clamp(clamp)

PCNA(clamp)

PCNA(clamp)

PCNA(clamp)

Maturation

Maturation(O

kazaki

fragmentp

rocessing)

PolI

(family

ADNApo

lymerase)

Fen1D

na2

Fen1

Fen1

RNaseH

RNaseH

RNaseH

RNaseH

DNAligase

DNAligase

DNAligase

DNAligase

a Exceptio

ntheo

rder

Halobacteria

les

b Not

know

nform

embersof

theE

uryarchaeota

ordersMethanococcalesandMethanopyrales

c GIN

S23hasb

eenfoun

dedon

lyin

theo

rder

Thermococcales

oftheE

uryarchaeota

d Sulfolobu

ssolfataric

usdidshow

prim

asea

ctivity

invitro

e Fam

ilyBDNApo

lymeraseisa

lsoessentialinHalobacteriu

mB

ecause

itsfunctio

nhasn

otbeen

clearlyelu

cidateditmight

also

play

aroleinreplicationin

thisandclo

selyrelated

organism

s

10 Archaea

interact with other unknown initiation enzymes resultingin a complex phylogeny of the MCM homologs [49] Pre-sumably these differences also account for the inability torecognize the origin of replication in these microorganismsThis unique scenario for initiation of DNA replicationmay bea direct consequence of various processes such as duplicationmobile genetic elements and interactions with viruses [58]

The differences in DNA replication among archaealhigher taxa demonstrate an unexpected variability and sug-gest two alternative evolutionary models In the first modelDNA replication evolved late after the diversification ofthe archaeal lineages Because the replicative system wasnot fully formed it was possible to develop differentlybetween the lineages Once formed replication would thenbe highly conserved However this model is not consistentwith differences observed between lineages that must haveformed relatively late such as those between the orders oreven in some cases within certain orders The alternativemodel is that DNA replication has changed throughout theevolution of the archaea Thus differences in the replicativesystems may represent ancient as well as modern adaptationsto changing environments In this case differences in thereplicative systems may provide important insights into theevolutionary pressures in play during different episodes ofarchaeal evolution From this perspective the differencesbetween the eukaryotic and archaeal replicative systems maynot be evidence for an ancient origin of the eukaryotesInstead it is entirely plausible that the replicative system ineukaryotes could have evolved relatively late from a well-developed archaeal system

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] E F DeLong and N R Pace ldquoEnvironmental diversity ofbacteria and archaeardquo Systematic Biology vol 50 no 4 pp 470ndash478 2001

[2] B Chaban S Y M Ng and K F Jarrell ldquoArchaeal habitatsmdashfrom the extreme to the ordinaryrdquo Canadian Journal of Micro-biology vol 52 no 2 pp 73ndash116 2006

[3] M J Hanford and T L Peeples ldquoArchaeal tetraether lipidsunique structures and applicationsrdquo Applied Biochemistry andBiotechnology A vol 97 no 1 pp 45ndash62 2002

[4] K Sandman and J N Reeve ldquoArchaeal histones and the originof the histone foldrdquo Current Opinion in Microbiology vol 9 no5 pp 520ndash525 2006

[5] O Lecompte R Ripp J-C Thierry D Moras and O PochldquoComparative analysis of ribosomal proteins in complete gen-omes an example of reductive evolution at the domain scalerdquoNucleic Acids Research vol 30 no 24 pp 5382ndash5390 2002

[6] D R Edgell and W F Doolittle ldquoArchaea and the origin(s) ofDNA rplication poteinsrdquo Cell vol 89 no 7 pp 995ndash998 1997

[7] E R Barry and S D Bell ldquoDNA replication in the archaeardquoMicrobiology and Molecular Biology Reviews vol 70 no 4 pp876ndash887 2006

[8] S Gribaldo and C Brochier-Armanet ldquoThe origin and evolu-tion of archaea a state of the artrdquo Philosophical Transactions ofthe Royal Society B vol 361 no 1470 pp 1007ndash1022 2006

[9] P Londei ldquoEvolution of translational initiation new insightsfrom the archaeardquo FEMS Microbiology Reviews vol 29 no 2pp 185ndash200 2005

[10] B Grabowski and Z Kelman ldquoArchaeal DNA replicationeukaryal proteins in a bacterial contextrdquo Annual Review ofMicrobiology vol 57 pp 487ndash516 2003

[11] P Forterre J Filee and H Myllykallio ldquoOrigin and evolutionof DNA and DNA replication machineriesrdquo in The GeneticCode and the Origin of Life L Ribas Ed Landes BioscienceGeorgetown Tex USA 2007

[12] E V Koonin ldquoThe origin and early evolution of eukaryotesin the light of phylogenomicsrdquo Genome Biology vol 11 no 5article 209 2010

[13] M Konneke A E Bernhard J R de la Torre C B WalkerJ B Waterbury and D A Stahl ldquoIsolation of an autotrophicammonia-oxidizing marine archaeonrdquo Nature vol 437 no7058 pp 543ndash546 2005

[14] C Brochier-Armanet B Boussau S Gribaldo and P ForterreldquoMesophilic crenarchaeota proposal for a third archaeal phy-lum theThaumarchaeotardquoNature Reviews Microbiology vol 6no 3 pp 245ndash252 2008

[15] J G Elkins M Podar D E Graham et al ldquoA korarchaealgenome reveals insights into the evolution of the ArchaeardquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 105 no 23 pp 8102ndash8107 2008

[16] T Nunoura Y Takaki J Kakuta et al ldquoInsights into theevolution of Archaea and eukaryotic protein modifier systemsrevealed by the genome of a novel archaeal grouprdquoNucleic AcidsResearch vol 39 no 8 pp 3204ndash3223 2011

[17] HHuberM J Hohn R Rachel T Fuchs V CWimmer andKO Stetter ldquoAnewphylumofArchaea represented by a nanosizedhyperthermophilic symbiontrdquoNature vol 417 no 6884 pp 63ndash67 2002

[18] C Brochier S Gribaldo Y Zivanovic F Confalonieri and PForterre ldquoNanoarchaea representatives of a novel archaeal phy-lum or a fast-evolving euryarchaeal lineage related to Therm-ococcalesrdquo Genome Biology vol 6 no 5 article R42 2005

[19] S J Aves ldquoDNA replication initiationrdquo Methods in MolecularBiology vol 521 pp 3ndash17 2009

[20] N P Robinson I Dionne M Lundgren V L Marsh RBernander and S D Bell ldquoIdentification of two origins ofreplication in the single chromosome of the archaeon Sulfolobussolfataricusrdquo Cell vol 116 no 1 pp 25ndash38 2004

[21] M Lundgren A Andersson L Chen P Nilsson and RBernander ldquoThree replication origins in Sulfolobus speciessynchronous initiation of chromosome replication and asyn-chronous terminationrdquo Proceedings of the National Academy ofSciences of theUnited States of America vol 101 no 18 pp 7046ndash7051 2004

[22] N P Robinson and S D Bell ldquoExtrachromosomal element cap-ture and the evolution ofmultiple replication origins in archaealchromosomesrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 104 no 14 pp 5806ndash58112007

[23] E A Pelve A C Lindas A Knoppel A Mira and R Bernan-der ldquoFour chromosome replication origins in the archaeonPyrobaculum calidifontisrdquo Molecular Microbiology vol 85 no5 pp 986ndash995 2012

Archaea 11

[24] A F Andersson E A Pelve S LindebergM Lundgren P Nils-son and R Bernander ldquoReplication-biased genome organisa-tion in the crenarchaeon Sulfolobusrdquo BMCGenomics vol 11 no1 article 454 2010

[25] H Myllykallio P Lopez P Lopez-Garcıa et al ldquoBacterial modeof replication with eukaryotic-like machinery in a hyperther-mophilic archaeonrdquo Science vol 288 no 5474 pp 2212ndash22152000

[26] F Matsunaga P Forterre Y Ishino and H Myllykallio ldquoInvivo interactions of archaeal Cdc6Orc1 and minichromosomemaintenance proteins with the replication originrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 98 no 20 pp 11152ndash11157 2001

[27] S Maisnier-Patin L Malandrin N K Birkeland and RBernander ldquoChromosome replication patterns in the hyper-thermophilic euryarchaeaArchaeoglobus fulgidus andMethano-caldococcus (Methanococcus) jannaschiirdquo Molecular Microbiol-ogy vol 45 no 5 pp 1443ndash1450 2002

[28] R Zhang and C-T Zhang ldquoMultiple replication origins ofthe archaeon Halobacterium species NRC-1rdquo Biochemical andBiophysical Research Communications vol 302 no 4 pp 728ndash734 2003

[29] C Norais M Hawkins A L Hartman J A Eisen H Myl-lykallio and T Allers ldquoGenetic and physical mapping of DNAreplication origins in Haloferax volcaniirdquo PLoS Genetics vol 3no 5 article e77 2007

[30] J A Coker P DasSarma M Capes et al ldquoMultiple replicationorigins of Halobacterium sp strain NRC-1 properties of theconserved orc7-dependent oriC1rdquo Journal of Bacteriology vol191 no 16 pp 5253ndash5261 2009

[31] Z Wu J Liu H Yang H Liu and H Xiang ldquoMultiple repli-cation origins with diverse control mechanisms in Haloarculahispanicardquo Nucleic Acids Research 2013

[32] M Hawkins S Malla M J Blythe C A Nieduszynski and TAllers ldquoAccelerated growth in the absence of DNA replicationoriginsrdquo Nature vol 503 no 7477 pp 544ndash547 2013

[33] A I Majernık and J P J Chong ldquoA conserved mechanismfor replication origin recognition and binding in archaeardquo TheBiochemical Journal vol 409 no 2 pp 511ndash518 2008

[34] J E Galagan C Nusbaum A Roy et al ldquoThe genome of Macetivorans reveals extensive metabolic and physiological diver-sityrdquo Genome Research vol 12 no 4 pp 532ndash542 2002

[35] R Zhang and C-T Zhang ldquoIdentification of replication originsin archaeal genomes based on the Z-curve methodrdquo Archaeavol 1 no 5 pp 335ndash346 2005

[36] A Spang R Hatzenpichler C Brochier-Armanet et al ldquoDis-tinct gene set in two different lineages of ammonia-oxidizingarchaea supports the phylum Thaumarchaeotardquo Trends inMicrobiology vol 18 no 8 pp 331ndash340 2010

[37] K J Marians ldquoProkaryotic DNA replicationrdquo Annual Review ofBiochemistry vol 61 pp 673ndash719 1992

[38] S P Bell ldquoThe origin recognition complex from simple originsto complex functionsrdquo Genes and Development vol 16 no 6pp 659ndash672 2002

[39] V L Marsh and S D Bell ldquoDNA replication and the cell cyclerdquoin Archaea Evolution Physiology and Molecular Biology R AGarrett and H P Klenk Eds Blackwell Publishing HobokenNJ USA 2007

[40] F Matsunaga A Glatigny M-H Mucchielli-Giorgi et alldquoGenomewide and biochemical analyses of DNA-binding activ-ity of Cdc6Orc1 and Mcm proteins in Pyrococcus sprdquo NucleicAcids Research vol 35 no 10 pp 3214ndash3222 2007

[41] J Liu C L Smith D DeRyckere K DeAngelis G S Martinand J M Berger ldquoStructure and function of Cdc6Cdc18implications for origin recognition and checkpoint controlrdquoMolecular Cell vol 6 no 3 pp 637ndash648 2000

[42] M R Singleton R Morales I Grainge N Cook M NIsupov and D B Wigley ldquoConformational changes inducedby nucleotide binding in Cdc6ORC from Aeropyrum pernixrdquoJournal of Molecular Biology vol 343 no 3 pp 547ndash557 2004

[43] Y Ishino and S Ishino ldquoRapid progress of DNA replicationstudies in Archaea the third domain of liferdquo Science China LifeSciences vol 55 no 5 pp 386ndash403 2012

[44] E L Hendrickson R Kaul Y Zhou et al ldquoComplete genomesequence of the genetically tractable hydrogenotrophic meth-anogen Methanococcus maripaludisrdquo Journal of Bacteriologyvol 186 no 20 pp 6956ndash6969 2004

[45] B K Tye ldquoMCM proteins in DNA replicationrdquo Annual Reviewof Biochemistry vol 68 pp 649ndash686 1999

[46] K Labib and J F X Diffley ldquoIs the MCM2-7 complex theeukaryotic DNA replication fork helicaserdquo Current Opinion inGenetics amp Development vol 11 no 1 pp 64ndash70 2001

[47] I Ilves T Petojevic J J Pesavento and M R Botchan ldquoActi-vation of the MCM2-7 helicase by association with Cdc45 andGINS proteinsrdquoMolecular Cell vol 37 no 2 pp 247ndash258 2010

[48] M L Bochman andA Schwacha ldquoTheMcm complex unwind-ing the mechanism of a replicative helicaserdquo Microbiology andMolecular Biology Reviews vol 73 no 4 pp 652ndash683 2009

[49] Y Ishimi ldquoADNAhelicase activity is associated with anMCM4-6 and -7 protein complexrdquoThe Journal of Biological Chemistryvol 272 no 39 pp 24508ndash24513 1997

[50] Z Kelman and M F White ldquoArchaeal DNA replication andrepairrdquo Current Opinion in Microbiology vol 8 no 6 pp 669ndash676 2005

[51] J H LeBowitz and R McMacken ldquoThe Escherichia coli dnaBreplication protein is a DNA helicaserdquoThe Journal of BiologicalChemistry vol 261 no 10 pp 4738ndash4748 1986

[52] Z Kelman J-K Lee and J Hurwitz ldquoThe single minichro-mosome maintenance protein ofMethanobacterium thermoau-totrophicum ΔH contains DNA helicase activityrdquo Proceedings ofthe National Academy of Sciences of the United States of Americavol 96 no 26 pp 14783ndash14788 1999

[53] D F Shechter C Y Ying and J Gautier ldquoThe intrinsic DNAhelicase activity of Methanobacterium thermoautotrophicumΔH minichromosome maintenance proteinrdquo The Journal ofBiological Chemistry vol 275 no 20 pp 15049ndash15059 2000

[54] M de Felice L Esposito B Pucci M de Falco M Rossi andF M Pisani ldquoA CDC6-like factor from the archaea Sulfolobussolfataricus promotes binding of the mini-chromosome main-tenance complex to DNArdquoThe Journal of Biological Chemistryvol 279 no 41 pp 43008ndash43012 2004

[55] R Kasiviswanathan J-H Shin and Z Kelman ldquoInteractionsbetween the archaeal Cdc6 and MCM proteins modulate theirbiochemical propertiesrdquo Nucleic Acids Research vol 33 no 15pp 4940ndash4950 2005

[56] J-H Shin B Grabowski R Kasiviswanathan S D Bell andZ Kelman ldquoRegulation of minichromosomemaintenance heli-case activity by Cdc6rdquo The Journal of Biological Chemistry vol278 no 39 pp 38059ndash38067 2003

[57] M Akita A Adachi K Takemura T Yamagami F Matsunagaand Y Ishino ldquoCdc6Orc1 from Pyrococcus furiosus may actas the origin recognition protein and Mcm helicase recruiterrdquoGenes to Cells vol 15 no 5 pp 537ndash552 2010

12 Archaea

[58] M Krupovic S Gribaldo D H Bamford and P Forterre ldquoTheevolutionary history of archaeal MCM helicases a case study ofvertical evolution combined with hitchhiking of mobile geneticelementsrdquo Molecular Biology and Evolution vol 27 no 12 pp2716ndash2732 2010

[59] ADWalters and J P J Chong ldquoAn archaeal orderwithmultipleminichromosome maintenance genesrdquo Microbiology vol 156part 5 pp 1405ndash1414 2010

[60] A DWalters and J P J Chong ldquoMethanococcusmaripaludis anarchaeon with multiple functional MCM proteinsrdquo Biochemi-cal Society Transactions vol 37 no 1 pp 1ndash6 2009

[61] Q Xia E L Hendrickson Y Zhang et al ldquoQuantitative pro-teomics of the archaeon Methanococcus maripaludis validatedbymicroarray analysis and real time PCRrdquoMolecularampCellularProteomics vol 5 no 5 pp 868ndash881 2006

[62] F Sarmiento J Mrazek and W B Whitman ldquoGenome-scaleanalysis of gene function in the hydrogenotrophic methano-genic archaeon Methanococcus maripaludisrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 110 no 12 pp 4726ndash4731 2013

[63] M Pan T J Santangelo Z Li J N Reeve and Z KelmanldquoThermococcus kodakarensis encodes threeMCMhomologs butonly one is essentialrdquo Nucleic Acids Research vol 39 no 22 pp9671ndash9680 2011

[64] S Ishino S Fujino H Tomita et al ldquoBiochemical and geneticalanalyses of the three mcm genes from the hyperthermophilicarchaeon Thermococcus kodakarensisrdquo Genes to Cells vol 16no 12 pp 1176ndash1189 2011

[65] K S Makarova Y I Wolf S L Mekhedov B G Mirkin and EV Koonin ldquoAncestral paralogs and pseudoparalogs and theirrole in the emergence of the eukaryotic cellrdquo Nucleic AcidsResearch vol 33 no 14 pp 4626ndash4638 2005

[66] N Marinsek E R Barry K S Makarova I Dionne E VKoonin and S D Bell ldquoGINS a central nexus in the archaealDNA replication forkrdquo EMBOReports vol 7 no 5 pp 539ndash5452006

[67] T Yoshimochi R Fujikane M Kawanami F Matsunaga and YIshino ldquoTheGINS complex from Pyrococcus furiosus stimulatesthe MCM helicase activityrdquoThe Journal of Biological Chemistryvol 283 no 3 pp 1601ndash1609 2008

[68] T Oyama S Ishino S Fujino et al ldquoArchitectures of archaealGINS complexes essential DNA replication initiation factorsrdquoBMC Biology vol 9 article 28 2011

[69] H Ogino S Ishino K Mayanagi et al ldquoThe GINS com-plex from the thermophilic archaeon Thermoplasma aci-dophilummay function as a homotetramer inDNA replicationrdquoExtremophiles vol 15 no 4 pp 529ndash539 2011

[70] L Sanchez-Pulido and C P Ponting ldquoCdc45 the missing recjortholog in eukaryotesrdquoBioinformatics vol 27 no 14 pp 1885ndash1888 2011

[71] Z Li T J Santangelo L Cubonova J N Reeve and Z KelmanldquoAffinity purification of an archaeal DNA replication proteinnetworkrdquomBio vol 1 no 5 2010

[72] Z Li M Pan T J Santangelo et al ldquoA novel DNA nucleaseis stimulated by association with the GINS complexrdquo NucleicAcids Research vol 39 no 14 pp 6114ndash6123 2011

[73] L A Rajman and S T Lovett ldquoA thermostable single-strandDNase from Methanococcus jannaschii related to the RecJrecombination and repair exonuclease from Escherichia colirdquoJournal of Bacteriology vol 182 no 3 pp 607ndash612 2000

[74] K RWilliams J B Murphy and JW Chase ldquoCharacterizationof the structural and functional defect in the Escherichia colisingle-stranded DNA binding protein encoded by the ssb-1 mutant gene Expression of the ssb-1 gene under 120582p(L)regulationrdquoThe Journal of Biological Chemistry vol 259 no 19pp 11804ndash11811 1984

[75] S Dąbrowski M Olszewski R Pitek and J Kur ldquoNovel ther-mostable ssDNA-binding proteins fromThermus thermophilusand T aquaticus-expression and purificationrdquo Protein Expres-sion and Purification vol 26 no 1 pp 131ndash138 2002

[76] C Iftode Y Daniely and J A Borowiec ldquoReplication proteinA (RPA) the eukaryotic SSBrdquo Critical Reviews in Biochemistryand Molecular Biology vol 34 no 3 pp 141ndash180 1999

[77] A G Murzin ldquoOB(oligonucleotideoligosaccharide binding)-fold common structural and functional solution for non-hom-ologous sequencesrdquo The EMBO Journal vol 12 no 3 pp 861ndash867 1993

[78] C A Haseltine and S C Kowalczykowski ldquoA distinctive single-stranded DNA-binding protein from the Archaeon Sulfolobussolfataricusrdquo Molecular Microbiology vol 43 no 6 pp 1505ndash1515 2002

[79] R I M Wadsworth and M F White ldquoIdentification and pro-perties of the crenarchaeal single-stranded DNA binding pro-tein from Sulfolobus solfataricusrdquoNucleic Acids Research vol 29no 4 pp 914ndash920 2001

[80] I D Kerr R I M Wadsworth L Cubeddu W Blankenfeldt JHNaismith andM FWhite ldquoInsights into ssDNA recognitionby the OB fold from a structural and thermodynamic study ofSulfolobus SSB proteinrdquo The EMBO Journal vol 22 no 11 pp2561ndash2570 2003

[81] X Luo U Schwarz-Linek C H Botting R Hensel B Siebersand M F White ldquoCC1 a novel crenarchaeal DNA binding pro-teinrdquo Journal of Bacteriology vol 189 no 2 pp 403ndash409 2007

[82] T J Kelly P Simancek and G S Brush ldquoIdentification andcharacterization of a single-stranded DNA-binding proteinfrom the archaeonMethanococcus jannaschiirdquoProceedings of theNational Academy of Sciences of theUnited States of America vol95 no 25 pp 14634ndash14639 1998

[83] Z Kelman S Pietrokovski and J Hurwitz ldquoIsolation and cha-racterization of a split B-type DNA polymerase from the arch-aeonMethanobacterium thermoautotrophicumΔHrdquoTheJournalof Biological Chemistry vol 274 no 40 pp 28751ndash28761 1999

[84] K Komori and Y Ishino ldquoReplication protein A in Pyrococcusfuriosus is involved in homologous DNA recombinationrdquo TheJournal of Biological Chemistry vol 276 no 28 pp 25654ndash25660 2001

[85] J B Robbins M C Murphy B A White R I Mackie THa and I K O Cann ldquoFunctional analysis of multiple single-stranded DNA-binding proteins from Methanosarcina acetivo-rans and their effects on DNA synthesis by DNA polymeraseBIrdquoThe Journal of Biological Chemistry vol 279 no 8 pp 6315ndash6326 2004

[86] Y Lin L-J Lin P Sriratana et al ldquoEngineering of functionalreplication protein a homologs based on insights into the evolu-tion of oligonucleotideoligosaccharide-binding foldsrdquo Journalof Bacteriology vol 190 no 17 pp 5766ndash5780 2008

[87] D N Frick and C C Richardson ldquoDNA primasesrdquo AnnualReview of Biochemistry vol 70 pp 39ndash80 2001

[88] G Desogus S Onesti P Brick M Rossi and F M PisanildquoIdentification and characterization of a DNA primase fromthe hyperthermophilic archaeon Methanococcus jannaschiirdquoNucleic Acids Research vol 27 no 22 pp 4444ndash4450 1999

Archaea 13

[89] A A Bocquier L Liu I K O Cann K Komori D Kohda andY Ishino ldquoArchaeal primase bridging the gap between RNAand DNA polymerasesrdquo Current Biology vol 11 no 6 pp 452ndash456 2001

[90] L Liu K Komori S Ishino et al ldquoThe archaeal DNA primasebiochemical characterization of the p41-p46 complex fromPyrococcus furiosusrdquo The Journal of Biological Chemistry vol276 no 48 pp 45484ndash45490 2001

[91] E Matsui M Nishio H Yokoyama K Harata S Darnisand I Matsui ldquoDistinct domain functions regulating de novoDNA synthesis of thermostable DNA primase from hyperther-mophile Pyrococcus horikoshiirdquo Biochemistry vol 42 no 50 pp14968ndash14976 2003

[92] N Ito I Matsui and EMatsui ldquoMolecular basis for the subunitassembly of the primase from an archaeon Pyrococcus hori-koshiirdquoThe FEBS Journal vol 274 no 5 pp 1340ndash1351 2007

[93] M le Breton G Henneke C Norais et al ldquoThe heterodimericprimase from the euryarchaeon Pyrococcus abyssi a multifunc-tional enzyme for initiation and repairrdquo Journal of MolecularBiology vol 374 no 5 pp 1172ndash1185 2007

[94] S-H Lao-Sirieix and S D Bell ldquoThe heterodimeric primaseof the hyperthermophilic archaeon Sulfolobus solfataricus pos-sesses DNA and RNA primase polymerase and 31015840-terminalnucleotidyl transferase activitiesrdquo Journal of Molecular Biologyvol 344 no 5 pp 1251ndash1263 2004

[95] S-H Lao-Sirieix L Pellegrini and S D Bell ldquoThe promiscuousprimaserdquo Trends in Genetics vol 21 no 10 pp 568ndash572 2005

[96] J Hu L Guo K Wu B Liu S Lang and L Huang ldquoTemplate-dependent polymerization across discontinuous templatesby the heterodimeric primase from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquoNucleic Acids Research vol 40no 8 pp 3470ndash3483 2012

[97] E Evguenieva-Hackenberg P Walter E Hochleitner FLottspeich and G Klug ldquoAn exosome-like complex in Sulfolo-bus solfataricusrdquo EMBOReports vol 4 no 9 pp 889ndash893 2003

[98] P Walter F Klein E Lorentzen A Ilchmann G Klug andE Evguenieva-Hackenberg ldquoCharacterization of native andreconstituted exosome complexes from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Microbiology vol62 no 4 pp 1076ndash1089 2006

[99] Z Zuo C J Rodgers A L Mikheikin and M A Trak-selis ldquoCharacterization of a functional DnaG-type primase inarchaea implications for a dual-primase systemrdquo Journal ofMolecular Biology vol 397 no 3 pp 664ndash676 2010

[100] B R Berquist P DasSarma and S DasSarma ldquoEssential andnon-essential DNA replication genes in the model halophilicArchaeon Halobacterium sp NRC-1rdquo BMC Genetics vol 8article 31 2007

[101] D K Braithwaite and J Ito ldquoCompilation alignment andphylogenetic relationships of DNA polymerasesrdquo Nucleic AcidsResearch vol 21 no 4 pp 787ndash802 1993

[102] I K O Cann and Y Ishino ldquoArchaeal DNA replication iden-tifying the pieces to solve a puzzlerdquo Genetics vol 152 no 4 pp1249ndash1267 1999

[103] G Lipps S Rother C Hart and G Krauss ldquoA novel typeof replicative enzyme harbouring ATpase primase and DNApolymerase activityrdquo The EMBO Journal vol 22 no 10 pp2516ndash2525 2003

[104] J Yamtich and J B Sweasy ldquoDNA polymerase family X func-tion structure and cellular rolesrdquoBiochimica et BiophysicaActavol 1804 no 5 pp 1136ndash1150 2010

[105] H Ohmori E C Friedberg R P P Fuchs et al ldquoThe Y-familyof DNA polymerasesrdquoMolecular Cell vol 8 no 1 pp 7ndash8 2001

[106] N Y Yao R E Georgescu J Finkelstein and M E OrsquoDonnellldquoSingle-molecule analysis reveals that the lagging strandincreases replisome processivity but slows replication forkprogressionrdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 106 no 32 pp 13236ndash132412009

[107] U Hubscher G Maga and S Spadari ldquoEukaryotic DNA poly-merasesrdquo Annual Review of Biochemistry vol 71 pp 133ndash1632002

[108] F Boudsocq S Iwai F Hanaoka and R Woodgate ldquoSulfolobussolfataricus P2 DNA polymerase IV (Dp04) an archaeal DinB-like DNA polymerase with lesion-bypass properties akin toeukaryotic pol120578rdquo Nucleic Acids Research vol 29 no 22 pp4607ndash4616 2001

[109] L-J Lin A Yoshinaga Y Lin et al ldquoMolecular analyses ofan unusual translesion DNA polymerase fromMethanosarcinaacetivorans C2Ardquo Journal of Molecular Biology vol 397 no 1pp 13ndash30 2010

[110] I K O Cann S Ishino NNomura Y Sako andY Ishino ldquoTwofamily B DNA polymerases from Aeropyrum pernix an aerobichyperthermophilic crenarchaeoterdquo Journal of Bacteriology vol181 no 19 pp 5984ndash5992 1999

[111] T Uemori Y Ishino H Doi and I Kato ldquoThe hyperther-mophilic archaeon Pyrodictium occultum has two 120572-like DNApolymerasesrdquo Journal of Bacteriology vol 177 no 8 pp 2164ndash2177 1995

[112] T Uemori Y Ishino H Toh K Asada and I Kato ldquoOrgani-zation and nucleotide sequence of the DNA polymerase genefrom the archaeon Pyrococcus furiosusrdquo Nucleic Acids Researchvol 21 no 2 pp 259ndash265 1993

[113] B A Connolly ldquoRecognition of deaminated bases by archaealfamily-B DNA polymerasesrdquo Biochemical Society Transactionsvol 37 no 1 pp 65ndash68 2009

[114] B A Connolly M J Fogg G Shuttleworth and B T WilsonldquoUracil recognition by archaeal family B DNA polymerasesrdquoBiochemical Society Transactions vol 31 no 3 pp 699ndash7022003

[115] T T Richardson X Wu B J Keith P Heslop A C Jones andB A Connolly ldquoUnwinding of primer-templates by archaealfamily-B DNA polymerases in response to template-stranduracilrdquo Nucleic Acids Research vol 41 no 4 pp 2466ndash24782013

[116] T Lindahl ldquoInstability and decay of the primary structure ofDNArdquo Nature vol 362 no 6422 pp 709ndash715 1993

[117] I B Rogozin K S Makarova Y I Pavlov and E V Koonin ldquoAhighly conserved family of inactivated archaeal B family DNApolymerasesrdquo Biology Direct vol 3 article 32 2008

[118] M Imamura T Uemori I Kato and Y Ishino ldquoA non-120572-like DNA polymerase from the hyperthermophilic archaeonPyrococcus furiosusrdquoBiological andPharmaceutical Bulletin vol18 no 12 pp 1647ndash1652 1995

[119] I K O Cann K Komori H Toh S Kanai and Y IshinoldquoA heterodimeric DNA polymerase evidence that members ofEuryarchaeota possess a distinct DNA polymeraserdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 95 no 24 pp 14250ndash14255 1998

[120] L Aravind D D Leipe and E V Koonin ldquoToprimmdasha con-served catalytic domain in type IA and II topoisomerases

14 Archaea

DnaG-type primases OLD family nucleases and RecR pro-teinsrdquo Nucleic Acids Research vol 26 no 18 pp 4205ndash42131998

[121] M Jokela A Eskelinen H Pospiech J Rouvinen and J ESyvaoja ldquoCharacterization of the 31015840 exonuclease subunit DP1of Methanococcus jannaschii replicative DNA polymerase DrdquoNucleic Acids Research vol 32 no 8 pp 2430ndash2440 2004

[122] T Uemori Y Sato I Kato H Doi and Y Ishino ldquoA novel DNApolymerase in the hyperthermophilic archaeon Pyrococcus fur-iosus gene cloning expression and characterizationrdquo Genes toCells vol 2 no 8 pp 499ndash512 1997

[123] Y Shen K Musti M Hiramoto H Kikuchi Y Kawarabayashiand I Matsui ldquoInvariant Asp-1122 and Asp-1124 are essentialresidues for polymerization catalysis of family D DNA poly-merase from Pyrococcus horikoshiirdquo The Journal of BiologicalChemistry vol 276 no 29 pp 27376ndash27383 2001

[124] G Henneke D Flament U Hubscher J Querellou and J-P Raffin ldquoThe hyperthermophilic euryarchaeota Pyrococcusabyssi likely requires the two DNA polymerases D and B forDNA replicationrdquo Journal of Molecular Biology vol 350 no 1pp 53ndash64 2005

[125] L Cubonova T Richardson B W Burkhart et al ldquoArchaealDNA polymerase D but not DNA polymerase B is required forgenome replication in Thermococcus kodakarensisrdquo Journal ofBacteriology vol 195 no 10 pp 2322ndash2328 2013

[126] C Rouillon G Henneke D Flament J Querellou and J-PRaffin ldquoDNA polymerase switching on homotrimeric PCNA atthe replication fork of the euryarchaea Pyrococcus abyssirdquo Jour-nal of Molecular Biology vol 369 no 2 pp 343ndash355 2007

[127] G Henneke ldquoIn vitro reconstitution of RNA primer removal inArchaea reveals the existence of two pathwaysrdquoTheBiochemicalJournal vol 447 no 2 pp 271ndash280 2012

[128] G-LMoldovan B Pfander and S Jentsch ldquoPCNA themaestroof the replication forkrdquo Cell vol 129 no 4 pp 665ndash679 2007

[129] X-P Kong R Onrust M OrsquoDonnell and J Kuriyan ldquoThree-dimensional structure of the 120573 subunit of E coli DNA poly-merase III holoenzyme a sliding DNA clamprdquo Cell vol 69 no3 pp 425ndash437 1992

[130] K Daimon Y Kawarabayasi H Kikuchi Y Sako and Y IshinoldquoThree proliferating cell nuclear antigen-like proteins foundin the hyperthermophilic archaeon Aeropyrum pemix interac-tions with the two DNA polymerasesrdquo Journal of Bacteriologyvol 184 no 3 pp 687ndash694 2002

[131] I Dionne R K Nookala S P Jackson A J Doherty andS D Bell ldquoA heterotrimeric PCNA in the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Cell vol 11 no 1pp 275ndash282 2003

[132] E Warbrick ldquoPCNA binding through a conserved motifrdquoBioEssays vol 20 no 3 pp 195ndash199 1998

[133] H Nishida K Mayanagi S Kiyonari et al ldquoStructural deter-minant for switching between the polymerase and exonucleasemodes in the PCNA-replicative DNA polymerase complexrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 106 no 49 pp 20693ndash20698 2009

[134] K Mayanagi S Kiyonari H Nishida et al ldquoArchitecture of theDNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complexrdquo Proceedings of the National Academy ofSciences of the United States of America vol 108 no 5 pp 1845ndash1849 2011

[135] B Castrec C Rouillon G Henneke D Flament J Querellouand J-P Raffin ldquoBinding to PCNA in Euryarchaeal DNA

replication requires two PIP motifs for DNA polymerase D andone PIP motif for DNA polymerase Brdquo Journal of MolecularBiology vol 394 no 2 pp 209ndash218 2009

[136] P F Pluchon T Fouqueau C Creze et al ldquoAn extendednetworkof genomic maintenance in the archaeon Pyrococcus abyssihighlights unexpected associations between eucaryotic homo-logsrdquo PLoS One vol 8 no 11 Article ID e79707 2013

[137] J E Ladner M Pan J Hurwitz and Z Kelman ldquoCrystalstructures of two active proliferating cell nuclear antigens(PCNAs) encoded byThermococcus kodakaraensisrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2711ndash2716 2011

[138] Y Kuba S Ishino T Yamagami et al ldquoComparative analyses ofthe two proliferating cell nuclear antigens from the hyperther-mophilic archaeonThermococcus kodakarensisrdquo Genes to Cellsvol 17 no 11 pp 923ndash937 2012

[139] T Fukui H Atomi T Kanai R Matsumi S Fujiwara andT Imanaka ldquoComplete genome sequence of the hyperther-mophilic archaeon Thermococcus kodakaraensis KOD1 andcomparison with Pyrococcus genomesrdquo Genome Research vol15 no 3 pp 352ndash363 2005

[140] D Jeruzalmi O Yurieva Y Zhao et al ldquoMechanism of proces-sivity clamp opening by the delta subunit wrench of the clamploader complex of E coliDNApolymerase IIIrdquoCell vol 106 no4 pp 417ndash428 2001

[141] Y Shiomi J Usukura Y Masamura et al ldquoATP-dependentstructural change of the eukaryotic clamp-loader protein repli-cation factor Crdquo Proceedings of the National Academy of Sciencesof the United States of America vol 97 no 26 pp 14127ndash141322000

[142] T Miyata T Oyama K Mayanagi S Ishino Y Ishino and KMorikawa ldquoThe clamp-loading complex for processive DNAreplicationrdquoNature Structural andMolecular Biology vol 11 no7 pp 632ndash636 2004

[143] T Oyama Y Ishino I K O Cann S Ishino and K MorikawaldquoAtomic structure of the clamp loader small subunit fromPyrococcus furiosusrdquo Molecular Cell vol 8 no 2 pp 455ndash4632001

[144] A Seybert D J Scott S Scaife M R Singleton and DB Wigley ldquoBiochemical characterisation of the clampclamploader proteins from the euryarchaeon Archaeoglobus fulgidusrdquoNucleic Acids Research vol 30 no 20 pp 4329ndash4338 2002

[145] Y-H Chen Y Lin A Yoshinaga et al ldquoMolecular analyses of athree-subunit euryarchaeal clamp loader complex from Meth-anosarcina acetivoransrdquo Journal of Bacteriology vol 191 no 21pp 6539ndash6549 2009

[146] Y-H Chen S A Kocherginskaya Y Lin et al ldquoBiochemicaland mutational analyses of a unique clamp loader complex inthe archaeon Methanosarcina acetivoransrdquo The Journal of Bio-logical Chemistry vol 280 no 51 pp 41852ndash41863 2005

[147] F Matsunaga C Norais P Forterre and H Myllykallio ldquoIden-tification of short ldquoeukaryoticrdquo Okazaki fragments synthesizedfrom a prokaryotic replication originrdquo EMBO Reports vol 4no 2 pp 154ndash158 2003

[148] H Kochiwa M Tomita and A Kanai ldquoEvolution of ribonucle-ase H genes in prokaryotes to avoid inheritance of redundantgenesrdquo BMC Evolutionary Biology vol 7 article 128 2007

[149] N OhtaniMHarukiMMorikawa and S Kanaya ldquoMoleculardiversities of RNases Hrdquo Journal of Bioscience and Bioengineer-ing vol 88 no 1 pp 12ndash19 1999

Archaea 15

[150] N Ohtani M Haruki M Morikawa R J Crouch M Itayaand S Kanaya ldquoIdentification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII fromBacillus subtilis classification of RNases H into three familiesrdquoBiochemistry vol 38 no 2 pp 605ndash618 1999

[151] N Ohtani H Yanagawa M Tomita and M Itaya ldquoIdentifi-cation of the first archaeal type 1 RNase H gene from Halobac-terium sp NRC-1 archaeal RNase HI can cleave an RNA-DNAjunctionrdquoThe Biochemical Journal vol 381 no 3 pp 795ndash8022004

[152] N Ohtani H Yanagawa M Tomita and M Itaya ldquoCleavage ofdouble-stranded RNA by RNase HI from a thermoacidophilicarchaeon Sulfolobus tokodaii 7rdquo Nucleic Acids Research vol 32no 19 pp 5809ndash5819 2004

[153] M A Nowak M C Boerlijst J Cooke and J M SmithldquoEvolution of genetic redundancyrdquo Nature vol 388 no 6638pp 167ndash170 1997

[154] A E Tomkinson S Vijayakumar J M Pascal and T Ellen-berger ldquoDNA ligases structure reactionmechanism and func-tionrdquo Chemical Reviews vol 106 no 2 pp 687ndash699 2006

[155] M Nakatani S Ezaki H Atomi and T Imanaka ldquoA DNAligase from a hyperthermophilic archaeon with unique cofactorspecificityrdquo Journal of Bacteriology vol 182 no 22 pp 6424ndash6433 2000

[156] Y Sun M S Seo J H Kim et al ldquoNovel DNA ligase with broadnucleotide cofactor specificity from the hyperthermophilic cre-narchaeon Sulfophobococcus zilligii influence of ancestral DNAligase on cofactor utilizationrdquo Environmental Microbiology vol10 no 12 pp 3212ndash3224 2008

[157] T R Beattie and S D Bell ldquoCoordination of multiple enzymeactivities by a single PCNA in archaeal Okazaki fragmentmaturationrdquo The EMBO Journal vol 31 no 6 pp 1556ndash15672012

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

2 Archaea

eukaryotes evolved In the archezoan scenario the ancestorsof the early eukaryotes are as ancient as the two prokaryoticlineages the Bacteria and Archaea In the symbiogenesisscenario the eukaryotes evolved relatively late after thediversification of the ancient archaeal and bacterial line-ages

The cultivated Archaea are taxonomically divided intofive phyla Crenarchaeota and Euryarchaeota are best char-acterized and this taxonomic division is strongly supportedby comparative genomics A number of genes with keyroles in chromosome structure and DNA replication arepresent in one phylum but absent in the other Crenar-chaeotes also exhibit a vast physiological diversity includingaerobes and anaerobes fermenters chemoheterotrophs andchemolithotrophs [2] The majority of the cultivated crenar-chaeotes are also thermophiles [13] Euryarchaeotes exhibitan even larger diversity with several different extremophilesamong their ranks in addition to large numbers ofmesophilicmicroorganisms Interestingly all the known methanogensbelong to this phylum Additionally environmental sequenc-ing 16S rRNA analysis and cultivation efforts provide strongevidence for three additional phylaThaumarchaeota Korar-chaeota and Aigarchaeota [14ndash16] A sixth phylum has alsobeen proposed previously the Nanoarchaeota This phy-lum includes the obligate symbiont Nanoarchaeum equitanswhich has a greatly reduced genome [17] However a morecomplete analysis of its genome suggests that N equitanscorresponds to a rapidly evolving euryarchaeal lineage andnot an early archaeal phylum [18]

2 General Overview ofthe DNA Replication Process

The general process of DNA replication is conserved amongthe three domains of life but each domain possesses somefunctional modifications and variations in key proteinsDNA replication may be divided into four main stepsStep 1 (Preinitiation) starts when specific proteins recognizeand bind the origin of replication forming a protein-DNAcomplex This complex recruits an ATP-dependent helicaseto unwind the double-stranded DNA (dsDNA) The single-stranded DNA (ssDNA) formed is then protected by ssDNA-binding proteins (SSB) Step 2 (Initiation) corresponds to therecruitment of the DNA primase and DNA polymerase Step3 (Elongation) corresponds to the duplication of both strandsof DNA at the same time by the same unidirectional replica-tion machine Because of the antiparallel nature of the DNAthe leading strand is copied continuously and the laggingstrand is copied discontinuously as Okazaki fragments [10]During replication a sliding-clamp protein surrounds theDNA and binds to the polymerase to increase processivityor the number of nucleotides added to the growing strandbefore disassociation of the polymerase from the templateStep 4 (Maturation) corresponds to the completion of thediscontinuous replication in the lagging strand by the actionsof RNase DNA ligase and Flap endonucleaseThe variabilityof the players involved in each of these processes between thethree domains of life andmore specifically within theArchaeadomain is discussed in further detail below

3 DNA Replication Components

31 Preinitiation (Origin of Replication and Origin Recogni-tion) The number of origins of replication in a genome iscorrelated with phylogeny and varies among the differentdomains [19] Members of the Bacteria domain usuallypossess only one replication origin but eukaryotic chromo-somes contain multiple replication origins This differencewas generally accepted as a clear divisor in DNA repli-cation of eukaryotes and prokaryotes However membersof the Archaea domain display either one or multiple ori-gins of replication The origins of replication in archaeaare commonly AT-rich regions which possess conservedsequences called origin of recognition boxes (ORB) and arewell conserved across many archaeal species Also smallerversions of the ORBs calledmini-ORBs have been identified[20] Members of the Crenarchaeota phylum display multipleorigins of replication For example species belonging to theSulfolobales order contain three origins of replication [20 21]Likewise two and four origins of replication have been foundin members of the Desulfurococcales (Aeropyrum pernix)and Thermoproteales (Pyrobaculum calidifontis) respectively[22 23] In addition to shortening the time required forreplication multiple origins may play a role in counteractingDNA damage during hyperthermophilic growth [24] Incontrast most members of the Euryarchaeota phylum seemto possess only one origin of replication For example speciesbelonging to the Thermococcales (Pyrococcus abyssi) andArchaeoglobales (Archaeoglobus fulgidus) orders contain onlyone origin of replication [25ndash27] However members ofthe order Halobacteriales (eg Halobacterium sp NRC-1Haloferax volcanii andHaloarcula hispanica) possess numer-ous origins of replication that may be part of an intricatereplication initiation system [28ndash30] In fact a recent reportdemonstrated that the different origins of replication inHaloarcula hispanica are controlled by diverse mechanismswhich suggest a high level of coordination between themultiple origins [31] In contrast the deletion of a singleorigin of replication in Haloferax volcanii affects replicationdynamics and growth but the simultaneous deletion of allfour origins of replication accelerated growth compared tothe wild type strain [32] These results suggest that initiationof replication in Haloferax volcanii may be dependent ofhomologous recombination as it is in some viruses andgenerate questions about the purpose of the replicationorigins [32] With the exception of Methanothermobacterthermautotrophicus the DNA replication origin has not beenexperimentally demonstrated in themethanogens [33] How-ever bioinformatics analysis by GC-skew in Methanosarcinaacetivorans [34] and119885-curve analysis forMethanocaldococcusjannaschii and Methanosarcina mazei suggest a single originof replication A similar analysis of M maripaludis S2 wasinconclusive [35] The fact that the order Halobacteriales isthe only euryarchaeote that displays multiple origin of repli-cation suggests that there may have been a lineage-specificduplication in this group Moreover the number of origins isnot highly conserved even within a single archaeal phylum

The origin of replication is recognized by specific proteinsthat bind and melt the dsDNA and assist in the loading of

Archaea 3

Order Phylum Number ofgenomes

Number of homologs for replication genesORCCDC6 GINS15 GINS23 RPA MCM RFCS PCNA PolB DP1 DP2

Nitrosopumilales Thaumarchaeota 2 1 0 or 1 0 or 1 1 1 1 1 1 1 1

Thermoproteales

Crenarchaeota

14 0 0 1 1 to 3 1 to 3 0 09 2 0 0 or 1 1 0 0Desulfurococcales

15 3 1 1 1 1 1 3 0 0SulfolobalesNot named Korarchaeota 1 2 0 0 0 1 1 1 2 1 1Nanoarchaeota 1 1 0 0 1 1 1 1 1 1 1Thermococcales 11 1 1 3 1 1 1

1Methanopyrales 1 0 0 0 0 1 1 1 1 11

Methanobacteriales 7 1 or 2 0 or 1 0 1 1 1 2 1 1

Methanococcales Euryarchaeota 15 0 0 0 2 to 4 2 to 8 1 1 1 1

Thermoplasmatales 4 0 1 1 1 1 1 1 1

Archaeoglobales 4 2 or 3 0 0 1 or 2 1 1 1 1

Halobacteriales 15 3 to 15 0 0 1 1 or 2 1 1 1

Methanomicrobiales 6 0 0 1 1 2 1 1 or 2 1 1

Methanocellales 1 2 0 0 1 1 1 1 3 1 1Methanosarcinales 9 0 0 3 1 1

0lowast

0lowast

0lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

3lowast

2lowast

2lowast

2lowast

2lowast

2lowast

2lowast

Figure 1 Homologs for some key genes involved in archaeal DNA replication Archaeal orders are phylogenetically organized followinga rooted maximum likelihood tree of Archaea based on 53 concatenated ribosomal proteins [36] The homology search was performedby RAST v40 (Rapid Annotation using Subsystem Technology) and the annotated data was viewed through the SEED viewer(httpwwwtheseedorg) A total of 115 archaeal genome sequences were obtained from NCBI and uploaded into the RAST server RASTannotation was performed using default parameters with the genetic code for Bacteria and Archaea The replication proteins homologswere checked through the SEED subsystem DNA replication Homology results of Thermococcus kodakaraensis KOD1 Pyrococcus furiosusDSM 3638 and Thermofilum pendens Hrk 5 were searched for replication protein homologs using BLAST (blastx v2228+) Results withhomology coverage of gt80 and 119864-values less than 0001 were considered as real homologs The results were also supplemented withdata from literature reviews and BLAST searches When indicated in the figure zero (0) homologs means that no homolog was foundfor a specific gene by using the described methodology Asterisks indicate that one or two of the analyzed microorganisms possessan exception for that specific feature Exceptions noted are (featureorder) ORC1CDC6Thermoproteales Thermofilum pendens Hrk5 (3homologs) and Thermosphaera aggregans DSM11486 (2 homologs) ORC1CDC6Thermoplasmatales and Picrophilus torridus DSM 9790(1 homolog) ORC1CDC6Methanomicrobiales and Methanoplanus petrolearius DSM11571 (4 homologs) ORC1CDC6Methanosarcinalesand Methanosalsum zhilinae DSM4017 (4 homologs) GINS15Thermoplasmatales and Thermoplasma acidophilum DSM1728 (1 homolog)GINS23Desulfurococcales Staphylothermus hellenicus DSM12710 (no homolog) and Staphylothermus marinus F1 (no homolog)GINS23Thermococcales Pyrococcus horikoshii OT3 (2 homologs) RPAThermoproteales Thermofilum pendens Hrk5 (3 homologs)and Thermosphaera aggregans DSM11486 (1 homolog) RPAMethanobacteriales and Methanothermus fervidus DSM2088 (no homolog)RPAArchaeoglobales and Archaeoglobus fulgidus DSM4304 (1 homolog) MCMThermococcales and Thermococcus kodakaraensis KOD1(3 homologs) MCMMethanosarcinales and Methanosarcina acetivorans C2A (2 homologs) RFCSDesulfurococcales and Hyperthermusbutylicus DSM 5456 (2 homologs) RFCSHalobacteriales and Haloquadratum walsbyi DSM16790 (1 homolog) RFCSMethanosarcinalesMethanosaeta concilii CG6 (2 homologs) and Methanosaeta thermophila PT (2 homologs) PCNADesulfurococcales and Ignisphaeraaggregans DSM17230 (1 homolog) PCNASulfolobales and Metallosphaera cuprina Ar-4 (1 homolog) PCNAThermococcales Pyrococcushorikoshii OT3 (2 homologs) and Thermococcus kodakaraensis KOD1 (2 homologs) PCNAMethanococcales Methanococcus maripaludisS2 (2 homologs) and Methanotorris igneus Kol5 (2 homologs) PolBThermoproteales Caldivirga maquilingensis IC-167 (3 homologs)and Pyrobaculum calidifontis JCM 11548 (3 homologs) PolBDesulfurococcales Staphylothermus hellenicus DSM12710 (3 homologs) andStaphylothermus marinus F1 (3 homologs) PolBArchaeoglobales Archaeoglobus fulgidus DSM4304 (2 homologs) PolBHalobacterialesHalorhabdus utahensis DSM12940 (2 homologs) PolBMethanosarcinales Methanosaeta concilii GP6 (2 homologs) DP1MethanosarcinalesMethanococcoides burtonii DSM6242 (2 homologs)

the replicative helicases In Bacteria this protein is DnaAwhich binds to the DnaA boxes [37] In eukaryotes aprotein complex known asORC (origin recognition complex)composed of 6 different proteins (Orc1-6) binds at thereplication origin and recruits other proteins [38] InArchaeathe candidate for replication initiation is a protein that shareshomology with the eukaryotic Orc1 and Cdc6 (cell divisioncycle 6) proteins and is encoded by almost all archaealgenomes [39] Their genes are commonly located adjacent tothe origin of replication These proteins termed Orc1Cdc6homologs have been studied in detail in representatives of theEuryarchaeota (Pyrococcus) and Crenarchaeota (Sulfolobus)and have been shown to bind to the ORB region with highspecificity [20 26 40] In addition purified Orc1Cdc6 from

S solfataricus binds to ORB elements from other crenar-chaeotes and euryarchaeotes in vitro suggesting that theseproteins recognize sequences conserved across the archaealdomain [20] The crystal structures of these proteins fromPyrobaculum aerophilum [41] and Aeropyrum pernix [42]have been solved contributing to the overall understandingof their activity during the initiation of replication (reviewedin [43]) In general the number of Orc1Cdc6 homologsfound in archaeal genomes varies between one and three(Figure 1) However there are some interesting exceptionsMembers of the order Halobacteriales possess between 3 and15Orc1Cdc6 homologs which may reflect the large numberof origins of replication Interestingly like other members oftheMethanosarcinales the extremely halophilic methanogen

4 Archaea

Methanohalobium evestigatum Z-7303 only possesses twoOrc1Cdc6 homologs Thus the ability to grow at extremelyhigh concentrations of salt and to maintain high intracellularsalt concentrations does not necessarily require a largenumber of Orc1Cdc6 homologsAlthoughmost members ofthe orderMethanomicrobiales possess two copies of this geneMethanoplanus petroleariusDSM 11571 possesses four copiesThus the number of Orc1Cdc6 homologs varies consider-ably among the euryarchaeotes In an extreme case repre-sentatives of the ordersMethanococcales andMethanopyralesdo not possess any recognizable homologs for the Orc1Cdc6protein [7 44] and the mechanics of replication initiation inthese archaea remain an intriguing unknown of the archaealreplication process

32 Initiation (DNA Unwinding and Primer Synthesis) AfterOrc1Cdc6 proteins bind to the origin of replication ahelicase is recruited to unwind the dsDNA In Bacteria thereplicative helicase is the homohexamer DnaB In eukaryotesthe most likely candidate for the replicative DNA helicase isthe MCM (minichromosome maintenance) complex whichis a heterohexamer that is activated when associated withother replicative proteins forming the CMG (Cdc45-MCM-GINS) complex [45ndash48] As in eukaryotes in Archaea themost probable candidate for the replicative helicase is theMCM complex Intriguingly theMCM complexes in eukary-otes and archaea possess a 31015840-51015840 unwinding polarity but thebacterialDnaBhelicase unwinds duplexDNAon the oppositedirection with a distinct 51015840-31015840 polarity [49ndash51]

Most archaeal genomes studied so far encode one MCMhomolog Its helicase activity has been demonstrated invitro for several archaea including Methanothermobacterthermautotrophicus ΔH where the MCM protein forms adimer of hexamers [52 53] The in vivo interaction betweenthe MCM complex and the Orc1Cdc6 proteins has beendemonstrated in other Archaea [54ndash56] Indeed through anin vitro recruiting assay Orc1CDC6 from P furiosus has beendemonstrated as the possible recruiter of the MCM complexto the origin of replication [57] A recent study identifiedthirteen species of archaeawithmultiplemcm genes encodingthe MCM complexes (Figure 1 [58]) The number of mcmhomologs is especially high in the order Methanococcaleswhere different representatives possess from 2 to 8 copies[59 60] For instance Methanococcus maripaludis S2 pos-sesses four homologs of the MCM protein [44] Through ashotgun proteomic study peptides for three of them havebeen detected [61] suggesting that multiple MCMs areexpressed and functional However a genome-wide surveyof gene functionality in M maripaludis demonstrated thatonly one of these genes MMP0030 was likely to be essentialfor growth [62] In addition coexpression of recombinantMCMs from M maripaludis S2 allowed copurification ofall four proteins [59] suggesting that M maripaludis mayform a heterologous multimeric MCM complex Howeverbecause MMP0030 protein is the only mcm gene essentialfor growth a homologous multimeric complex may alsobe possible Similar results have been found in Thermo-coccus kodakaraensis in which three MCM homologs arepresent but only one is essential [63] The T kodakaraensis

MCM system is suggested to form homologous multimericcomplexes [64] A recent study proposed that two of theMCMhomologs that are conserved among representatives ofthe order Methanococcales are a consequence of an ancientduplication that occurred prior to the divergence of thisgroup [59] It has also been proposed that the large numberof MCM homologs in the order Methanococcales is a directconsequence of mobile elements which may have takenadvantage of the ancient duplication of the MCM genes totake over the replication system by forming cellular MCMheterocomplexes [58] In any case the large number of MCMhomologs in the order Methanococcales may be a product ofan intricate and complex evolutionary history Whether ornot it is related to the absence of the replication initiationprotein Orc1Cdc6 is an interesting possibility [58]

In eukaryotes the MCM complex is not active on itsown and requires the association of two accessory factorsthe heterotetrameric GINS complex (from the Japanese go-ishi-ni-san meaning 5-1-2-3 after the four subunits Sld5Psf1 Psf2 and Psf3) and the Cdc45 protein This complexcalled CMG (Cdc45-MCM-GINS) is thought to be the activereplicative helicase [47] Homologs for GINS subunits havebeen identified in Archaea by bioinformatics analysis Onehomolog is most similar to the eukaryotic proteins Psf2and Psf3 (GINS23) and is common in the crenarchaeotesAnother homolog is most similar to the eukaryotic pro-teins Psf1 and Sld5 (GINS15) and is found largely in theeuryarchaeotes [65] The GINS complex is expected to beessential for DNA replication but the distribution of thesetwo different GINS homologs suggests that the presence ofone of them is sufficient for archaeal DNA replication SomeCrenarchaeota (S solfataricus) and some Euryarchaeota (Pfuriosus and T kodakaraensis) possess both homologs andform heterotetramers similar to the ones found in eukaryoteswith a ratio 2 2 [66ndash68] To find homologs of GINS15 andGINS23 in Archaea two known GINS15 (from Sulfolobussolfataricus P2 and Thermococcus gammatolerans EJ3) andthree known GINS23 (from Sulfolobus solfataricus P2 Pyro-coccus yayanosii CH1 andThermococcus gammatolerans EJ3)were used for homology searches These analyses failed toidentifyGINShomologs in several archaeal groups (Figure 1)These results suggest that there are other unknown GINShomologs in archaea or that the sequences have divergedenough between genera not to be recognized by homologysearches In any case a more comprehensive analysis of GINSproteins is necessary to fully understand their function anddistribution in Archaea

The detailed interactions of the GINS andMCM proteinsin archaea appear to be highly variable Although the Ssolfataricus GINS and MCM proteins physically interactin vitro MCM helicase activity was not stimulated in thecomplex [66] In contrast the MCM helicase activity of Tkodakaraensis and P furiosus is clearly stimulated by theirGINS complexes [64 67] The crystal structure of the GINScomplex of T kodakaraensis was recently determined Thebackbone structure and the assembly are similar to thehuman complex with some notable differences [68] Interest-ingly many other euryarchaeotes possess only the homologto GINS15 One of those Thermoplasma acidophilum forms

Archaea 5

a homotetrameric complex [68 69] Moreover in vitro the Tacidophilum MCM helicase activity was not affected by theGINS complex [69] These results suggest that other proteinsmay be involved in the formation of a stable helicase in manyArchaea M maripaludis S2 possesses a hypothetical proteinwhich may correspond to the gene encoding for GINS15which is probably essential for growth [60 62] No homologsof GINS23 are present in the genome ofM maripaludis

The replication related Cdc45 protein is ubiquitous ineukaryotes but its exact role has not yet been elucidatedInterestingly homologs of the Cdc45 protein are not presentin Archaea However a bioinformatics analysis revealed thatthe eukaryotic Cdc45 and the prokaryotic RecJ which is aconserved 51015840-31015840exonuclease in most bacteria and archaeapossess a common ancestry and share a homologous DHHdomain [70] These results suggest that the archaeal RecJmay substitute for the eukaryotic Cdc45 during replicationCircumstantial evidence supports this conclusion In S solfa-taricus a homolog of the DNA binding domain of RecJ waspurified together with a GINS protein [66] Similarly in Tkodakaraensis the RecJ homolog (TK1252p) copurified withproteins of theGINS complex [71] and formed a stable in vitroassociation with the GINS complex [72] Two RecJ homologsare found inM jannaschii (MJ0977 and 0831) and they par-tially complement a recJ mutation in E coliThe recombinantMJ0977 also possesses high levels of thermostable single-stranded DNA degrading activity similar to RecJ [73] In Mmaripaludis S2 four proteins possess the DHH domain withsimilarity to the M jannaschii RecJ homologs (MMP16820547 1078 and 1314) However none of them was essentialfor growth suggesting that the activities were redundant [62]Alternatively another protein which has a low similaritywith M jannaschii RecJ homolog (MMP0285) but possessesthe DHH domain was possibly essential for growth [62]However this protein possesses other domains related totransport which make it an unlikely candidate for RecJThese results are not definitive and more experimental datais needed to assign a function to this protein

As soon as the DNA is unwound ssDNA is protectedfromnucleases chemicalmodification and other disruptionsby ssDNA binding proteins These proteins are present in allthree domains of life and are called SSB in Bacteria wherethey form homotetramers or homodimers [74 75] and RPA(replication protein A) in eukaryotes where they form astable heterotrimer composed of 70 32 and 14 kDa proteins[76] Although all ssDNA binding proteins contain dif-ferent combinations of the oligonucleotideoligosaccharide-binding fold or OB-fold [77] the sequence similarity is lowamong RPA and the bacterial SSBs [43] In Archaea differ-ent types of ssDNA binding proteins have been reportedIn crenarchaeotes an ssDNA binding protein is only wellcharacterized in S solfataricus The S solfataricus ssDNAbinding protein contains only one OB-fold and can adopt aheterotetramer conformation [78] However the protein alsoappears to exist as a monomer [79] This protein appears tobe more similar to the bacterial proteins in sequence but itsstructure is more similar to that of the eukaryotic RPAs [4380] While homologs are recognizable in other members ofthe Sulfolobales andmost otherArchaea they are absent from

the genomes of many members of the closely related orderThermoproteales with some few exceptions (Figure 1) [81]

RPAs have been studied from different representativesof the euryarchaeotes revealing additional diversity M jan-naschii andM thermautotrophicus possess a single RPA sub-unit which shares amino acid similarity with the eukaryoticRPA70 and possesses four and five OB-folds respectively [8283] P furiosus possesses three different RPA subunits whichform a stable heterotrimer that is involved in homologousrecombination in vitro [84] The P furiosus RPA thereforeis similar in subunit organization to the eukaryotic RPATheother members of the Thermococcales genera also possessthree RPA homologs which likely form the homotrimericcomplex described for P furiosus (Figure 1) Methanosarcinaacetivorans also possesses three different RPAproteins (RPA1-3) with four two and two OB-folds respectively Howeverthey do not interact with each other and appear to functionas homodimers [85] This arrangement is common amongthe Methanosarcinales but is not found in the closely relatedmethanogen orders such as the Methanocellales (Figure 1)Members of the order Methanococcales possess two to fourRPA homologs The genome of M maripaludis S2 containsthree possible RPA homologs (MMP0122 0616 and 1032)[60] Only MMP0616 and 1032 were likely to be essential forgrowth [62] suggesting a possible different complex configu-ration for RPA proteins in this archaeon It has been hypoth-esized that the diversity in OB-folds in the archaeal RPAs is adirect consequence of homologous recombination [86]

DNA synthesis starts with the production of a RNAprimer since the DNA polymerases that replicate genomesare incapable of de novo DNA synthesis The RNA primeris synthesized by a DNA-dependent RNA polymerase orprimase DnaG a single subunit protein is the primase inBacteria In eukaryotes a two-subunit primase consisting ofa small catalytic subunit (PriS) and a large subunit (PriL)is found in a complex with DNA polymerase 120572 and itsaccessory B subunit [87] In Archaea the first biochemicallycharacterized primase was the eukaryotic primase-like smallsubunit PriS in M jannaschii [88] Later homologs of thePriS and PriL subunits were described in several Pyrococ-cus species [89ndash93] The eukaryotic-like DNA primase hasalso been characterized in the crenarchaeote S solfataricus[94 95] where it has been shown to interact with MCMthrough GINS23 [66] A unique polymerization activityacross discontinuous DNA templates has been characterizedin the PriSL of S solfataricus suggesting that this primasemay be involved in double-stranded break repair in Archaea[96] So far the eukaryotic-like primases found in archaeaexhibit similar properties PriS functions as the catalyticsubunit and PriL modulate its activity [87] In additionthe archaeal eukaryotic-like primase has the unique abilityto synthesize both DNA and RNA in vitro Indeed theP furiosus PriS synthesizes long DNA fragments but theaddition of PriL regulates the process by decreasing theDNA polymerase activity increasing the RNA polymeraseactivity and decreasing the product length [90] Additionallystudies of the P abyssi enzyme suggest that DNA primasemay also be involved in DNA repair because of the DNApolymerase gap filling and strand displacement activities

6 Archaea

also present in vitro [93] Interestingly the archaeal primasesmall subunit resembles DNA polymerases from the Pol Xfamily in sequence and structure suggesting a similarity intheir catalytic mechanism [96]

Homologs of the bacterial DnaG primase are also foundin archaea However in vitro studies of the P furiosusenzyme failed to detect primer synthesis activity and the TkodakaraensisDnaG was copurified with proteins of the exo-some [71] Also in S solfataricus DnaG primase was found tobe a core exosome subunit involved in RNA degradation [9798] However recent studies demonstrated that the S solfa-taricus DnaG homolog has limited primer synthesis activityand a dual primase system with PriSL has been proposed tofunction during DNA replication [99] Hu et al hypothesizedan interesting theory which suggests that LUCA employed adual-primase system comprisingDnaG and PriSL which alsoserved roles in RNA degradation and the nonhomologousend joining (NHEJ) pathwayThe system was inherited by allthree domains In theArchaea domain it retained its originalfunctions However in the Bacteria domain DnaG becamethe major replicative primase and PriSL evolved into the Poldomain of LigD involved in the NHEJ pathway In contrastDnaG was lost in the Eukaryota domain and PriSL becamethe only replicative primase In addition it also evolved intothe DNA Pol X family involved in NHEJ [96]

Like other ArchaeaM maripaludis S2 possesses both theeukaryotic- and bacterial-like primases A new genome-widesurvey of this methanoarchaea revealed that genes encodingboth subunits of the eukaryotic like primase PriS and PriL(MMP0009 and MMP0071) were likely to be essential forgrowth which is consistent with a role in replication Similarobservations have been demonstrated in other Archaea suchas Halobacterium sp NRC-1and Haloferax volcanii [93 100]In contrast the DnaG primase (MMP1286) was nonessentialwhich would be consistent with a role in the exosome [62]These results suggest that in M maripaludis and probablyother euryarchaeotes a dual primase system is not pre-sent

33 Elongation (Replicative DNA Polymerase) The primersynthesized by the primase is further extended by a replicativeDNA polymerase DNA polymerases have been classifiedinto seven families based on their amino acid sequencesimilarity (A B C D E X and Y) [101ndash105] In Bacteria Ecoli possesses five DNA polymerases Pol IndashV where the firstthree belong to families A B and C respectively and the lasttwo belong to the Y family The major replicative DNA poly-merase in E coli is Pol III a member of the C family whichsynthesizes DNA with high processivity when functioningwithin the holoenzyme [106] In eukaryotes a great diversityof DNA polymerases is also found but DNA replicationrequires three replicative DNA polymerases which belongto family B (Pol120572 Pol120575 and Pol120576) [107] In Archaea fewertypes of DNA polymerases are present but they have aninteresting evolutionary division Representatives of theDNApolymerase B family are found in all Archaea The D familyDNA polymerase is present in every phyla studied so farwith the exception of the Crenarchaeota (Figure 1) Lastly amember of theY family has been identified andbiochemically

characterized in S solfataricus [108] and the Methanosarci-nales in which several species harbor two homologs [109]Even though the activity of DNA polymerases belongingto the Y family in archaea is not fully understood they aresuggested to play an important role in DNA repair [109]

Representatives of the DNA polymerase family B havebeen identified in all Archaea The crenarchaeotes possess atleast two family B DNA polymerases (PolB I and PolB IIand in some cases PolB III) [102 110 111] The recombinantS solfataricus Pyrodictium occultum and A pernix enzymeshave been characterized [102] In contrast euryarchaeotesonly contain PolB I The recombinant P furiosus enzymehas been characterized [112] The PolB I enzymes havesimilar amino acid sequence and overall structure and theypossess a potent 31015840-51015840exonuclease proofreading activity [102]A unique property of the archaeal family B DNA polymeraseis the ability to stall DNA polymerization in the presenceof uracil or hypoxanthine deaminated bases [113 114] thisproperty helps to prevent the copy of template-strand uraciland the transmission of fixed mutations to progeny [115]Commonly cytosine deamination converts GC base pairsinto the promutagenic GU mismatches which result in50 of the offspring containing an AT transition mutationafter replication [116] In addition when A-U base pairs areformed the loss of the 5-methyl moiety upon replacementof thymine can exert a detrimental effect on protein DNAinteractions Interestingly in some crenarchaeotes and eur-yarchaeotes one of the B family DNA polymerase paralogspossesses disrupted versions of the sequence motifs thatare essential for catalysis Possibly these enzymes possess astructural role [117]

DNA polymerase family D (PolD) is a novel enzyme thatwas originally discovered in P furiosus [118] It has sincethen been identified in all euryarchaeotes [119] For a longtime this enzyme was considered a euryarchaeote-specificpolymerase but the three newly discovered archaeal phylawere also found to possess genes for PolD [14ndash16] PolD isa heterodimer with a small subunit (DP1) and a large subunit(DP2) It has been proposed that the large subunit harborsthe polymerase activity although its sequence is very differentfrom other hitherto described DNA polymerases The smallsubunit possesses high similarity with the noncatalytic B-subunits of the eukaryoticDNApolymerases120572 120575 and 120576 [120]Studies of the M jannaschii enzyme demonstrated that thesmall subunit possesses a strong 31015840-51015840exonuclease activitysuggesting that it may be involved in proofreading activity[7 121] Efficient polymerase and proofreading activity havealso been detected from a purified PolD of P furiosus andthe residues Asp-1122 and Asp-1124 are essential for thepolymerization reaction in P horikoshii [122 123] Everyeuryarchaeote examined possessed one homolog for DP1 andDP2 except forMethanococcoides burtoniiDSM 6242 whichpossesses two homologs for DP1 (Figure 1)

Because the crenarchaeotes only possess family B DNApolymerases one of themmust be the replicative polymeraseHowever in euryarchaeotes it was not clear which enzymewas involved in replication Studies in Halobacterium spNRC-1 showed that both PolB and PolD were essential forviability and it was proposed that they could be working

Archaea 7

together at the replication fork synthesizing the leading andlagging strand respectively [100 124] However in otherEuryarchaeota PolB does not appear to be essential Forinstance a recent report demonstrated that both subunits ofPolDwere essential but PolB was nonessential for the growthof M maripaludis S2 [62] Likewise in T kodakaraensisPolD can be coisolated with different proteins of the archaealreplication fork but PolB wasmainly coisolated with proteinsof unknown function [71] A deletion of the PolB in Tkodakaraensis also had no detectable effect on cell viability[125] Interestingly T kodakaraensis PolB mutants haveincreased sensitivity to UV radiation These results togethersuggest that PolD is the essential replicative DNA polymerasein these euryarchaeotes and not a PolB family polymeraseIn this scenario PolB may have some other crucial functionin Halobacterium and possibly other closely related specieswhich it is not conserved throughout the phylum Finallyit has been demonstrated that purified PolD from P abyssiis able to perform strand displacement and RNA primerextension in vitro Purified PolB on its own cannot performthese activities in vitro but in the presence of PCNA stranddisplacement activity is stimulated [124 126] A recent in vitrostudy in P abyssi demonstrated that RNase HII is required toinitiate strand displacement DNA synthesis by PolB [127]

34 Elongation (Other Accessory Proteins) Purified DNApolymerases possess low processivity however the addi-tion of an accessory factor the sliding clamp gives DNApolymerases the required processivity to replicate genomesThis factor whose structure resembles a doughnut functionsas a molecular platform which recruits several replication-associated enzymes and act together with DNA and thepolymerase to stabilize their interactions during replication[128] The structure of sliding clamps is conserved in thethree domains of life In Bacteria the sliding clamp or 120573-subunit is a homodimeric ring [129] In eukaryotes thesliding clamp or proliferating cell nuclear antigen (PCNA)is a homotrimeric ring [128] In Archaea the majority ofcrenarchaeotes have multiple PCNA homologs which formheterotrimeric rings [130 131] (Figure 1) In contrast mosteuryarchaeotes possess a single PCNA homolog (Figure 1)Interactions of DNA polymerase with the sliding clampare mediated through a common motif called the PCNAInteracting Protein (PIP) box [132] The three dimensionalstructures of PCNA-PolB and the PolB-PCNA-DNA complexfrom P furiosus have been solved shedding light on theinteractions between these molecules [133 134] In additiona study demonstrated that the PolDPCNA and PolBPCNAinteractions require two and one PIP boxes respectively[135] Recently through a protein-interaction network of Pabyssi a previously unknown protein with nuclease activity(Pab0431) and a PIP canonical motif was discovered tointeract with PCNA suggesting a possible involvement inDNA replication [136] T kodakaraensis is the only well-documented example of an euryarchaeotewith twohomologsfor PCNA TK0535 (PCNA1) and TK0582 (PCNA2) Recentwork demonstrated both proteins form stable homotrimericrings that interact with T kodakaraensis PolB in vitro [137]A more detailed study of the two homologs of PCNA in T

kodakaraensis demonstrated that both homologs stimulate invitro the primer extension activity of PolB but only PCNA1and not PCNA2 stimulates the same activity of PolD [138]Also the same report showed that the pcna2 gene can bedisrupted without causing growth deficiencies but it was notpossible to isolate mutants of pcna1 These results suggestthat PCNA1 but not PCNA2 is essential for DNA replication[138] It has been proposed that one of the PCNA geneswas acquired by lateral gene transfer [139] Members of theorderMethanococcales possess one PCNA homolog with twoexceptionsMmaripaludis S2 possesses twoPCNAhomologs(MMP1126 and 1711) [60] Both genes appeared to be essentialfor growth suggesting that they both play an importantrole in replication [62] The gene MMP1711 possesses highsimilarity to both T kodakaraensis genes and is likely thetrue methanococcal PCNA In contrast MMP1126 possessesonly low similarity to the T kodakaraensis genes and alsocontains an S-adenosylmethionine-dependent methyltrans-ferases domain Thus it is likely to possess some alternativefunction Methanotorris igneus Kol 5 also possesses twoPCNA homologs

For PCNA to assemble around DNA a specific loadingfactor is required In Bacteria the loading factor is knownas 120574-complex and comprises three different subunits ina 1205743-120575-1205751015840 stoichiometry [140] In eukaryotes the loading

factor is known as Replication Factor C (RFC) and is aheteropentameric complex comprising one large subunit andfour different small subunits [141] In contrast inArchaea theRFC consists of two different proteins a small subunit RFCSand a large subunit RFCLThey also form a heteropentamericcomplex in a 4 1 ratio (RFCS RFCL) Interestingly manycrenarchaeotes possess one homolog of RFCL and two orthree homologs of RFCS Alternatively most euryarchaeotespossess only one RFCL and RFCS homolog The exceptionsare somemembers of the ordersHalobacteriales Methanomi-crobiales and Methanosarcinales which possess two RFCShomologs (Figure 1) Structural and biochemical studies ofRFC have been conducted in several euryarchaeotes such asArchaeoglobus fulgidus and Pyrococcus species [142ndash144] Aninteresting case is observed in Methanosarcina acetivoransThis RFC possesses three subunits (RFC1 2 L) found ina ratio 3 1 1 [145] Homologs for these three subunits arealso present in most of the genomes of the haloarchaea[145] It is inferred that this type of RFC complex representsan intermediary form transitional between the canonicalarchaeal RFC complex of one small and one large subunit andthe eukaryotic RFC complex of four different small and onelarge subunit [146] The organization and spatial distributionexhibit a similarity to the E coliminimal 120574-complex but thefunction of the subunits is probably not conserved [145]

35 Maturation During DNA replication the lagging strandis discontinuously synthesized by extending the RNAprimersor Okazaki fragments This discontinuously synthesizedDNA strand requires maturation to form a single covalentlyclosed strand to end the replication process In ArchaeaOkazaki fragments were first demonstrated during replica-tion in P abyssi and Sulfolobus acidocaldarius [147] Duringreplication these RNA primers are replaced with DNA The

8 Archaea

removal of the primers is performed by the enzyme RNase Hwhich is ubiquitous in the three domains of life Accordingto their sequence similarity in prokaryotes the RNase Hproteins are classified into three groups RNase HI HII andHIII In eukaryotes they are classified as RNase H1 and H2[148] However phylogenetic analyses suggest that the RNaseH proteins can also be classified into two different groupsType 1 (prokaryotic RNaseHI eukaryotic RNaseH1 and viralRNase H) and Type 2 (prokaryotic RNase HII and HIII andeukaryotic RNase H2) [149] These two types of RNase Hpossess different specific activities metal ion preferences andcleavage sites [150] Originally it was thought that Archaeaonly possess type 2 RNase H [149] but several type 1 archaealRNase H enzymes have since then been discovered [151 152]Interestingly in eukaryotes RNaseH1 andH2 tend to coexistand different combinations of the three prokaryotic RNasesH(I II and III) are found except for the combination of RNasesHI and HIII This mutually exclusive evolution of some ofthe prokaryotic RNases seems to be related to functionalredundancy [148]

Another enzyme involved in primer replacement inDNA replication is the Flap endonuclease I (FEN-1) whichrecognizes double-strandedDNAwith an unannealed 51015840-flapand cleaves it A eukaryotic homolog of FEN-1 is found inevery archaeal member analyzed and one member of theThermoproteales Thermofilum pendens Hrk5 possesses twohomologs

M maripaludis S2 possesses genes for the prokaryoticRNase HI and HII and for FEN-1 but none are essentialsuggesting that they may be redundant in their functions[44 62] Possibly both RNase H proteins persist and areevolutionary stable in the genome The gene products mayperform the same function but one is less efficient than theother [153]

After the Okazaki fragments are replaced by DNA inthe lagging strand the nick between the newly synthesizedand the elongated DNA is repaired by a DNA ligase Thisenzyme uses a nucleotide cofactor to catalyze the formationof the phosphodiester bond in three well-characterized steps[154]The enzyme is common to all three domains but can begrouped into two families based on cofactor specificity (ATPor NAD+) The DNA ligases from several crenarchaeotes andeuryarchaeotes have been further characterized (reviewedin [43]) Many archaeal DNA ligases possess dual cofactorspecificity (ATPNAD+ or ATPADP) but every archaealDNA ligase characterized so far uses ATP A thermophilicDNA ligase from M thermautotrophicus which uses ATP assole cofactor was characterized in vitro [155] A characterizedDNA ligase from the crenarchaeote Sulfophobococcus zilligiidisplayed specificity for three cofactors (ATPNAD+GTP)[156]Major structuralwork in this enzymehas been achievedin P furiosus and S solfataricus and the findings have beenreviewed in detail [43] InM maripaludis S2 the DNA ligaseis likely to be essential for growth [44 62]

Understanding the maturation process in archaea hasbecome a focus of increasing research in recent years An invitro study reconstituted the Okazaki fragment maturationusing proteins derived from the crenarchaeote S solfataricusThey demonstrated that only six proteins are necessary for

coupled DNA synthesis RNA primer removal and DNAligation In this model a single PCNA (heterotrimeric ring)coordinates the activities of PolBI FEN-1 and DNA ligaseinto an efficient maturation complex [157] A different invitro study in P abyssi has demonstrated two different modelsfor Okazaki fragments maturation which differ in the RNAprimer removal process In the first model RNA primerelimination is executed by continuous PolD strand displace-ment DNA synthesis and 51015840RNA flap cleavage by FEN-1The resulting nicks are closed by DNA ligase Alternativelythe second model proposes that RNase HII cleaves theRNA primer followed by the action of FEN-1 and stranddisplacement DNA synthesis by polB or polD The nick isthen sealed by DNA ligase [127] Testing these models invivo is of great interest to complete the picture of how theseprocesses behave in the cell In addition other factors that canmodulate these processesmay be required for coordination ofthe in vivomaturation process

4 Conclusions

DNA replication in archaea possesses a dual nature wherethe machinery is structurally and functionally similar to theeukaryotic replication system but it is executed within abacterial context [11 25] Additionally unique archaeal fea-tures demonstrate the complexity of this process and it doesnot appear to be just a simplified version of the eukary-otic system For example the archaeal specific DNA poly-merase D is conserved across the Archaea domain with theexception of the Crenarchaeota phylumThe recent discoverythat it is the essential replicative polymerase in two differenteuryarchaeotic species demonstrates an unanticipated vari-ability in archaeal DNA replication and a fundamental differ-ence in the replication mechanism between crenarchaeotesand euryarchaeotes Interestingly the absence of PolD increnarchaeotes is not the only difference in DNA repli-cation These differences include the absence of histonesin crenarchaeotes [4] the presence of multiple origins ofreplication in crenarchaeotes and a single origin of repli-cation in most euryarchaeotes the absence of GINS23 inmost euryarchaeotes the absence of RPA protein in manycrenarchaeotes the presence of multiple MCM homologs inMethanococcales and the presence of one homolog of PCNAin euryarchaeotes compared to the multiple homologs increnarchaeotes These distinctive characteristics between thephyla highlight the complexity of archaeal DNA replicationand suggest a complex evolutionary history (Table 1)

Among the Euryarchaeota the ordersHalobacteriales andMethanococcales possess differences in the DNA replicationsystem that make them unique For instance Halobac-teriales possess many more origin recognition proteins(Orc1Cdc6) compared to the rest of the archaea On theother hand Methanococcales and Methanopyrales lack rec-ognizable homologs for the Orc1Cdc6 proteins suggestingthe presence of a very different mechanism for initiation ofreplication In addition the Methanococcales possess a largenumber of MCM protein homologs It has been proposedthat these distinctive features are connected and because ofthe absence of the Orc1Cdc6 proteins MCM proteins may

Archaea 9

Table1DNAreplicationproteins

andfeatures

inthed

omains

BacteriaEukaryotaand

thetwomajor

phylao

fthe

Archaeado

main

Mod

ified

from

[43]

DNAreplicationstage

Process

Bacteria

Eukaryota

Archaea

Crenarchaeota

Euryarchaeota

Preinitia

tion

Orig

inof

replication

Sing

leMultip

leMultip

leSing

lea

Orig

inrecogn

ition

DnaA

ORC

complex

(ORC

1-6)

Orc1C

dc6

Orc1C

dc6b

Initiation

DNAun

winding

(Helicase)

DnaB

MCM

complex

(MCM

2-7)

MCM

complex

MCM

complex

DNAun

winding

(Accessory

proteins)

DnaC

Cdc6

GIN

S23GIN

S15

GIN

S15c

Cdt1

GIN

Scomplex

(Sld5Psf1-3)

RecJho

molog

RecJho

molog

Cdc45

Prim

ersynthesis

DnaG

Pol120572

prim

asec

omplex

DNAprim

ase

(PriS

L)D

naG

dDNAprim

ase(PriSL)

Elon

gatio

n

DNAsynthesis

(polym

erase)

PolIII(Fam

ilyCDNApo

lymerase)

Pol120575and

Pol120576(Fam

ilyBDNA

polymerase)

Family

BDNApo

lymerase

Family

DDNA

polymerasee

DNAsynthesis

(Processivity

factors)

120574-com

plex

(clamploader)

RFC(clamploader)

RFC(clamploader)

RFC(clamploader)

120573-clamp(clamp)

PCNA(clamp)

PCNA(clamp)

PCNA(clamp)

Maturation

Maturation(O

kazaki

fragmentp

rocessing)

PolI

(family

ADNApo

lymerase)

Fen1D

na2

Fen1

Fen1

RNaseH

RNaseH

RNaseH

RNaseH

DNAligase

DNAligase

DNAligase

DNAligase

a Exceptio

ntheo

rder

Halobacteria

les

b Not

know

nform

embersof

theE

uryarchaeota

ordersMethanococcalesandMethanopyrales

c GIN

S23hasb

eenfoun

dedon

lyin

theo

rder

Thermococcales

oftheE

uryarchaeota

d Sulfolobu

ssolfataric

usdidshow

prim

asea

ctivity

invitro

e Fam

ilyBDNApo

lymeraseisa

lsoessentialinHalobacteriu

mB

ecause

itsfunctio

nhasn

otbeen

clearlyelu

cidateditmight

also

play

aroleinreplicationin

thisandclo

selyrelated

organism

s

10 Archaea

interact with other unknown initiation enzymes resultingin a complex phylogeny of the MCM homologs [49] Pre-sumably these differences also account for the inability torecognize the origin of replication in these microorganismsThis unique scenario for initiation of DNA replicationmay bea direct consequence of various processes such as duplicationmobile genetic elements and interactions with viruses [58]

The differences in DNA replication among archaealhigher taxa demonstrate an unexpected variability and sug-gest two alternative evolutionary models In the first modelDNA replication evolved late after the diversification ofthe archaeal lineages Because the replicative system wasnot fully formed it was possible to develop differentlybetween the lineages Once formed replication would thenbe highly conserved However this model is not consistentwith differences observed between lineages that must haveformed relatively late such as those between the orders oreven in some cases within certain orders The alternativemodel is that DNA replication has changed throughout theevolution of the archaea Thus differences in the replicativesystems may represent ancient as well as modern adaptationsto changing environments In this case differences in thereplicative systems may provide important insights into theevolutionary pressures in play during different episodes ofarchaeal evolution From this perspective the differencesbetween the eukaryotic and archaeal replicative systems maynot be evidence for an ancient origin of the eukaryotesInstead it is entirely plausible that the replicative system ineukaryotes could have evolved relatively late from a well-developed archaeal system

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] E F DeLong and N R Pace ldquoEnvironmental diversity ofbacteria and archaeardquo Systematic Biology vol 50 no 4 pp 470ndash478 2001

[2] B Chaban S Y M Ng and K F Jarrell ldquoArchaeal habitatsmdashfrom the extreme to the ordinaryrdquo Canadian Journal of Micro-biology vol 52 no 2 pp 73ndash116 2006

[3] M J Hanford and T L Peeples ldquoArchaeal tetraether lipidsunique structures and applicationsrdquo Applied Biochemistry andBiotechnology A vol 97 no 1 pp 45ndash62 2002

[4] K Sandman and J N Reeve ldquoArchaeal histones and the originof the histone foldrdquo Current Opinion in Microbiology vol 9 no5 pp 520ndash525 2006

[5] O Lecompte R Ripp J-C Thierry D Moras and O PochldquoComparative analysis of ribosomal proteins in complete gen-omes an example of reductive evolution at the domain scalerdquoNucleic Acids Research vol 30 no 24 pp 5382ndash5390 2002

[6] D R Edgell and W F Doolittle ldquoArchaea and the origin(s) ofDNA rplication poteinsrdquo Cell vol 89 no 7 pp 995ndash998 1997

[7] E R Barry and S D Bell ldquoDNA replication in the archaeardquoMicrobiology and Molecular Biology Reviews vol 70 no 4 pp876ndash887 2006

[8] S Gribaldo and C Brochier-Armanet ldquoThe origin and evolu-tion of archaea a state of the artrdquo Philosophical Transactions ofthe Royal Society B vol 361 no 1470 pp 1007ndash1022 2006

[9] P Londei ldquoEvolution of translational initiation new insightsfrom the archaeardquo FEMS Microbiology Reviews vol 29 no 2pp 185ndash200 2005

[10] B Grabowski and Z Kelman ldquoArchaeal DNA replicationeukaryal proteins in a bacterial contextrdquo Annual Review ofMicrobiology vol 57 pp 487ndash516 2003

[11] P Forterre J Filee and H Myllykallio ldquoOrigin and evolutionof DNA and DNA replication machineriesrdquo in The GeneticCode and the Origin of Life L Ribas Ed Landes BioscienceGeorgetown Tex USA 2007

[12] E V Koonin ldquoThe origin and early evolution of eukaryotesin the light of phylogenomicsrdquo Genome Biology vol 11 no 5article 209 2010

[13] M Konneke A E Bernhard J R de la Torre C B WalkerJ B Waterbury and D A Stahl ldquoIsolation of an autotrophicammonia-oxidizing marine archaeonrdquo Nature vol 437 no7058 pp 543ndash546 2005

[14] C Brochier-Armanet B Boussau S Gribaldo and P ForterreldquoMesophilic crenarchaeota proposal for a third archaeal phy-lum theThaumarchaeotardquoNature Reviews Microbiology vol 6no 3 pp 245ndash252 2008

[15] J G Elkins M Podar D E Graham et al ldquoA korarchaealgenome reveals insights into the evolution of the ArchaeardquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 105 no 23 pp 8102ndash8107 2008

[16] T Nunoura Y Takaki J Kakuta et al ldquoInsights into theevolution of Archaea and eukaryotic protein modifier systemsrevealed by the genome of a novel archaeal grouprdquoNucleic AcidsResearch vol 39 no 8 pp 3204ndash3223 2011

[17] HHuberM J Hohn R Rachel T Fuchs V CWimmer andKO Stetter ldquoAnewphylumofArchaea represented by a nanosizedhyperthermophilic symbiontrdquoNature vol 417 no 6884 pp 63ndash67 2002

[18] C Brochier S Gribaldo Y Zivanovic F Confalonieri and PForterre ldquoNanoarchaea representatives of a novel archaeal phy-lum or a fast-evolving euryarchaeal lineage related to Therm-ococcalesrdquo Genome Biology vol 6 no 5 article R42 2005

[19] S J Aves ldquoDNA replication initiationrdquo Methods in MolecularBiology vol 521 pp 3ndash17 2009

[20] N P Robinson I Dionne M Lundgren V L Marsh RBernander and S D Bell ldquoIdentification of two origins ofreplication in the single chromosome of the archaeon Sulfolobussolfataricusrdquo Cell vol 116 no 1 pp 25ndash38 2004

[21] M Lundgren A Andersson L Chen P Nilsson and RBernander ldquoThree replication origins in Sulfolobus speciessynchronous initiation of chromosome replication and asyn-chronous terminationrdquo Proceedings of the National Academy ofSciences of theUnited States of America vol 101 no 18 pp 7046ndash7051 2004

[22] N P Robinson and S D Bell ldquoExtrachromosomal element cap-ture and the evolution ofmultiple replication origins in archaealchromosomesrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 104 no 14 pp 5806ndash58112007

[23] E A Pelve A C Lindas A Knoppel A Mira and R Bernan-der ldquoFour chromosome replication origins in the archaeonPyrobaculum calidifontisrdquo Molecular Microbiology vol 85 no5 pp 986ndash995 2012

Archaea 11

[24] A F Andersson E A Pelve S LindebergM Lundgren P Nils-son and R Bernander ldquoReplication-biased genome organisa-tion in the crenarchaeon Sulfolobusrdquo BMCGenomics vol 11 no1 article 454 2010

[25] H Myllykallio P Lopez P Lopez-Garcıa et al ldquoBacterial modeof replication with eukaryotic-like machinery in a hyperther-mophilic archaeonrdquo Science vol 288 no 5474 pp 2212ndash22152000

[26] F Matsunaga P Forterre Y Ishino and H Myllykallio ldquoInvivo interactions of archaeal Cdc6Orc1 and minichromosomemaintenance proteins with the replication originrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 98 no 20 pp 11152ndash11157 2001

[27] S Maisnier-Patin L Malandrin N K Birkeland and RBernander ldquoChromosome replication patterns in the hyper-thermophilic euryarchaeaArchaeoglobus fulgidus andMethano-caldococcus (Methanococcus) jannaschiirdquo Molecular Microbiol-ogy vol 45 no 5 pp 1443ndash1450 2002

[28] R Zhang and C-T Zhang ldquoMultiple replication origins ofthe archaeon Halobacterium species NRC-1rdquo Biochemical andBiophysical Research Communications vol 302 no 4 pp 728ndash734 2003

[29] C Norais M Hawkins A L Hartman J A Eisen H Myl-lykallio and T Allers ldquoGenetic and physical mapping of DNAreplication origins in Haloferax volcaniirdquo PLoS Genetics vol 3no 5 article e77 2007

[30] J A Coker P DasSarma M Capes et al ldquoMultiple replicationorigins of Halobacterium sp strain NRC-1 properties of theconserved orc7-dependent oriC1rdquo Journal of Bacteriology vol191 no 16 pp 5253ndash5261 2009

[31] Z Wu J Liu H Yang H Liu and H Xiang ldquoMultiple repli-cation origins with diverse control mechanisms in Haloarculahispanicardquo Nucleic Acids Research 2013

[32] M Hawkins S Malla M J Blythe C A Nieduszynski and TAllers ldquoAccelerated growth in the absence of DNA replicationoriginsrdquo Nature vol 503 no 7477 pp 544ndash547 2013

[33] A I Majernık and J P J Chong ldquoA conserved mechanismfor replication origin recognition and binding in archaeardquo TheBiochemical Journal vol 409 no 2 pp 511ndash518 2008

[34] J E Galagan C Nusbaum A Roy et al ldquoThe genome of Macetivorans reveals extensive metabolic and physiological diver-sityrdquo Genome Research vol 12 no 4 pp 532ndash542 2002

[35] R Zhang and C-T Zhang ldquoIdentification of replication originsin archaeal genomes based on the Z-curve methodrdquo Archaeavol 1 no 5 pp 335ndash346 2005

[36] A Spang R Hatzenpichler C Brochier-Armanet et al ldquoDis-tinct gene set in two different lineages of ammonia-oxidizingarchaea supports the phylum Thaumarchaeotardquo Trends inMicrobiology vol 18 no 8 pp 331ndash340 2010

[37] K J Marians ldquoProkaryotic DNA replicationrdquo Annual Review ofBiochemistry vol 61 pp 673ndash719 1992

[38] S P Bell ldquoThe origin recognition complex from simple originsto complex functionsrdquo Genes and Development vol 16 no 6pp 659ndash672 2002

[39] V L Marsh and S D Bell ldquoDNA replication and the cell cyclerdquoin Archaea Evolution Physiology and Molecular Biology R AGarrett and H P Klenk Eds Blackwell Publishing HobokenNJ USA 2007

[40] F Matsunaga A Glatigny M-H Mucchielli-Giorgi et alldquoGenomewide and biochemical analyses of DNA-binding activ-ity of Cdc6Orc1 and Mcm proteins in Pyrococcus sprdquo NucleicAcids Research vol 35 no 10 pp 3214ndash3222 2007

[41] J Liu C L Smith D DeRyckere K DeAngelis G S Martinand J M Berger ldquoStructure and function of Cdc6Cdc18implications for origin recognition and checkpoint controlrdquoMolecular Cell vol 6 no 3 pp 637ndash648 2000

[42] M R Singleton R Morales I Grainge N Cook M NIsupov and D B Wigley ldquoConformational changes inducedby nucleotide binding in Cdc6ORC from Aeropyrum pernixrdquoJournal of Molecular Biology vol 343 no 3 pp 547ndash557 2004

[43] Y Ishino and S Ishino ldquoRapid progress of DNA replicationstudies in Archaea the third domain of liferdquo Science China LifeSciences vol 55 no 5 pp 386ndash403 2012

[44] E L Hendrickson R Kaul Y Zhou et al ldquoComplete genomesequence of the genetically tractable hydrogenotrophic meth-anogen Methanococcus maripaludisrdquo Journal of Bacteriologyvol 186 no 20 pp 6956ndash6969 2004

[45] B K Tye ldquoMCM proteins in DNA replicationrdquo Annual Reviewof Biochemistry vol 68 pp 649ndash686 1999

[46] K Labib and J F X Diffley ldquoIs the MCM2-7 complex theeukaryotic DNA replication fork helicaserdquo Current Opinion inGenetics amp Development vol 11 no 1 pp 64ndash70 2001

[47] I Ilves T Petojevic J J Pesavento and M R Botchan ldquoActi-vation of the MCM2-7 helicase by association with Cdc45 andGINS proteinsrdquoMolecular Cell vol 37 no 2 pp 247ndash258 2010

[48] M L Bochman andA Schwacha ldquoTheMcm complex unwind-ing the mechanism of a replicative helicaserdquo Microbiology andMolecular Biology Reviews vol 73 no 4 pp 652ndash683 2009

[49] Y Ishimi ldquoADNAhelicase activity is associated with anMCM4-6 and -7 protein complexrdquoThe Journal of Biological Chemistryvol 272 no 39 pp 24508ndash24513 1997

[50] Z Kelman and M F White ldquoArchaeal DNA replication andrepairrdquo Current Opinion in Microbiology vol 8 no 6 pp 669ndash676 2005

[51] J H LeBowitz and R McMacken ldquoThe Escherichia coli dnaBreplication protein is a DNA helicaserdquoThe Journal of BiologicalChemistry vol 261 no 10 pp 4738ndash4748 1986

[52] Z Kelman J-K Lee and J Hurwitz ldquoThe single minichro-mosome maintenance protein ofMethanobacterium thermoau-totrophicum ΔH contains DNA helicase activityrdquo Proceedings ofthe National Academy of Sciences of the United States of Americavol 96 no 26 pp 14783ndash14788 1999

[53] D F Shechter C Y Ying and J Gautier ldquoThe intrinsic DNAhelicase activity of Methanobacterium thermoautotrophicumΔH minichromosome maintenance proteinrdquo The Journal ofBiological Chemistry vol 275 no 20 pp 15049ndash15059 2000

[54] M de Felice L Esposito B Pucci M de Falco M Rossi andF M Pisani ldquoA CDC6-like factor from the archaea Sulfolobussolfataricus promotes binding of the mini-chromosome main-tenance complex to DNArdquoThe Journal of Biological Chemistryvol 279 no 41 pp 43008ndash43012 2004

[55] R Kasiviswanathan J-H Shin and Z Kelman ldquoInteractionsbetween the archaeal Cdc6 and MCM proteins modulate theirbiochemical propertiesrdquo Nucleic Acids Research vol 33 no 15pp 4940ndash4950 2005

[56] J-H Shin B Grabowski R Kasiviswanathan S D Bell andZ Kelman ldquoRegulation of minichromosomemaintenance heli-case activity by Cdc6rdquo The Journal of Biological Chemistry vol278 no 39 pp 38059ndash38067 2003

[57] M Akita A Adachi K Takemura T Yamagami F Matsunagaand Y Ishino ldquoCdc6Orc1 from Pyrococcus furiosus may actas the origin recognition protein and Mcm helicase recruiterrdquoGenes to Cells vol 15 no 5 pp 537ndash552 2010

12 Archaea

[58] M Krupovic S Gribaldo D H Bamford and P Forterre ldquoTheevolutionary history of archaeal MCM helicases a case study ofvertical evolution combined with hitchhiking of mobile geneticelementsrdquo Molecular Biology and Evolution vol 27 no 12 pp2716ndash2732 2010

[59] ADWalters and J P J Chong ldquoAn archaeal orderwithmultipleminichromosome maintenance genesrdquo Microbiology vol 156part 5 pp 1405ndash1414 2010

[60] A DWalters and J P J Chong ldquoMethanococcusmaripaludis anarchaeon with multiple functional MCM proteinsrdquo Biochemi-cal Society Transactions vol 37 no 1 pp 1ndash6 2009

[61] Q Xia E L Hendrickson Y Zhang et al ldquoQuantitative pro-teomics of the archaeon Methanococcus maripaludis validatedbymicroarray analysis and real time PCRrdquoMolecularampCellularProteomics vol 5 no 5 pp 868ndash881 2006

[62] F Sarmiento J Mrazek and W B Whitman ldquoGenome-scaleanalysis of gene function in the hydrogenotrophic methano-genic archaeon Methanococcus maripaludisrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 110 no 12 pp 4726ndash4731 2013

[63] M Pan T J Santangelo Z Li J N Reeve and Z KelmanldquoThermococcus kodakarensis encodes threeMCMhomologs butonly one is essentialrdquo Nucleic Acids Research vol 39 no 22 pp9671ndash9680 2011

[64] S Ishino S Fujino H Tomita et al ldquoBiochemical and geneticalanalyses of the three mcm genes from the hyperthermophilicarchaeon Thermococcus kodakarensisrdquo Genes to Cells vol 16no 12 pp 1176ndash1189 2011

[65] K S Makarova Y I Wolf S L Mekhedov B G Mirkin and EV Koonin ldquoAncestral paralogs and pseudoparalogs and theirrole in the emergence of the eukaryotic cellrdquo Nucleic AcidsResearch vol 33 no 14 pp 4626ndash4638 2005

[66] N Marinsek E R Barry K S Makarova I Dionne E VKoonin and S D Bell ldquoGINS a central nexus in the archaealDNA replication forkrdquo EMBOReports vol 7 no 5 pp 539ndash5452006

[67] T Yoshimochi R Fujikane M Kawanami F Matsunaga and YIshino ldquoTheGINS complex from Pyrococcus furiosus stimulatesthe MCM helicase activityrdquoThe Journal of Biological Chemistryvol 283 no 3 pp 1601ndash1609 2008

[68] T Oyama S Ishino S Fujino et al ldquoArchitectures of archaealGINS complexes essential DNA replication initiation factorsrdquoBMC Biology vol 9 article 28 2011

[69] H Ogino S Ishino K Mayanagi et al ldquoThe GINS com-plex from the thermophilic archaeon Thermoplasma aci-dophilummay function as a homotetramer inDNA replicationrdquoExtremophiles vol 15 no 4 pp 529ndash539 2011

[70] L Sanchez-Pulido and C P Ponting ldquoCdc45 the missing recjortholog in eukaryotesrdquoBioinformatics vol 27 no 14 pp 1885ndash1888 2011

[71] Z Li T J Santangelo L Cubonova J N Reeve and Z KelmanldquoAffinity purification of an archaeal DNA replication proteinnetworkrdquomBio vol 1 no 5 2010

[72] Z Li M Pan T J Santangelo et al ldquoA novel DNA nucleaseis stimulated by association with the GINS complexrdquo NucleicAcids Research vol 39 no 14 pp 6114ndash6123 2011

[73] L A Rajman and S T Lovett ldquoA thermostable single-strandDNase from Methanococcus jannaschii related to the RecJrecombination and repair exonuclease from Escherichia colirdquoJournal of Bacteriology vol 182 no 3 pp 607ndash612 2000

[74] K RWilliams J B Murphy and JW Chase ldquoCharacterizationof the structural and functional defect in the Escherichia colisingle-stranded DNA binding protein encoded by the ssb-1 mutant gene Expression of the ssb-1 gene under 120582p(L)regulationrdquoThe Journal of Biological Chemistry vol 259 no 19pp 11804ndash11811 1984

[75] S Dąbrowski M Olszewski R Pitek and J Kur ldquoNovel ther-mostable ssDNA-binding proteins fromThermus thermophilusand T aquaticus-expression and purificationrdquo Protein Expres-sion and Purification vol 26 no 1 pp 131ndash138 2002

[76] C Iftode Y Daniely and J A Borowiec ldquoReplication proteinA (RPA) the eukaryotic SSBrdquo Critical Reviews in Biochemistryand Molecular Biology vol 34 no 3 pp 141ndash180 1999

[77] A G Murzin ldquoOB(oligonucleotideoligosaccharide binding)-fold common structural and functional solution for non-hom-ologous sequencesrdquo The EMBO Journal vol 12 no 3 pp 861ndash867 1993

[78] C A Haseltine and S C Kowalczykowski ldquoA distinctive single-stranded DNA-binding protein from the Archaeon Sulfolobussolfataricusrdquo Molecular Microbiology vol 43 no 6 pp 1505ndash1515 2002

[79] R I M Wadsworth and M F White ldquoIdentification and pro-perties of the crenarchaeal single-stranded DNA binding pro-tein from Sulfolobus solfataricusrdquoNucleic Acids Research vol 29no 4 pp 914ndash920 2001

[80] I D Kerr R I M Wadsworth L Cubeddu W Blankenfeldt JHNaismith andM FWhite ldquoInsights into ssDNA recognitionby the OB fold from a structural and thermodynamic study ofSulfolobus SSB proteinrdquo The EMBO Journal vol 22 no 11 pp2561ndash2570 2003

[81] X Luo U Schwarz-Linek C H Botting R Hensel B Siebersand M F White ldquoCC1 a novel crenarchaeal DNA binding pro-teinrdquo Journal of Bacteriology vol 189 no 2 pp 403ndash409 2007

[82] T J Kelly P Simancek and G S Brush ldquoIdentification andcharacterization of a single-stranded DNA-binding proteinfrom the archaeonMethanococcus jannaschiirdquoProceedings of theNational Academy of Sciences of theUnited States of America vol95 no 25 pp 14634ndash14639 1998

[83] Z Kelman S Pietrokovski and J Hurwitz ldquoIsolation and cha-racterization of a split B-type DNA polymerase from the arch-aeonMethanobacterium thermoautotrophicumΔHrdquoTheJournalof Biological Chemistry vol 274 no 40 pp 28751ndash28761 1999

[84] K Komori and Y Ishino ldquoReplication protein A in Pyrococcusfuriosus is involved in homologous DNA recombinationrdquo TheJournal of Biological Chemistry vol 276 no 28 pp 25654ndash25660 2001

[85] J B Robbins M C Murphy B A White R I Mackie THa and I K O Cann ldquoFunctional analysis of multiple single-stranded DNA-binding proteins from Methanosarcina acetivo-rans and their effects on DNA synthesis by DNA polymeraseBIrdquoThe Journal of Biological Chemistry vol 279 no 8 pp 6315ndash6326 2004

[86] Y Lin L-J Lin P Sriratana et al ldquoEngineering of functionalreplication protein a homologs based on insights into the evolu-tion of oligonucleotideoligosaccharide-binding foldsrdquo Journalof Bacteriology vol 190 no 17 pp 5766ndash5780 2008

[87] D N Frick and C C Richardson ldquoDNA primasesrdquo AnnualReview of Biochemistry vol 70 pp 39ndash80 2001

[88] G Desogus S Onesti P Brick M Rossi and F M PisanildquoIdentification and characterization of a DNA primase fromthe hyperthermophilic archaeon Methanococcus jannaschiirdquoNucleic Acids Research vol 27 no 22 pp 4444ndash4450 1999

Archaea 13

[89] A A Bocquier L Liu I K O Cann K Komori D Kohda andY Ishino ldquoArchaeal primase bridging the gap between RNAand DNA polymerasesrdquo Current Biology vol 11 no 6 pp 452ndash456 2001

[90] L Liu K Komori S Ishino et al ldquoThe archaeal DNA primasebiochemical characterization of the p41-p46 complex fromPyrococcus furiosusrdquo The Journal of Biological Chemistry vol276 no 48 pp 45484ndash45490 2001

[91] E Matsui M Nishio H Yokoyama K Harata S Darnisand I Matsui ldquoDistinct domain functions regulating de novoDNA synthesis of thermostable DNA primase from hyperther-mophile Pyrococcus horikoshiirdquo Biochemistry vol 42 no 50 pp14968ndash14976 2003

[92] N Ito I Matsui and EMatsui ldquoMolecular basis for the subunitassembly of the primase from an archaeon Pyrococcus hori-koshiirdquoThe FEBS Journal vol 274 no 5 pp 1340ndash1351 2007

[93] M le Breton G Henneke C Norais et al ldquoThe heterodimericprimase from the euryarchaeon Pyrococcus abyssi a multifunc-tional enzyme for initiation and repairrdquo Journal of MolecularBiology vol 374 no 5 pp 1172ndash1185 2007

[94] S-H Lao-Sirieix and S D Bell ldquoThe heterodimeric primaseof the hyperthermophilic archaeon Sulfolobus solfataricus pos-sesses DNA and RNA primase polymerase and 31015840-terminalnucleotidyl transferase activitiesrdquo Journal of Molecular Biologyvol 344 no 5 pp 1251ndash1263 2004

[95] S-H Lao-Sirieix L Pellegrini and S D Bell ldquoThe promiscuousprimaserdquo Trends in Genetics vol 21 no 10 pp 568ndash572 2005

[96] J Hu L Guo K Wu B Liu S Lang and L Huang ldquoTemplate-dependent polymerization across discontinuous templatesby the heterodimeric primase from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquoNucleic Acids Research vol 40no 8 pp 3470ndash3483 2012

[97] E Evguenieva-Hackenberg P Walter E Hochleitner FLottspeich and G Klug ldquoAn exosome-like complex in Sulfolo-bus solfataricusrdquo EMBOReports vol 4 no 9 pp 889ndash893 2003

[98] P Walter F Klein E Lorentzen A Ilchmann G Klug andE Evguenieva-Hackenberg ldquoCharacterization of native andreconstituted exosome complexes from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Microbiology vol62 no 4 pp 1076ndash1089 2006

[99] Z Zuo C J Rodgers A L Mikheikin and M A Trak-selis ldquoCharacterization of a functional DnaG-type primase inarchaea implications for a dual-primase systemrdquo Journal ofMolecular Biology vol 397 no 3 pp 664ndash676 2010

[100] B R Berquist P DasSarma and S DasSarma ldquoEssential andnon-essential DNA replication genes in the model halophilicArchaeon Halobacterium sp NRC-1rdquo BMC Genetics vol 8article 31 2007

[101] D K Braithwaite and J Ito ldquoCompilation alignment andphylogenetic relationships of DNA polymerasesrdquo Nucleic AcidsResearch vol 21 no 4 pp 787ndash802 1993

[102] I K O Cann and Y Ishino ldquoArchaeal DNA replication iden-tifying the pieces to solve a puzzlerdquo Genetics vol 152 no 4 pp1249ndash1267 1999

[103] G Lipps S Rother C Hart and G Krauss ldquoA novel typeof replicative enzyme harbouring ATpase primase and DNApolymerase activityrdquo The EMBO Journal vol 22 no 10 pp2516ndash2525 2003

[104] J Yamtich and J B Sweasy ldquoDNA polymerase family X func-tion structure and cellular rolesrdquoBiochimica et BiophysicaActavol 1804 no 5 pp 1136ndash1150 2010

[105] H Ohmori E C Friedberg R P P Fuchs et al ldquoThe Y-familyof DNA polymerasesrdquoMolecular Cell vol 8 no 1 pp 7ndash8 2001

[106] N Y Yao R E Georgescu J Finkelstein and M E OrsquoDonnellldquoSingle-molecule analysis reveals that the lagging strandincreases replisome processivity but slows replication forkprogressionrdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 106 no 32 pp 13236ndash132412009

[107] U Hubscher G Maga and S Spadari ldquoEukaryotic DNA poly-merasesrdquo Annual Review of Biochemistry vol 71 pp 133ndash1632002

[108] F Boudsocq S Iwai F Hanaoka and R Woodgate ldquoSulfolobussolfataricus P2 DNA polymerase IV (Dp04) an archaeal DinB-like DNA polymerase with lesion-bypass properties akin toeukaryotic pol120578rdquo Nucleic Acids Research vol 29 no 22 pp4607ndash4616 2001

[109] L-J Lin A Yoshinaga Y Lin et al ldquoMolecular analyses ofan unusual translesion DNA polymerase fromMethanosarcinaacetivorans C2Ardquo Journal of Molecular Biology vol 397 no 1pp 13ndash30 2010

[110] I K O Cann S Ishino NNomura Y Sako andY Ishino ldquoTwofamily B DNA polymerases from Aeropyrum pernix an aerobichyperthermophilic crenarchaeoterdquo Journal of Bacteriology vol181 no 19 pp 5984ndash5992 1999

[111] T Uemori Y Ishino H Doi and I Kato ldquoThe hyperther-mophilic archaeon Pyrodictium occultum has two 120572-like DNApolymerasesrdquo Journal of Bacteriology vol 177 no 8 pp 2164ndash2177 1995

[112] T Uemori Y Ishino H Toh K Asada and I Kato ldquoOrgani-zation and nucleotide sequence of the DNA polymerase genefrom the archaeon Pyrococcus furiosusrdquo Nucleic Acids Researchvol 21 no 2 pp 259ndash265 1993

[113] B A Connolly ldquoRecognition of deaminated bases by archaealfamily-B DNA polymerasesrdquo Biochemical Society Transactionsvol 37 no 1 pp 65ndash68 2009

[114] B A Connolly M J Fogg G Shuttleworth and B T WilsonldquoUracil recognition by archaeal family B DNA polymerasesrdquoBiochemical Society Transactions vol 31 no 3 pp 699ndash7022003

[115] T T Richardson X Wu B J Keith P Heslop A C Jones andB A Connolly ldquoUnwinding of primer-templates by archaealfamily-B DNA polymerases in response to template-stranduracilrdquo Nucleic Acids Research vol 41 no 4 pp 2466ndash24782013

[116] T Lindahl ldquoInstability and decay of the primary structure ofDNArdquo Nature vol 362 no 6422 pp 709ndash715 1993

[117] I B Rogozin K S Makarova Y I Pavlov and E V Koonin ldquoAhighly conserved family of inactivated archaeal B family DNApolymerasesrdquo Biology Direct vol 3 article 32 2008

[118] M Imamura T Uemori I Kato and Y Ishino ldquoA non-120572-like DNA polymerase from the hyperthermophilic archaeonPyrococcus furiosusrdquoBiological andPharmaceutical Bulletin vol18 no 12 pp 1647ndash1652 1995

[119] I K O Cann K Komori H Toh S Kanai and Y IshinoldquoA heterodimeric DNA polymerase evidence that members ofEuryarchaeota possess a distinct DNA polymeraserdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 95 no 24 pp 14250ndash14255 1998

[120] L Aravind D D Leipe and E V Koonin ldquoToprimmdasha con-served catalytic domain in type IA and II topoisomerases

14 Archaea

DnaG-type primases OLD family nucleases and RecR pro-teinsrdquo Nucleic Acids Research vol 26 no 18 pp 4205ndash42131998

[121] M Jokela A Eskelinen H Pospiech J Rouvinen and J ESyvaoja ldquoCharacterization of the 31015840 exonuclease subunit DP1of Methanococcus jannaschii replicative DNA polymerase DrdquoNucleic Acids Research vol 32 no 8 pp 2430ndash2440 2004

[122] T Uemori Y Sato I Kato H Doi and Y Ishino ldquoA novel DNApolymerase in the hyperthermophilic archaeon Pyrococcus fur-iosus gene cloning expression and characterizationrdquo Genes toCells vol 2 no 8 pp 499ndash512 1997

[123] Y Shen K Musti M Hiramoto H Kikuchi Y Kawarabayashiand I Matsui ldquoInvariant Asp-1122 and Asp-1124 are essentialresidues for polymerization catalysis of family D DNA poly-merase from Pyrococcus horikoshiirdquo The Journal of BiologicalChemistry vol 276 no 29 pp 27376ndash27383 2001

[124] G Henneke D Flament U Hubscher J Querellou and J-P Raffin ldquoThe hyperthermophilic euryarchaeota Pyrococcusabyssi likely requires the two DNA polymerases D and B forDNA replicationrdquo Journal of Molecular Biology vol 350 no 1pp 53ndash64 2005

[125] L Cubonova T Richardson B W Burkhart et al ldquoArchaealDNA polymerase D but not DNA polymerase B is required forgenome replication in Thermococcus kodakarensisrdquo Journal ofBacteriology vol 195 no 10 pp 2322ndash2328 2013

[126] C Rouillon G Henneke D Flament J Querellou and J-PRaffin ldquoDNA polymerase switching on homotrimeric PCNA atthe replication fork of the euryarchaea Pyrococcus abyssirdquo Jour-nal of Molecular Biology vol 369 no 2 pp 343ndash355 2007

[127] G Henneke ldquoIn vitro reconstitution of RNA primer removal inArchaea reveals the existence of two pathwaysrdquoTheBiochemicalJournal vol 447 no 2 pp 271ndash280 2012

[128] G-LMoldovan B Pfander and S Jentsch ldquoPCNA themaestroof the replication forkrdquo Cell vol 129 no 4 pp 665ndash679 2007

[129] X-P Kong R Onrust M OrsquoDonnell and J Kuriyan ldquoThree-dimensional structure of the 120573 subunit of E coli DNA poly-merase III holoenzyme a sliding DNA clamprdquo Cell vol 69 no3 pp 425ndash437 1992

[130] K Daimon Y Kawarabayasi H Kikuchi Y Sako and Y IshinoldquoThree proliferating cell nuclear antigen-like proteins foundin the hyperthermophilic archaeon Aeropyrum pemix interac-tions with the two DNA polymerasesrdquo Journal of Bacteriologyvol 184 no 3 pp 687ndash694 2002

[131] I Dionne R K Nookala S P Jackson A J Doherty andS D Bell ldquoA heterotrimeric PCNA in the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Cell vol 11 no 1pp 275ndash282 2003

[132] E Warbrick ldquoPCNA binding through a conserved motifrdquoBioEssays vol 20 no 3 pp 195ndash199 1998

[133] H Nishida K Mayanagi S Kiyonari et al ldquoStructural deter-minant for switching between the polymerase and exonucleasemodes in the PCNA-replicative DNA polymerase complexrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 106 no 49 pp 20693ndash20698 2009

[134] K Mayanagi S Kiyonari H Nishida et al ldquoArchitecture of theDNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complexrdquo Proceedings of the National Academy ofSciences of the United States of America vol 108 no 5 pp 1845ndash1849 2011

[135] B Castrec C Rouillon G Henneke D Flament J Querellouand J-P Raffin ldquoBinding to PCNA in Euryarchaeal DNA

replication requires two PIP motifs for DNA polymerase D andone PIP motif for DNA polymerase Brdquo Journal of MolecularBiology vol 394 no 2 pp 209ndash218 2009

[136] P F Pluchon T Fouqueau C Creze et al ldquoAn extendednetworkof genomic maintenance in the archaeon Pyrococcus abyssihighlights unexpected associations between eucaryotic homo-logsrdquo PLoS One vol 8 no 11 Article ID e79707 2013

[137] J E Ladner M Pan J Hurwitz and Z Kelman ldquoCrystalstructures of two active proliferating cell nuclear antigens(PCNAs) encoded byThermococcus kodakaraensisrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2711ndash2716 2011

[138] Y Kuba S Ishino T Yamagami et al ldquoComparative analyses ofthe two proliferating cell nuclear antigens from the hyperther-mophilic archaeonThermococcus kodakarensisrdquo Genes to Cellsvol 17 no 11 pp 923ndash937 2012

[139] T Fukui H Atomi T Kanai R Matsumi S Fujiwara andT Imanaka ldquoComplete genome sequence of the hyperther-mophilic archaeon Thermococcus kodakaraensis KOD1 andcomparison with Pyrococcus genomesrdquo Genome Research vol15 no 3 pp 352ndash363 2005

[140] D Jeruzalmi O Yurieva Y Zhao et al ldquoMechanism of proces-sivity clamp opening by the delta subunit wrench of the clamploader complex of E coliDNApolymerase IIIrdquoCell vol 106 no4 pp 417ndash428 2001

[141] Y Shiomi J Usukura Y Masamura et al ldquoATP-dependentstructural change of the eukaryotic clamp-loader protein repli-cation factor Crdquo Proceedings of the National Academy of Sciencesof the United States of America vol 97 no 26 pp 14127ndash141322000

[142] T Miyata T Oyama K Mayanagi S Ishino Y Ishino and KMorikawa ldquoThe clamp-loading complex for processive DNAreplicationrdquoNature Structural andMolecular Biology vol 11 no7 pp 632ndash636 2004

[143] T Oyama Y Ishino I K O Cann S Ishino and K MorikawaldquoAtomic structure of the clamp loader small subunit fromPyrococcus furiosusrdquo Molecular Cell vol 8 no 2 pp 455ndash4632001

[144] A Seybert D J Scott S Scaife M R Singleton and DB Wigley ldquoBiochemical characterisation of the clampclamploader proteins from the euryarchaeon Archaeoglobus fulgidusrdquoNucleic Acids Research vol 30 no 20 pp 4329ndash4338 2002

[145] Y-H Chen Y Lin A Yoshinaga et al ldquoMolecular analyses of athree-subunit euryarchaeal clamp loader complex from Meth-anosarcina acetivoransrdquo Journal of Bacteriology vol 191 no 21pp 6539ndash6549 2009

[146] Y-H Chen S A Kocherginskaya Y Lin et al ldquoBiochemicaland mutational analyses of a unique clamp loader complex inthe archaeon Methanosarcina acetivoransrdquo The Journal of Bio-logical Chemistry vol 280 no 51 pp 41852ndash41863 2005

[147] F Matsunaga C Norais P Forterre and H Myllykallio ldquoIden-tification of short ldquoeukaryoticrdquo Okazaki fragments synthesizedfrom a prokaryotic replication originrdquo EMBO Reports vol 4no 2 pp 154ndash158 2003

[148] H Kochiwa M Tomita and A Kanai ldquoEvolution of ribonucle-ase H genes in prokaryotes to avoid inheritance of redundantgenesrdquo BMC Evolutionary Biology vol 7 article 128 2007

[149] N OhtaniMHarukiMMorikawa and S Kanaya ldquoMoleculardiversities of RNases Hrdquo Journal of Bioscience and Bioengineer-ing vol 88 no 1 pp 12ndash19 1999

Archaea 15

[150] N Ohtani M Haruki M Morikawa R J Crouch M Itayaand S Kanaya ldquoIdentification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII fromBacillus subtilis classification of RNases H into three familiesrdquoBiochemistry vol 38 no 2 pp 605ndash618 1999

[151] N Ohtani H Yanagawa M Tomita and M Itaya ldquoIdentifi-cation of the first archaeal type 1 RNase H gene from Halobac-terium sp NRC-1 archaeal RNase HI can cleave an RNA-DNAjunctionrdquoThe Biochemical Journal vol 381 no 3 pp 795ndash8022004

[152] N Ohtani H Yanagawa M Tomita and M Itaya ldquoCleavage ofdouble-stranded RNA by RNase HI from a thermoacidophilicarchaeon Sulfolobus tokodaii 7rdquo Nucleic Acids Research vol 32no 19 pp 5809ndash5819 2004

[153] M A Nowak M C Boerlijst J Cooke and J M SmithldquoEvolution of genetic redundancyrdquo Nature vol 388 no 6638pp 167ndash170 1997

[154] A E Tomkinson S Vijayakumar J M Pascal and T Ellen-berger ldquoDNA ligases structure reactionmechanism and func-tionrdquo Chemical Reviews vol 106 no 2 pp 687ndash699 2006

[155] M Nakatani S Ezaki H Atomi and T Imanaka ldquoA DNAligase from a hyperthermophilic archaeon with unique cofactorspecificityrdquo Journal of Bacteriology vol 182 no 22 pp 6424ndash6433 2000

[156] Y Sun M S Seo J H Kim et al ldquoNovel DNA ligase with broadnucleotide cofactor specificity from the hyperthermophilic cre-narchaeon Sulfophobococcus zilligii influence of ancestral DNAligase on cofactor utilizationrdquo Environmental Microbiology vol10 no 12 pp 3212ndash3224 2008

[157] T R Beattie and S D Bell ldquoCoordination of multiple enzymeactivities by a single PCNA in archaeal Okazaki fragmentmaturationrdquo The EMBO Journal vol 31 no 6 pp 1556ndash15672012

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

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BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Archaea 3

Order Phylum Number ofgenomes

Number of homologs for replication genesORCCDC6 GINS15 GINS23 RPA MCM RFCS PCNA PolB DP1 DP2

Nitrosopumilales Thaumarchaeota 2 1 0 or 1 0 or 1 1 1 1 1 1 1 1

Thermoproteales

Crenarchaeota

14 0 0 1 1 to 3 1 to 3 0 09 2 0 0 or 1 1 0 0Desulfurococcales

15 3 1 1 1 1 1 3 0 0SulfolobalesNot named Korarchaeota 1 2 0 0 0 1 1 1 2 1 1Nanoarchaeota 1 1 0 0 1 1 1 1 1 1 1Thermococcales 11 1 1 3 1 1 1

1Methanopyrales 1 0 0 0 0 1 1 1 1 11

Methanobacteriales 7 1 or 2 0 or 1 0 1 1 1 2 1 1

Methanococcales Euryarchaeota 15 0 0 0 2 to 4 2 to 8 1 1 1 1

Thermoplasmatales 4 0 1 1 1 1 1 1 1

Archaeoglobales 4 2 or 3 0 0 1 or 2 1 1 1 1

Halobacteriales 15 3 to 15 0 0 1 1 or 2 1 1 1

Methanomicrobiales 6 0 0 1 1 2 1 1 or 2 1 1

Methanocellales 1 2 0 0 1 1 1 1 3 1 1Methanosarcinales 9 0 0 3 1 1

0lowast

0lowast

0lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

1lowast

3lowast

2lowast

2lowast

2lowast

2lowast

2lowast

2lowast

Figure 1 Homologs for some key genes involved in archaeal DNA replication Archaeal orders are phylogenetically organized followinga rooted maximum likelihood tree of Archaea based on 53 concatenated ribosomal proteins [36] The homology search was performedby RAST v40 (Rapid Annotation using Subsystem Technology) and the annotated data was viewed through the SEED viewer(httpwwwtheseedorg) A total of 115 archaeal genome sequences were obtained from NCBI and uploaded into the RAST server RASTannotation was performed using default parameters with the genetic code for Bacteria and Archaea The replication proteins homologswere checked through the SEED subsystem DNA replication Homology results of Thermococcus kodakaraensis KOD1 Pyrococcus furiosusDSM 3638 and Thermofilum pendens Hrk 5 were searched for replication protein homologs using BLAST (blastx v2228+) Results withhomology coverage of gt80 and 119864-values less than 0001 were considered as real homologs The results were also supplemented withdata from literature reviews and BLAST searches When indicated in the figure zero (0) homologs means that no homolog was foundfor a specific gene by using the described methodology Asterisks indicate that one or two of the analyzed microorganisms possessan exception for that specific feature Exceptions noted are (featureorder) ORC1CDC6Thermoproteales Thermofilum pendens Hrk5 (3homologs) and Thermosphaera aggregans DSM11486 (2 homologs) ORC1CDC6Thermoplasmatales and Picrophilus torridus DSM 9790(1 homolog) ORC1CDC6Methanomicrobiales and Methanoplanus petrolearius DSM11571 (4 homologs) ORC1CDC6Methanosarcinalesand Methanosalsum zhilinae DSM4017 (4 homologs) GINS15Thermoplasmatales and Thermoplasma acidophilum DSM1728 (1 homolog)GINS23Desulfurococcales Staphylothermus hellenicus DSM12710 (no homolog) and Staphylothermus marinus F1 (no homolog)GINS23Thermococcales Pyrococcus horikoshii OT3 (2 homologs) RPAThermoproteales Thermofilum pendens Hrk5 (3 homologs)and Thermosphaera aggregans DSM11486 (1 homolog) RPAMethanobacteriales and Methanothermus fervidus DSM2088 (no homolog)RPAArchaeoglobales and Archaeoglobus fulgidus DSM4304 (1 homolog) MCMThermococcales and Thermococcus kodakaraensis KOD1(3 homologs) MCMMethanosarcinales and Methanosarcina acetivorans C2A (2 homologs) RFCSDesulfurococcales and Hyperthermusbutylicus DSM 5456 (2 homologs) RFCSHalobacteriales and Haloquadratum walsbyi DSM16790 (1 homolog) RFCSMethanosarcinalesMethanosaeta concilii CG6 (2 homologs) and Methanosaeta thermophila PT (2 homologs) PCNADesulfurococcales and Ignisphaeraaggregans DSM17230 (1 homolog) PCNASulfolobales and Metallosphaera cuprina Ar-4 (1 homolog) PCNAThermococcales Pyrococcushorikoshii OT3 (2 homologs) and Thermococcus kodakaraensis KOD1 (2 homologs) PCNAMethanococcales Methanococcus maripaludisS2 (2 homologs) and Methanotorris igneus Kol5 (2 homologs) PolBThermoproteales Caldivirga maquilingensis IC-167 (3 homologs)and Pyrobaculum calidifontis JCM 11548 (3 homologs) PolBDesulfurococcales Staphylothermus hellenicus DSM12710 (3 homologs) andStaphylothermus marinus F1 (3 homologs) PolBArchaeoglobales Archaeoglobus fulgidus DSM4304 (2 homologs) PolBHalobacterialesHalorhabdus utahensis DSM12940 (2 homologs) PolBMethanosarcinales Methanosaeta concilii GP6 (2 homologs) DP1MethanosarcinalesMethanococcoides burtonii DSM6242 (2 homologs)

the replicative helicases In Bacteria this protein is DnaAwhich binds to the DnaA boxes [37] In eukaryotes aprotein complex known asORC (origin recognition complex)composed of 6 different proteins (Orc1-6) binds at thereplication origin and recruits other proteins [38] InArchaeathe candidate for replication initiation is a protein that shareshomology with the eukaryotic Orc1 and Cdc6 (cell divisioncycle 6) proteins and is encoded by almost all archaealgenomes [39] Their genes are commonly located adjacent tothe origin of replication These proteins termed Orc1Cdc6homologs have been studied in detail in representatives of theEuryarchaeota (Pyrococcus) and Crenarchaeota (Sulfolobus)and have been shown to bind to the ORB region with highspecificity [20 26 40] In addition purified Orc1Cdc6 from

S solfataricus binds to ORB elements from other crenar-chaeotes and euryarchaeotes in vitro suggesting that theseproteins recognize sequences conserved across the archaealdomain [20] The crystal structures of these proteins fromPyrobaculum aerophilum [41] and Aeropyrum pernix [42]have been solved contributing to the overall understandingof their activity during the initiation of replication (reviewedin [43]) In general the number of Orc1Cdc6 homologsfound in archaeal genomes varies between one and three(Figure 1) However there are some interesting exceptionsMembers of the order Halobacteriales possess between 3 and15Orc1Cdc6 homologs which may reflect the large numberof origins of replication Interestingly like other members oftheMethanosarcinales the extremely halophilic methanogen

4 Archaea

Methanohalobium evestigatum Z-7303 only possesses twoOrc1Cdc6 homologs Thus the ability to grow at extremelyhigh concentrations of salt and to maintain high intracellularsalt concentrations does not necessarily require a largenumber of Orc1Cdc6 homologsAlthoughmost members ofthe orderMethanomicrobiales possess two copies of this geneMethanoplanus petroleariusDSM 11571 possesses four copiesThus the number of Orc1Cdc6 homologs varies consider-ably among the euryarchaeotes In an extreme case repre-sentatives of the ordersMethanococcales andMethanopyralesdo not possess any recognizable homologs for the Orc1Cdc6protein [7 44] and the mechanics of replication initiation inthese archaea remain an intriguing unknown of the archaealreplication process

32 Initiation (DNA Unwinding and Primer Synthesis) AfterOrc1Cdc6 proteins bind to the origin of replication ahelicase is recruited to unwind the dsDNA In Bacteria thereplicative helicase is the homohexamer DnaB In eukaryotesthe most likely candidate for the replicative DNA helicase isthe MCM (minichromosome maintenance) complex whichis a heterohexamer that is activated when associated withother replicative proteins forming the CMG (Cdc45-MCM-GINS) complex [45ndash48] As in eukaryotes in Archaea themost probable candidate for the replicative helicase is theMCM complex Intriguingly theMCM complexes in eukary-otes and archaea possess a 31015840-51015840 unwinding polarity but thebacterialDnaBhelicase unwinds duplexDNAon the oppositedirection with a distinct 51015840-31015840 polarity [49ndash51]

Most archaeal genomes studied so far encode one MCMhomolog Its helicase activity has been demonstrated invitro for several archaea including Methanothermobacterthermautotrophicus ΔH where the MCM protein forms adimer of hexamers [52 53] The in vivo interaction betweenthe MCM complex and the Orc1Cdc6 proteins has beendemonstrated in other Archaea [54ndash56] Indeed through anin vitro recruiting assay Orc1CDC6 from P furiosus has beendemonstrated as the possible recruiter of the MCM complexto the origin of replication [57] A recent study identifiedthirteen species of archaeawithmultiplemcm genes encodingthe MCM complexes (Figure 1 [58]) The number of mcmhomologs is especially high in the order Methanococcaleswhere different representatives possess from 2 to 8 copies[59 60] For instance Methanococcus maripaludis S2 pos-sesses four homologs of the MCM protein [44] Through ashotgun proteomic study peptides for three of them havebeen detected [61] suggesting that multiple MCMs areexpressed and functional However a genome-wide surveyof gene functionality in M maripaludis demonstrated thatonly one of these genes MMP0030 was likely to be essentialfor growth [62] In addition coexpression of recombinantMCMs from M maripaludis S2 allowed copurification ofall four proteins [59] suggesting that M maripaludis mayform a heterologous multimeric MCM complex Howeverbecause MMP0030 protein is the only mcm gene essentialfor growth a homologous multimeric complex may alsobe possible Similar results have been found in Thermo-coccus kodakaraensis in which three MCM homologs arepresent but only one is essential [63] The T kodakaraensis

MCM system is suggested to form homologous multimericcomplexes [64] A recent study proposed that two of theMCMhomologs that are conserved among representatives ofthe order Methanococcales are a consequence of an ancientduplication that occurred prior to the divergence of thisgroup [59] It has also been proposed that the large numberof MCM homologs in the order Methanococcales is a directconsequence of mobile elements which may have takenadvantage of the ancient duplication of the MCM genes totake over the replication system by forming cellular MCMheterocomplexes [58] In any case the large number of MCMhomologs in the order Methanococcales may be a product ofan intricate and complex evolutionary history Whether ornot it is related to the absence of the replication initiationprotein Orc1Cdc6 is an interesting possibility [58]

In eukaryotes the MCM complex is not active on itsown and requires the association of two accessory factorsthe heterotetrameric GINS complex (from the Japanese go-ishi-ni-san meaning 5-1-2-3 after the four subunits Sld5Psf1 Psf2 and Psf3) and the Cdc45 protein This complexcalled CMG (Cdc45-MCM-GINS) is thought to be the activereplicative helicase [47] Homologs for GINS subunits havebeen identified in Archaea by bioinformatics analysis Onehomolog is most similar to the eukaryotic proteins Psf2and Psf3 (GINS23) and is common in the crenarchaeotesAnother homolog is most similar to the eukaryotic pro-teins Psf1 and Sld5 (GINS15) and is found largely in theeuryarchaeotes [65] The GINS complex is expected to beessential for DNA replication but the distribution of thesetwo different GINS homologs suggests that the presence ofone of them is sufficient for archaeal DNA replication SomeCrenarchaeota (S solfataricus) and some Euryarchaeota (Pfuriosus and T kodakaraensis) possess both homologs andform heterotetramers similar to the ones found in eukaryoteswith a ratio 2 2 [66ndash68] To find homologs of GINS15 andGINS23 in Archaea two known GINS15 (from Sulfolobussolfataricus P2 and Thermococcus gammatolerans EJ3) andthree known GINS23 (from Sulfolobus solfataricus P2 Pyro-coccus yayanosii CH1 andThermococcus gammatolerans EJ3)were used for homology searches These analyses failed toidentifyGINShomologs in several archaeal groups (Figure 1)These results suggest that there are other unknown GINShomologs in archaea or that the sequences have divergedenough between genera not to be recognized by homologysearches In any case a more comprehensive analysis of GINSproteins is necessary to fully understand their function anddistribution in Archaea

The detailed interactions of the GINS andMCM proteinsin archaea appear to be highly variable Although the Ssolfataricus GINS and MCM proteins physically interactin vitro MCM helicase activity was not stimulated in thecomplex [66] In contrast the MCM helicase activity of Tkodakaraensis and P furiosus is clearly stimulated by theirGINS complexes [64 67] The crystal structure of the GINScomplex of T kodakaraensis was recently determined Thebackbone structure and the assembly are similar to thehuman complex with some notable differences [68] Interest-ingly many other euryarchaeotes possess only the homologto GINS15 One of those Thermoplasma acidophilum forms

Archaea 5

a homotetrameric complex [68 69] Moreover in vitro the Tacidophilum MCM helicase activity was not affected by theGINS complex [69] These results suggest that other proteinsmay be involved in the formation of a stable helicase in manyArchaea M maripaludis S2 possesses a hypothetical proteinwhich may correspond to the gene encoding for GINS15which is probably essential for growth [60 62] No homologsof GINS23 are present in the genome ofM maripaludis

The replication related Cdc45 protein is ubiquitous ineukaryotes but its exact role has not yet been elucidatedInterestingly homologs of the Cdc45 protein are not presentin Archaea However a bioinformatics analysis revealed thatthe eukaryotic Cdc45 and the prokaryotic RecJ which is aconserved 51015840-31015840exonuclease in most bacteria and archaeapossess a common ancestry and share a homologous DHHdomain [70] These results suggest that the archaeal RecJmay substitute for the eukaryotic Cdc45 during replicationCircumstantial evidence supports this conclusion In S solfa-taricus a homolog of the DNA binding domain of RecJ waspurified together with a GINS protein [66] Similarly in Tkodakaraensis the RecJ homolog (TK1252p) copurified withproteins of theGINS complex [71] and formed a stable in vitroassociation with the GINS complex [72] Two RecJ homologsare found inM jannaschii (MJ0977 and 0831) and they par-tially complement a recJ mutation in E coliThe recombinantMJ0977 also possesses high levels of thermostable single-stranded DNA degrading activity similar to RecJ [73] In Mmaripaludis S2 four proteins possess the DHH domain withsimilarity to the M jannaschii RecJ homologs (MMP16820547 1078 and 1314) However none of them was essentialfor growth suggesting that the activities were redundant [62]Alternatively another protein which has a low similaritywith M jannaschii RecJ homolog (MMP0285) but possessesthe DHH domain was possibly essential for growth [62]However this protein possesses other domains related totransport which make it an unlikely candidate for RecJThese results are not definitive and more experimental datais needed to assign a function to this protein

As soon as the DNA is unwound ssDNA is protectedfromnucleases chemicalmodification and other disruptionsby ssDNA binding proteins These proteins are present in allthree domains of life and are called SSB in Bacteria wherethey form homotetramers or homodimers [74 75] and RPA(replication protein A) in eukaryotes where they form astable heterotrimer composed of 70 32 and 14 kDa proteins[76] Although all ssDNA binding proteins contain dif-ferent combinations of the oligonucleotideoligosaccharide-binding fold or OB-fold [77] the sequence similarity is lowamong RPA and the bacterial SSBs [43] In Archaea differ-ent types of ssDNA binding proteins have been reportedIn crenarchaeotes an ssDNA binding protein is only wellcharacterized in S solfataricus The S solfataricus ssDNAbinding protein contains only one OB-fold and can adopt aheterotetramer conformation [78] However the protein alsoappears to exist as a monomer [79] This protein appears tobe more similar to the bacterial proteins in sequence but itsstructure is more similar to that of the eukaryotic RPAs [4380] While homologs are recognizable in other members ofthe Sulfolobales andmost otherArchaea they are absent from

the genomes of many members of the closely related orderThermoproteales with some few exceptions (Figure 1) [81]

RPAs have been studied from different representativesof the euryarchaeotes revealing additional diversity M jan-naschii andM thermautotrophicus possess a single RPA sub-unit which shares amino acid similarity with the eukaryoticRPA70 and possesses four and five OB-folds respectively [8283] P furiosus possesses three different RPA subunits whichform a stable heterotrimer that is involved in homologousrecombination in vitro [84] The P furiosus RPA thereforeis similar in subunit organization to the eukaryotic RPATheother members of the Thermococcales genera also possessthree RPA homologs which likely form the homotrimericcomplex described for P furiosus (Figure 1) Methanosarcinaacetivorans also possesses three different RPAproteins (RPA1-3) with four two and two OB-folds respectively Howeverthey do not interact with each other and appear to functionas homodimers [85] This arrangement is common amongthe Methanosarcinales but is not found in the closely relatedmethanogen orders such as the Methanocellales (Figure 1)Members of the order Methanococcales possess two to fourRPA homologs The genome of M maripaludis S2 containsthree possible RPA homologs (MMP0122 0616 and 1032)[60] Only MMP0616 and 1032 were likely to be essential forgrowth [62] suggesting a possible different complex configu-ration for RPA proteins in this archaeon It has been hypoth-esized that the diversity in OB-folds in the archaeal RPAs is adirect consequence of homologous recombination [86]

DNA synthesis starts with the production of a RNAprimer since the DNA polymerases that replicate genomesare incapable of de novo DNA synthesis The RNA primeris synthesized by a DNA-dependent RNA polymerase orprimase DnaG a single subunit protein is the primase inBacteria In eukaryotes a two-subunit primase consisting ofa small catalytic subunit (PriS) and a large subunit (PriL)is found in a complex with DNA polymerase 120572 and itsaccessory B subunit [87] In Archaea the first biochemicallycharacterized primase was the eukaryotic primase-like smallsubunit PriS in M jannaschii [88] Later homologs of thePriS and PriL subunits were described in several Pyrococ-cus species [89ndash93] The eukaryotic-like DNA primase hasalso been characterized in the crenarchaeote S solfataricus[94 95] where it has been shown to interact with MCMthrough GINS23 [66] A unique polymerization activityacross discontinuous DNA templates has been characterizedin the PriSL of S solfataricus suggesting that this primasemay be involved in double-stranded break repair in Archaea[96] So far the eukaryotic-like primases found in archaeaexhibit similar properties PriS functions as the catalyticsubunit and PriL modulate its activity [87] In additionthe archaeal eukaryotic-like primase has the unique abilityto synthesize both DNA and RNA in vitro Indeed theP furiosus PriS synthesizes long DNA fragments but theaddition of PriL regulates the process by decreasing theDNA polymerase activity increasing the RNA polymeraseactivity and decreasing the product length [90] Additionallystudies of the P abyssi enzyme suggest that DNA primasemay also be involved in DNA repair because of the DNApolymerase gap filling and strand displacement activities

6 Archaea

also present in vitro [93] Interestingly the archaeal primasesmall subunit resembles DNA polymerases from the Pol Xfamily in sequence and structure suggesting a similarity intheir catalytic mechanism [96]

Homologs of the bacterial DnaG primase are also foundin archaea However in vitro studies of the P furiosusenzyme failed to detect primer synthesis activity and the TkodakaraensisDnaG was copurified with proteins of the exo-some [71] Also in S solfataricus DnaG primase was found tobe a core exosome subunit involved in RNA degradation [9798] However recent studies demonstrated that the S solfa-taricus DnaG homolog has limited primer synthesis activityand a dual primase system with PriSL has been proposed tofunction during DNA replication [99] Hu et al hypothesizedan interesting theory which suggests that LUCA employed adual-primase system comprisingDnaG and PriSL which alsoserved roles in RNA degradation and the nonhomologousend joining (NHEJ) pathwayThe system was inherited by allthree domains In theArchaea domain it retained its originalfunctions However in the Bacteria domain DnaG becamethe major replicative primase and PriSL evolved into the Poldomain of LigD involved in the NHEJ pathway In contrastDnaG was lost in the Eukaryota domain and PriSL becamethe only replicative primase In addition it also evolved intothe DNA Pol X family involved in NHEJ [96]

Like other ArchaeaM maripaludis S2 possesses both theeukaryotic- and bacterial-like primases A new genome-widesurvey of this methanoarchaea revealed that genes encodingboth subunits of the eukaryotic like primase PriS and PriL(MMP0009 and MMP0071) were likely to be essential forgrowth which is consistent with a role in replication Similarobservations have been demonstrated in other Archaea suchas Halobacterium sp NRC-1and Haloferax volcanii [93 100]In contrast the DnaG primase (MMP1286) was nonessentialwhich would be consistent with a role in the exosome [62]These results suggest that in M maripaludis and probablyother euryarchaeotes a dual primase system is not pre-sent

33 Elongation (Replicative DNA Polymerase) The primersynthesized by the primase is further extended by a replicativeDNA polymerase DNA polymerases have been classifiedinto seven families based on their amino acid sequencesimilarity (A B C D E X and Y) [101ndash105] In Bacteria Ecoli possesses five DNA polymerases Pol IndashV where the firstthree belong to families A B and C respectively and the lasttwo belong to the Y family The major replicative DNA poly-merase in E coli is Pol III a member of the C family whichsynthesizes DNA with high processivity when functioningwithin the holoenzyme [106] In eukaryotes a great diversityof DNA polymerases is also found but DNA replicationrequires three replicative DNA polymerases which belongto family B (Pol120572 Pol120575 and Pol120576) [107] In Archaea fewertypes of DNA polymerases are present but they have aninteresting evolutionary division Representatives of theDNApolymerase B family are found in all Archaea The D familyDNA polymerase is present in every phyla studied so farwith the exception of the Crenarchaeota (Figure 1) Lastly amember of theY family has been identified andbiochemically

characterized in S solfataricus [108] and the Methanosarci-nales in which several species harbor two homologs [109]Even though the activity of DNA polymerases belongingto the Y family in archaea is not fully understood they aresuggested to play an important role in DNA repair [109]

Representatives of the DNA polymerase family B havebeen identified in all Archaea The crenarchaeotes possess atleast two family B DNA polymerases (PolB I and PolB IIand in some cases PolB III) [102 110 111] The recombinantS solfataricus Pyrodictium occultum and A pernix enzymeshave been characterized [102] In contrast euryarchaeotesonly contain PolB I The recombinant P furiosus enzymehas been characterized [112] The PolB I enzymes havesimilar amino acid sequence and overall structure and theypossess a potent 31015840-51015840exonuclease proofreading activity [102]A unique property of the archaeal family B DNA polymeraseis the ability to stall DNA polymerization in the presenceof uracil or hypoxanthine deaminated bases [113 114] thisproperty helps to prevent the copy of template-strand uraciland the transmission of fixed mutations to progeny [115]Commonly cytosine deamination converts GC base pairsinto the promutagenic GU mismatches which result in50 of the offspring containing an AT transition mutationafter replication [116] In addition when A-U base pairs areformed the loss of the 5-methyl moiety upon replacementof thymine can exert a detrimental effect on protein DNAinteractions Interestingly in some crenarchaeotes and eur-yarchaeotes one of the B family DNA polymerase paralogspossesses disrupted versions of the sequence motifs thatare essential for catalysis Possibly these enzymes possess astructural role [117]

DNA polymerase family D (PolD) is a novel enzyme thatwas originally discovered in P furiosus [118] It has sincethen been identified in all euryarchaeotes [119] For a longtime this enzyme was considered a euryarchaeote-specificpolymerase but the three newly discovered archaeal phylawere also found to possess genes for PolD [14ndash16] PolD isa heterodimer with a small subunit (DP1) and a large subunit(DP2) It has been proposed that the large subunit harborsthe polymerase activity although its sequence is very differentfrom other hitherto described DNA polymerases The smallsubunit possesses high similarity with the noncatalytic B-subunits of the eukaryoticDNApolymerases120572 120575 and 120576 [120]Studies of the M jannaschii enzyme demonstrated that thesmall subunit possesses a strong 31015840-51015840exonuclease activitysuggesting that it may be involved in proofreading activity[7 121] Efficient polymerase and proofreading activity havealso been detected from a purified PolD of P furiosus andthe residues Asp-1122 and Asp-1124 are essential for thepolymerization reaction in P horikoshii [122 123] Everyeuryarchaeote examined possessed one homolog for DP1 andDP2 except forMethanococcoides burtoniiDSM 6242 whichpossesses two homologs for DP1 (Figure 1)

Because the crenarchaeotes only possess family B DNApolymerases one of themmust be the replicative polymeraseHowever in euryarchaeotes it was not clear which enzymewas involved in replication Studies in Halobacterium spNRC-1 showed that both PolB and PolD were essential forviability and it was proposed that they could be working

Archaea 7

together at the replication fork synthesizing the leading andlagging strand respectively [100 124] However in otherEuryarchaeota PolB does not appear to be essential Forinstance a recent report demonstrated that both subunits ofPolDwere essential but PolB was nonessential for the growthof M maripaludis S2 [62] Likewise in T kodakaraensisPolD can be coisolated with different proteins of the archaealreplication fork but PolB wasmainly coisolated with proteinsof unknown function [71] A deletion of the PolB in Tkodakaraensis also had no detectable effect on cell viability[125] Interestingly T kodakaraensis PolB mutants haveincreased sensitivity to UV radiation These results togethersuggest that PolD is the essential replicative DNA polymerasein these euryarchaeotes and not a PolB family polymeraseIn this scenario PolB may have some other crucial functionin Halobacterium and possibly other closely related specieswhich it is not conserved throughout the phylum Finallyit has been demonstrated that purified PolD from P abyssiis able to perform strand displacement and RNA primerextension in vitro Purified PolB on its own cannot performthese activities in vitro but in the presence of PCNA stranddisplacement activity is stimulated [124 126] A recent in vitrostudy in P abyssi demonstrated that RNase HII is required toinitiate strand displacement DNA synthesis by PolB [127]

34 Elongation (Other Accessory Proteins) Purified DNApolymerases possess low processivity however the addi-tion of an accessory factor the sliding clamp gives DNApolymerases the required processivity to replicate genomesThis factor whose structure resembles a doughnut functionsas a molecular platform which recruits several replication-associated enzymes and act together with DNA and thepolymerase to stabilize their interactions during replication[128] The structure of sliding clamps is conserved in thethree domains of life In Bacteria the sliding clamp or 120573-subunit is a homodimeric ring [129] In eukaryotes thesliding clamp or proliferating cell nuclear antigen (PCNA)is a homotrimeric ring [128] In Archaea the majority ofcrenarchaeotes have multiple PCNA homologs which formheterotrimeric rings [130 131] (Figure 1) In contrast mosteuryarchaeotes possess a single PCNA homolog (Figure 1)Interactions of DNA polymerase with the sliding clampare mediated through a common motif called the PCNAInteracting Protein (PIP) box [132] The three dimensionalstructures of PCNA-PolB and the PolB-PCNA-DNA complexfrom P furiosus have been solved shedding light on theinteractions between these molecules [133 134] In additiona study demonstrated that the PolDPCNA and PolBPCNAinteractions require two and one PIP boxes respectively[135] Recently through a protein-interaction network of Pabyssi a previously unknown protein with nuclease activity(Pab0431) and a PIP canonical motif was discovered tointeract with PCNA suggesting a possible involvement inDNA replication [136] T kodakaraensis is the only well-documented example of an euryarchaeotewith twohomologsfor PCNA TK0535 (PCNA1) and TK0582 (PCNA2) Recentwork demonstrated both proteins form stable homotrimericrings that interact with T kodakaraensis PolB in vitro [137]A more detailed study of the two homologs of PCNA in T

kodakaraensis demonstrated that both homologs stimulate invitro the primer extension activity of PolB but only PCNA1and not PCNA2 stimulates the same activity of PolD [138]Also the same report showed that the pcna2 gene can bedisrupted without causing growth deficiencies but it was notpossible to isolate mutants of pcna1 These results suggestthat PCNA1 but not PCNA2 is essential for DNA replication[138] It has been proposed that one of the PCNA geneswas acquired by lateral gene transfer [139] Members of theorderMethanococcales possess one PCNA homolog with twoexceptionsMmaripaludis S2 possesses twoPCNAhomologs(MMP1126 and 1711) [60] Both genes appeared to be essentialfor growth suggesting that they both play an importantrole in replication [62] The gene MMP1711 possesses highsimilarity to both T kodakaraensis genes and is likely thetrue methanococcal PCNA In contrast MMP1126 possessesonly low similarity to the T kodakaraensis genes and alsocontains an S-adenosylmethionine-dependent methyltrans-ferases domain Thus it is likely to possess some alternativefunction Methanotorris igneus Kol 5 also possesses twoPCNA homologs

For PCNA to assemble around DNA a specific loadingfactor is required In Bacteria the loading factor is knownas 120574-complex and comprises three different subunits ina 1205743-120575-1205751015840 stoichiometry [140] In eukaryotes the loading

factor is known as Replication Factor C (RFC) and is aheteropentameric complex comprising one large subunit andfour different small subunits [141] In contrast inArchaea theRFC consists of two different proteins a small subunit RFCSand a large subunit RFCLThey also form a heteropentamericcomplex in a 4 1 ratio (RFCS RFCL) Interestingly manycrenarchaeotes possess one homolog of RFCL and two orthree homologs of RFCS Alternatively most euryarchaeotespossess only one RFCL and RFCS homolog The exceptionsare somemembers of the ordersHalobacteriales Methanomi-crobiales and Methanosarcinales which possess two RFCShomologs (Figure 1) Structural and biochemical studies ofRFC have been conducted in several euryarchaeotes such asArchaeoglobus fulgidus and Pyrococcus species [142ndash144] Aninteresting case is observed in Methanosarcina acetivoransThis RFC possesses three subunits (RFC1 2 L) found ina ratio 3 1 1 [145] Homologs for these three subunits arealso present in most of the genomes of the haloarchaea[145] It is inferred that this type of RFC complex representsan intermediary form transitional between the canonicalarchaeal RFC complex of one small and one large subunit andthe eukaryotic RFC complex of four different small and onelarge subunit [146] The organization and spatial distributionexhibit a similarity to the E coliminimal 120574-complex but thefunction of the subunits is probably not conserved [145]

35 Maturation During DNA replication the lagging strandis discontinuously synthesized by extending the RNAprimersor Okazaki fragments This discontinuously synthesizedDNA strand requires maturation to form a single covalentlyclosed strand to end the replication process In ArchaeaOkazaki fragments were first demonstrated during replica-tion in P abyssi and Sulfolobus acidocaldarius [147] Duringreplication these RNA primers are replaced with DNA The

8 Archaea

removal of the primers is performed by the enzyme RNase Hwhich is ubiquitous in the three domains of life Accordingto their sequence similarity in prokaryotes the RNase Hproteins are classified into three groups RNase HI HII andHIII In eukaryotes they are classified as RNase H1 and H2[148] However phylogenetic analyses suggest that the RNaseH proteins can also be classified into two different groupsType 1 (prokaryotic RNaseHI eukaryotic RNaseH1 and viralRNase H) and Type 2 (prokaryotic RNase HII and HIII andeukaryotic RNase H2) [149] These two types of RNase Hpossess different specific activities metal ion preferences andcleavage sites [150] Originally it was thought that Archaeaonly possess type 2 RNase H [149] but several type 1 archaealRNase H enzymes have since then been discovered [151 152]Interestingly in eukaryotes RNaseH1 andH2 tend to coexistand different combinations of the three prokaryotic RNasesH(I II and III) are found except for the combination of RNasesHI and HIII This mutually exclusive evolution of some ofthe prokaryotic RNases seems to be related to functionalredundancy [148]

Another enzyme involved in primer replacement inDNA replication is the Flap endonuclease I (FEN-1) whichrecognizes double-strandedDNAwith an unannealed 51015840-flapand cleaves it A eukaryotic homolog of FEN-1 is found inevery archaeal member analyzed and one member of theThermoproteales Thermofilum pendens Hrk5 possesses twohomologs

M maripaludis S2 possesses genes for the prokaryoticRNase HI and HII and for FEN-1 but none are essentialsuggesting that they may be redundant in their functions[44 62] Possibly both RNase H proteins persist and areevolutionary stable in the genome The gene products mayperform the same function but one is less efficient than theother [153]

After the Okazaki fragments are replaced by DNA inthe lagging strand the nick between the newly synthesizedand the elongated DNA is repaired by a DNA ligase Thisenzyme uses a nucleotide cofactor to catalyze the formationof the phosphodiester bond in three well-characterized steps[154]The enzyme is common to all three domains but can begrouped into two families based on cofactor specificity (ATPor NAD+) The DNA ligases from several crenarchaeotes andeuryarchaeotes have been further characterized (reviewedin [43]) Many archaeal DNA ligases possess dual cofactorspecificity (ATPNAD+ or ATPADP) but every archaealDNA ligase characterized so far uses ATP A thermophilicDNA ligase from M thermautotrophicus which uses ATP assole cofactor was characterized in vitro [155] A characterizedDNA ligase from the crenarchaeote Sulfophobococcus zilligiidisplayed specificity for three cofactors (ATPNAD+GTP)[156]Major structuralwork in this enzymehas been achievedin P furiosus and S solfataricus and the findings have beenreviewed in detail [43] InM maripaludis S2 the DNA ligaseis likely to be essential for growth [44 62]

Understanding the maturation process in archaea hasbecome a focus of increasing research in recent years An invitro study reconstituted the Okazaki fragment maturationusing proteins derived from the crenarchaeote S solfataricusThey demonstrated that only six proteins are necessary for

coupled DNA synthesis RNA primer removal and DNAligation In this model a single PCNA (heterotrimeric ring)coordinates the activities of PolBI FEN-1 and DNA ligaseinto an efficient maturation complex [157] A different invitro study in P abyssi has demonstrated two different modelsfor Okazaki fragments maturation which differ in the RNAprimer removal process In the first model RNA primerelimination is executed by continuous PolD strand displace-ment DNA synthesis and 51015840RNA flap cleavage by FEN-1The resulting nicks are closed by DNA ligase Alternativelythe second model proposes that RNase HII cleaves theRNA primer followed by the action of FEN-1 and stranddisplacement DNA synthesis by polB or polD The nick isthen sealed by DNA ligase [127] Testing these models invivo is of great interest to complete the picture of how theseprocesses behave in the cell In addition other factors that canmodulate these processesmay be required for coordination ofthe in vivomaturation process

4 Conclusions

DNA replication in archaea possesses a dual nature wherethe machinery is structurally and functionally similar to theeukaryotic replication system but it is executed within abacterial context [11 25] Additionally unique archaeal fea-tures demonstrate the complexity of this process and it doesnot appear to be just a simplified version of the eukary-otic system For example the archaeal specific DNA poly-merase D is conserved across the Archaea domain with theexception of the Crenarchaeota phylumThe recent discoverythat it is the essential replicative polymerase in two differenteuryarchaeotic species demonstrates an unanticipated vari-ability in archaeal DNA replication and a fundamental differ-ence in the replication mechanism between crenarchaeotesand euryarchaeotes Interestingly the absence of PolD increnarchaeotes is not the only difference in DNA repli-cation These differences include the absence of histonesin crenarchaeotes [4] the presence of multiple origins ofreplication in crenarchaeotes and a single origin of repli-cation in most euryarchaeotes the absence of GINS23 inmost euryarchaeotes the absence of RPA protein in manycrenarchaeotes the presence of multiple MCM homologs inMethanococcales and the presence of one homolog of PCNAin euryarchaeotes compared to the multiple homologs increnarchaeotes These distinctive characteristics between thephyla highlight the complexity of archaeal DNA replicationand suggest a complex evolutionary history (Table 1)

Among the Euryarchaeota the ordersHalobacteriales andMethanococcales possess differences in the DNA replicationsystem that make them unique For instance Halobac-teriales possess many more origin recognition proteins(Orc1Cdc6) compared to the rest of the archaea On theother hand Methanococcales and Methanopyrales lack rec-ognizable homologs for the Orc1Cdc6 proteins suggestingthe presence of a very different mechanism for initiation ofreplication In addition the Methanococcales possess a largenumber of MCM protein homologs It has been proposedthat these distinctive features are connected and because ofthe absence of the Orc1Cdc6 proteins MCM proteins may

Archaea 9

Table1DNAreplicationproteins

andfeatures

inthed

omains

BacteriaEukaryotaand

thetwomajor

phylao

fthe

Archaeado

main

Mod

ified

from

[43]

DNAreplicationstage

Process

Bacteria

Eukaryota

Archaea

Crenarchaeota

Euryarchaeota

Preinitia

tion

Orig

inof

replication

Sing

leMultip

leMultip

leSing

lea

Orig

inrecogn

ition

DnaA

ORC

complex

(ORC

1-6)

Orc1C

dc6

Orc1C

dc6b

Initiation

DNAun

winding

(Helicase)

DnaB

MCM

complex

(MCM

2-7)

MCM

complex

MCM

complex

DNAun

winding

(Accessory

proteins)

DnaC

Cdc6

GIN

S23GIN

S15

GIN

S15c

Cdt1

GIN

Scomplex

(Sld5Psf1-3)

RecJho

molog

RecJho

molog

Cdc45

Prim

ersynthesis

DnaG

Pol120572

prim

asec

omplex

DNAprim

ase

(PriS

L)D

naG

dDNAprim

ase(PriSL)

Elon

gatio

n

DNAsynthesis

(polym

erase)

PolIII(Fam

ilyCDNApo

lymerase)

Pol120575and

Pol120576(Fam

ilyBDNA

polymerase)

Family

BDNApo

lymerase

Family

DDNA

polymerasee

DNAsynthesis

(Processivity

factors)

120574-com

plex

(clamploader)

RFC(clamploader)

RFC(clamploader)

RFC(clamploader)

120573-clamp(clamp)

PCNA(clamp)

PCNA(clamp)

PCNA(clamp)

Maturation

Maturation(O

kazaki

fragmentp

rocessing)

PolI

(family

ADNApo

lymerase)

Fen1D

na2

Fen1

Fen1

RNaseH

RNaseH

RNaseH

RNaseH

DNAligase

DNAligase

DNAligase

DNAligase

a Exceptio

ntheo

rder

Halobacteria

les

b Not

know

nform

embersof

theE

uryarchaeota

ordersMethanococcalesandMethanopyrales

c GIN

S23hasb

eenfoun

dedon

lyin

theo

rder

Thermococcales

oftheE

uryarchaeota

d Sulfolobu

ssolfataric

usdidshow

prim

asea

ctivity

invitro

e Fam

ilyBDNApo

lymeraseisa

lsoessentialinHalobacteriu

mB

ecause

itsfunctio

nhasn

otbeen

clearlyelu

cidateditmight

also

play

aroleinreplicationin

thisandclo

selyrelated

organism

s

10 Archaea

interact with other unknown initiation enzymes resultingin a complex phylogeny of the MCM homologs [49] Pre-sumably these differences also account for the inability torecognize the origin of replication in these microorganismsThis unique scenario for initiation of DNA replicationmay bea direct consequence of various processes such as duplicationmobile genetic elements and interactions with viruses [58]

The differences in DNA replication among archaealhigher taxa demonstrate an unexpected variability and sug-gest two alternative evolutionary models In the first modelDNA replication evolved late after the diversification ofthe archaeal lineages Because the replicative system wasnot fully formed it was possible to develop differentlybetween the lineages Once formed replication would thenbe highly conserved However this model is not consistentwith differences observed between lineages that must haveformed relatively late such as those between the orders oreven in some cases within certain orders The alternativemodel is that DNA replication has changed throughout theevolution of the archaea Thus differences in the replicativesystems may represent ancient as well as modern adaptationsto changing environments In this case differences in thereplicative systems may provide important insights into theevolutionary pressures in play during different episodes ofarchaeal evolution From this perspective the differencesbetween the eukaryotic and archaeal replicative systems maynot be evidence for an ancient origin of the eukaryotesInstead it is entirely plausible that the replicative system ineukaryotes could have evolved relatively late from a well-developed archaeal system

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] E F DeLong and N R Pace ldquoEnvironmental diversity ofbacteria and archaeardquo Systematic Biology vol 50 no 4 pp 470ndash478 2001

[2] B Chaban S Y M Ng and K F Jarrell ldquoArchaeal habitatsmdashfrom the extreme to the ordinaryrdquo Canadian Journal of Micro-biology vol 52 no 2 pp 73ndash116 2006

[3] M J Hanford and T L Peeples ldquoArchaeal tetraether lipidsunique structures and applicationsrdquo Applied Biochemistry andBiotechnology A vol 97 no 1 pp 45ndash62 2002

[4] K Sandman and J N Reeve ldquoArchaeal histones and the originof the histone foldrdquo Current Opinion in Microbiology vol 9 no5 pp 520ndash525 2006

[5] O Lecompte R Ripp J-C Thierry D Moras and O PochldquoComparative analysis of ribosomal proteins in complete gen-omes an example of reductive evolution at the domain scalerdquoNucleic Acids Research vol 30 no 24 pp 5382ndash5390 2002

[6] D R Edgell and W F Doolittle ldquoArchaea and the origin(s) ofDNA rplication poteinsrdquo Cell vol 89 no 7 pp 995ndash998 1997

[7] E R Barry and S D Bell ldquoDNA replication in the archaeardquoMicrobiology and Molecular Biology Reviews vol 70 no 4 pp876ndash887 2006

[8] S Gribaldo and C Brochier-Armanet ldquoThe origin and evolu-tion of archaea a state of the artrdquo Philosophical Transactions ofthe Royal Society B vol 361 no 1470 pp 1007ndash1022 2006

[9] P Londei ldquoEvolution of translational initiation new insightsfrom the archaeardquo FEMS Microbiology Reviews vol 29 no 2pp 185ndash200 2005

[10] B Grabowski and Z Kelman ldquoArchaeal DNA replicationeukaryal proteins in a bacterial contextrdquo Annual Review ofMicrobiology vol 57 pp 487ndash516 2003

[11] P Forterre J Filee and H Myllykallio ldquoOrigin and evolutionof DNA and DNA replication machineriesrdquo in The GeneticCode and the Origin of Life L Ribas Ed Landes BioscienceGeorgetown Tex USA 2007

[12] E V Koonin ldquoThe origin and early evolution of eukaryotesin the light of phylogenomicsrdquo Genome Biology vol 11 no 5article 209 2010

[13] M Konneke A E Bernhard J R de la Torre C B WalkerJ B Waterbury and D A Stahl ldquoIsolation of an autotrophicammonia-oxidizing marine archaeonrdquo Nature vol 437 no7058 pp 543ndash546 2005

[14] C Brochier-Armanet B Boussau S Gribaldo and P ForterreldquoMesophilic crenarchaeota proposal for a third archaeal phy-lum theThaumarchaeotardquoNature Reviews Microbiology vol 6no 3 pp 245ndash252 2008

[15] J G Elkins M Podar D E Graham et al ldquoA korarchaealgenome reveals insights into the evolution of the ArchaeardquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 105 no 23 pp 8102ndash8107 2008

[16] T Nunoura Y Takaki J Kakuta et al ldquoInsights into theevolution of Archaea and eukaryotic protein modifier systemsrevealed by the genome of a novel archaeal grouprdquoNucleic AcidsResearch vol 39 no 8 pp 3204ndash3223 2011

[17] HHuberM J Hohn R Rachel T Fuchs V CWimmer andKO Stetter ldquoAnewphylumofArchaea represented by a nanosizedhyperthermophilic symbiontrdquoNature vol 417 no 6884 pp 63ndash67 2002

[18] C Brochier S Gribaldo Y Zivanovic F Confalonieri and PForterre ldquoNanoarchaea representatives of a novel archaeal phy-lum or a fast-evolving euryarchaeal lineage related to Therm-ococcalesrdquo Genome Biology vol 6 no 5 article R42 2005

[19] S J Aves ldquoDNA replication initiationrdquo Methods in MolecularBiology vol 521 pp 3ndash17 2009

[20] N P Robinson I Dionne M Lundgren V L Marsh RBernander and S D Bell ldquoIdentification of two origins ofreplication in the single chromosome of the archaeon Sulfolobussolfataricusrdquo Cell vol 116 no 1 pp 25ndash38 2004

[21] M Lundgren A Andersson L Chen P Nilsson and RBernander ldquoThree replication origins in Sulfolobus speciessynchronous initiation of chromosome replication and asyn-chronous terminationrdquo Proceedings of the National Academy ofSciences of theUnited States of America vol 101 no 18 pp 7046ndash7051 2004

[22] N P Robinson and S D Bell ldquoExtrachromosomal element cap-ture and the evolution ofmultiple replication origins in archaealchromosomesrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 104 no 14 pp 5806ndash58112007

[23] E A Pelve A C Lindas A Knoppel A Mira and R Bernan-der ldquoFour chromosome replication origins in the archaeonPyrobaculum calidifontisrdquo Molecular Microbiology vol 85 no5 pp 986ndash995 2012

Archaea 11

[24] A F Andersson E A Pelve S LindebergM Lundgren P Nils-son and R Bernander ldquoReplication-biased genome organisa-tion in the crenarchaeon Sulfolobusrdquo BMCGenomics vol 11 no1 article 454 2010

[25] H Myllykallio P Lopez P Lopez-Garcıa et al ldquoBacterial modeof replication with eukaryotic-like machinery in a hyperther-mophilic archaeonrdquo Science vol 288 no 5474 pp 2212ndash22152000

[26] F Matsunaga P Forterre Y Ishino and H Myllykallio ldquoInvivo interactions of archaeal Cdc6Orc1 and minichromosomemaintenance proteins with the replication originrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 98 no 20 pp 11152ndash11157 2001

[27] S Maisnier-Patin L Malandrin N K Birkeland and RBernander ldquoChromosome replication patterns in the hyper-thermophilic euryarchaeaArchaeoglobus fulgidus andMethano-caldococcus (Methanococcus) jannaschiirdquo Molecular Microbiol-ogy vol 45 no 5 pp 1443ndash1450 2002

[28] R Zhang and C-T Zhang ldquoMultiple replication origins ofthe archaeon Halobacterium species NRC-1rdquo Biochemical andBiophysical Research Communications vol 302 no 4 pp 728ndash734 2003

[29] C Norais M Hawkins A L Hartman J A Eisen H Myl-lykallio and T Allers ldquoGenetic and physical mapping of DNAreplication origins in Haloferax volcaniirdquo PLoS Genetics vol 3no 5 article e77 2007

[30] J A Coker P DasSarma M Capes et al ldquoMultiple replicationorigins of Halobacterium sp strain NRC-1 properties of theconserved orc7-dependent oriC1rdquo Journal of Bacteriology vol191 no 16 pp 5253ndash5261 2009

[31] Z Wu J Liu H Yang H Liu and H Xiang ldquoMultiple repli-cation origins with diverse control mechanisms in Haloarculahispanicardquo Nucleic Acids Research 2013

[32] M Hawkins S Malla M J Blythe C A Nieduszynski and TAllers ldquoAccelerated growth in the absence of DNA replicationoriginsrdquo Nature vol 503 no 7477 pp 544ndash547 2013

[33] A I Majernık and J P J Chong ldquoA conserved mechanismfor replication origin recognition and binding in archaeardquo TheBiochemical Journal vol 409 no 2 pp 511ndash518 2008

[34] J E Galagan C Nusbaum A Roy et al ldquoThe genome of Macetivorans reveals extensive metabolic and physiological diver-sityrdquo Genome Research vol 12 no 4 pp 532ndash542 2002

[35] R Zhang and C-T Zhang ldquoIdentification of replication originsin archaeal genomes based on the Z-curve methodrdquo Archaeavol 1 no 5 pp 335ndash346 2005

[36] A Spang R Hatzenpichler C Brochier-Armanet et al ldquoDis-tinct gene set in two different lineages of ammonia-oxidizingarchaea supports the phylum Thaumarchaeotardquo Trends inMicrobiology vol 18 no 8 pp 331ndash340 2010

[37] K J Marians ldquoProkaryotic DNA replicationrdquo Annual Review ofBiochemistry vol 61 pp 673ndash719 1992

[38] S P Bell ldquoThe origin recognition complex from simple originsto complex functionsrdquo Genes and Development vol 16 no 6pp 659ndash672 2002

[39] V L Marsh and S D Bell ldquoDNA replication and the cell cyclerdquoin Archaea Evolution Physiology and Molecular Biology R AGarrett and H P Klenk Eds Blackwell Publishing HobokenNJ USA 2007

[40] F Matsunaga A Glatigny M-H Mucchielli-Giorgi et alldquoGenomewide and biochemical analyses of DNA-binding activ-ity of Cdc6Orc1 and Mcm proteins in Pyrococcus sprdquo NucleicAcids Research vol 35 no 10 pp 3214ndash3222 2007

[41] J Liu C L Smith D DeRyckere K DeAngelis G S Martinand J M Berger ldquoStructure and function of Cdc6Cdc18implications for origin recognition and checkpoint controlrdquoMolecular Cell vol 6 no 3 pp 637ndash648 2000

[42] M R Singleton R Morales I Grainge N Cook M NIsupov and D B Wigley ldquoConformational changes inducedby nucleotide binding in Cdc6ORC from Aeropyrum pernixrdquoJournal of Molecular Biology vol 343 no 3 pp 547ndash557 2004

[43] Y Ishino and S Ishino ldquoRapid progress of DNA replicationstudies in Archaea the third domain of liferdquo Science China LifeSciences vol 55 no 5 pp 386ndash403 2012

[44] E L Hendrickson R Kaul Y Zhou et al ldquoComplete genomesequence of the genetically tractable hydrogenotrophic meth-anogen Methanococcus maripaludisrdquo Journal of Bacteriologyvol 186 no 20 pp 6956ndash6969 2004

[45] B K Tye ldquoMCM proteins in DNA replicationrdquo Annual Reviewof Biochemistry vol 68 pp 649ndash686 1999

[46] K Labib and J F X Diffley ldquoIs the MCM2-7 complex theeukaryotic DNA replication fork helicaserdquo Current Opinion inGenetics amp Development vol 11 no 1 pp 64ndash70 2001

[47] I Ilves T Petojevic J J Pesavento and M R Botchan ldquoActi-vation of the MCM2-7 helicase by association with Cdc45 andGINS proteinsrdquoMolecular Cell vol 37 no 2 pp 247ndash258 2010

[48] M L Bochman andA Schwacha ldquoTheMcm complex unwind-ing the mechanism of a replicative helicaserdquo Microbiology andMolecular Biology Reviews vol 73 no 4 pp 652ndash683 2009

[49] Y Ishimi ldquoADNAhelicase activity is associated with anMCM4-6 and -7 protein complexrdquoThe Journal of Biological Chemistryvol 272 no 39 pp 24508ndash24513 1997

[50] Z Kelman and M F White ldquoArchaeal DNA replication andrepairrdquo Current Opinion in Microbiology vol 8 no 6 pp 669ndash676 2005

[51] J H LeBowitz and R McMacken ldquoThe Escherichia coli dnaBreplication protein is a DNA helicaserdquoThe Journal of BiologicalChemistry vol 261 no 10 pp 4738ndash4748 1986

[52] Z Kelman J-K Lee and J Hurwitz ldquoThe single minichro-mosome maintenance protein ofMethanobacterium thermoau-totrophicum ΔH contains DNA helicase activityrdquo Proceedings ofthe National Academy of Sciences of the United States of Americavol 96 no 26 pp 14783ndash14788 1999

[53] D F Shechter C Y Ying and J Gautier ldquoThe intrinsic DNAhelicase activity of Methanobacterium thermoautotrophicumΔH minichromosome maintenance proteinrdquo The Journal ofBiological Chemistry vol 275 no 20 pp 15049ndash15059 2000

[54] M de Felice L Esposito B Pucci M de Falco M Rossi andF M Pisani ldquoA CDC6-like factor from the archaea Sulfolobussolfataricus promotes binding of the mini-chromosome main-tenance complex to DNArdquoThe Journal of Biological Chemistryvol 279 no 41 pp 43008ndash43012 2004

[55] R Kasiviswanathan J-H Shin and Z Kelman ldquoInteractionsbetween the archaeal Cdc6 and MCM proteins modulate theirbiochemical propertiesrdquo Nucleic Acids Research vol 33 no 15pp 4940ndash4950 2005

[56] J-H Shin B Grabowski R Kasiviswanathan S D Bell andZ Kelman ldquoRegulation of minichromosomemaintenance heli-case activity by Cdc6rdquo The Journal of Biological Chemistry vol278 no 39 pp 38059ndash38067 2003

[57] M Akita A Adachi K Takemura T Yamagami F Matsunagaand Y Ishino ldquoCdc6Orc1 from Pyrococcus furiosus may actas the origin recognition protein and Mcm helicase recruiterrdquoGenes to Cells vol 15 no 5 pp 537ndash552 2010

12 Archaea

[58] M Krupovic S Gribaldo D H Bamford and P Forterre ldquoTheevolutionary history of archaeal MCM helicases a case study ofvertical evolution combined with hitchhiking of mobile geneticelementsrdquo Molecular Biology and Evolution vol 27 no 12 pp2716ndash2732 2010

[59] ADWalters and J P J Chong ldquoAn archaeal orderwithmultipleminichromosome maintenance genesrdquo Microbiology vol 156part 5 pp 1405ndash1414 2010

[60] A DWalters and J P J Chong ldquoMethanococcusmaripaludis anarchaeon with multiple functional MCM proteinsrdquo Biochemi-cal Society Transactions vol 37 no 1 pp 1ndash6 2009

[61] Q Xia E L Hendrickson Y Zhang et al ldquoQuantitative pro-teomics of the archaeon Methanococcus maripaludis validatedbymicroarray analysis and real time PCRrdquoMolecularampCellularProteomics vol 5 no 5 pp 868ndash881 2006

[62] F Sarmiento J Mrazek and W B Whitman ldquoGenome-scaleanalysis of gene function in the hydrogenotrophic methano-genic archaeon Methanococcus maripaludisrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 110 no 12 pp 4726ndash4731 2013

[63] M Pan T J Santangelo Z Li J N Reeve and Z KelmanldquoThermococcus kodakarensis encodes threeMCMhomologs butonly one is essentialrdquo Nucleic Acids Research vol 39 no 22 pp9671ndash9680 2011

[64] S Ishino S Fujino H Tomita et al ldquoBiochemical and geneticalanalyses of the three mcm genes from the hyperthermophilicarchaeon Thermococcus kodakarensisrdquo Genes to Cells vol 16no 12 pp 1176ndash1189 2011

[65] K S Makarova Y I Wolf S L Mekhedov B G Mirkin and EV Koonin ldquoAncestral paralogs and pseudoparalogs and theirrole in the emergence of the eukaryotic cellrdquo Nucleic AcidsResearch vol 33 no 14 pp 4626ndash4638 2005

[66] N Marinsek E R Barry K S Makarova I Dionne E VKoonin and S D Bell ldquoGINS a central nexus in the archaealDNA replication forkrdquo EMBOReports vol 7 no 5 pp 539ndash5452006

[67] T Yoshimochi R Fujikane M Kawanami F Matsunaga and YIshino ldquoTheGINS complex from Pyrococcus furiosus stimulatesthe MCM helicase activityrdquoThe Journal of Biological Chemistryvol 283 no 3 pp 1601ndash1609 2008

[68] T Oyama S Ishino S Fujino et al ldquoArchitectures of archaealGINS complexes essential DNA replication initiation factorsrdquoBMC Biology vol 9 article 28 2011

[69] H Ogino S Ishino K Mayanagi et al ldquoThe GINS com-plex from the thermophilic archaeon Thermoplasma aci-dophilummay function as a homotetramer inDNA replicationrdquoExtremophiles vol 15 no 4 pp 529ndash539 2011

[70] L Sanchez-Pulido and C P Ponting ldquoCdc45 the missing recjortholog in eukaryotesrdquoBioinformatics vol 27 no 14 pp 1885ndash1888 2011

[71] Z Li T J Santangelo L Cubonova J N Reeve and Z KelmanldquoAffinity purification of an archaeal DNA replication proteinnetworkrdquomBio vol 1 no 5 2010

[72] Z Li M Pan T J Santangelo et al ldquoA novel DNA nucleaseis stimulated by association with the GINS complexrdquo NucleicAcids Research vol 39 no 14 pp 6114ndash6123 2011

[73] L A Rajman and S T Lovett ldquoA thermostable single-strandDNase from Methanococcus jannaschii related to the RecJrecombination and repair exonuclease from Escherichia colirdquoJournal of Bacteriology vol 182 no 3 pp 607ndash612 2000

[74] K RWilliams J B Murphy and JW Chase ldquoCharacterizationof the structural and functional defect in the Escherichia colisingle-stranded DNA binding protein encoded by the ssb-1 mutant gene Expression of the ssb-1 gene under 120582p(L)regulationrdquoThe Journal of Biological Chemistry vol 259 no 19pp 11804ndash11811 1984

[75] S Dąbrowski M Olszewski R Pitek and J Kur ldquoNovel ther-mostable ssDNA-binding proteins fromThermus thermophilusand T aquaticus-expression and purificationrdquo Protein Expres-sion and Purification vol 26 no 1 pp 131ndash138 2002

[76] C Iftode Y Daniely and J A Borowiec ldquoReplication proteinA (RPA) the eukaryotic SSBrdquo Critical Reviews in Biochemistryand Molecular Biology vol 34 no 3 pp 141ndash180 1999

[77] A G Murzin ldquoOB(oligonucleotideoligosaccharide binding)-fold common structural and functional solution for non-hom-ologous sequencesrdquo The EMBO Journal vol 12 no 3 pp 861ndash867 1993

[78] C A Haseltine and S C Kowalczykowski ldquoA distinctive single-stranded DNA-binding protein from the Archaeon Sulfolobussolfataricusrdquo Molecular Microbiology vol 43 no 6 pp 1505ndash1515 2002

[79] R I M Wadsworth and M F White ldquoIdentification and pro-perties of the crenarchaeal single-stranded DNA binding pro-tein from Sulfolobus solfataricusrdquoNucleic Acids Research vol 29no 4 pp 914ndash920 2001

[80] I D Kerr R I M Wadsworth L Cubeddu W Blankenfeldt JHNaismith andM FWhite ldquoInsights into ssDNA recognitionby the OB fold from a structural and thermodynamic study ofSulfolobus SSB proteinrdquo The EMBO Journal vol 22 no 11 pp2561ndash2570 2003

[81] X Luo U Schwarz-Linek C H Botting R Hensel B Siebersand M F White ldquoCC1 a novel crenarchaeal DNA binding pro-teinrdquo Journal of Bacteriology vol 189 no 2 pp 403ndash409 2007

[82] T J Kelly P Simancek and G S Brush ldquoIdentification andcharacterization of a single-stranded DNA-binding proteinfrom the archaeonMethanococcus jannaschiirdquoProceedings of theNational Academy of Sciences of theUnited States of America vol95 no 25 pp 14634ndash14639 1998

[83] Z Kelman S Pietrokovski and J Hurwitz ldquoIsolation and cha-racterization of a split B-type DNA polymerase from the arch-aeonMethanobacterium thermoautotrophicumΔHrdquoTheJournalof Biological Chemistry vol 274 no 40 pp 28751ndash28761 1999

[84] K Komori and Y Ishino ldquoReplication protein A in Pyrococcusfuriosus is involved in homologous DNA recombinationrdquo TheJournal of Biological Chemistry vol 276 no 28 pp 25654ndash25660 2001

[85] J B Robbins M C Murphy B A White R I Mackie THa and I K O Cann ldquoFunctional analysis of multiple single-stranded DNA-binding proteins from Methanosarcina acetivo-rans and their effects on DNA synthesis by DNA polymeraseBIrdquoThe Journal of Biological Chemistry vol 279 no 8 pp 6315ndash6326 2004

[86] Y Lin L-J Lin P Sriratana et al ldquoEngineering of functionalreplication protein a homologs based on insights into the evolu-tion of oligonucleotideoligosaccharide-binding foldsrdquo Journalof Bacteriology vol 190 no 17 pp 5766ndash5780 2008

[87] D N Frick and C C Richardson ldquoDNA primasesrdquo AnnualReview of Biochemistry vol 70 pp 39ndash80 2001

[88] G Desogus S Onesti P Brick M Rossi and F M PisanildquoIdentification and characterization of a DNA primase fromthe hyperthermophilic archaeon Methanococcus jannaschiirdquoNucleic Acids Research vol 27 no 22 pp 4444ndash4450 1999

Archaea 13

[89] A A Bocquier L Liu I K O Cann K Komori D Kohda andY Ishino ldquoArchaeal primase bridging the gap between RNAand DNA polymerasesrdquo Current Biology vol 11 no 6 pp 452ndash456 2001

[90] L Liu K Komori S Ishino et al ldquoThe archaeal DNA primasebiochemical characterization of the p41-p46 complex fromPyrococcus furiosusrdquo The Journal of Biological Chemistry vol276 no 48 pp 45484ndash45490 2001

[91] E Matsui M Nishio H Yokoyama K Harata S Darnisand I Matsui ldquoDistinct domain functions regulating de novoDNA synthesis of thermostable DNA primase from hyperther-mophile Pyrococcus horikoshiirdquo Biochemistry vol 42 no 50 pp14968ndash14976 2003

[92] N Ito I Matsui and EMatsui ldquoMolecular basis for the subunitassembly of the primase from an archaeon Pyrococcus hori-koshiirdquoThe FEBS Journal vol 274 no 5 pp 1340ndash1351 2007

[93] M le Breton G Henneke C Norais et al ldquoThe heterodimericprimase from the euryarchaeon Pyrococcus abyssi a multifunc-tional enzyme for initiation and repairrdquo Journal of MolecularBiology vol 374 no 5 pp 1172ndash1185 2007

[94] S-H Lao-Sirieix and S D Bell ldquoThe heterodimeric primaseof the hyperthermophilic archaeon Sulfolobus solfataricus pos-sesses DNA and RNA primase polymerase and 31015840-terminalnucleotidyl transferase activitiesrdquo Journal of Molecular Biologyvol 344 no 5 pp 1251ndash1263 2004

[95] S-H Lao-Sirieix L Pellegrini and S D Bell ldquoThe promiscuousprimaserdquo Trends in Genetics vol 21 no 10 pp 568ndash572 2005

[96] J Hu L Guo K Wu B Liu S Lang and L Huang ldquoTemplate-dependent polymerization across discontinuous templatesby the heterodimeric primase from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquoNucleic Acids Research vol 40no 8 pp 3470ndash3483 2012

[97] E Evguenieva-Hackenberg P Walter E Hochleitner FLottspeich and G Klug ldquoAn exosome-like complex in Sulfolo-bus solfataricusrdquo EMBOReports vol 4 no 9 pp 889ndash893 2003

[98] P Walter F Klein E Lorentzen A Ilchmann G Klug andE Evguenieva-Hackenberg ldquoCharacterization of native andreconstituted exosome complexes from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Microbiology vol62 no 4 pp 1076ndash1089 2006

[99] Z Zuo C J Rodgers A L Mikheikin and M A Trak-selis ldquoCharacterization of a functional DnaG-type primase inarchaea implications for a dual-primase systemrdquo Journal ofMolecular Biology vol 397 no 3 pp 664ndash676 2010

[100] B R Berquist P DasSarma and S DasSarma ldquoEssential andnon-essential DNA replication genes in the model halophilicArchaeon Halobacterium sp NRC-1rdquo BMC Genetics vol 8article 31 2007

[101] D K Braithwaite and J Ito ldquoCompilation alignment andphylogenetic relationships of DNA polymerasesrdquo Nucleic AcidsResearch vol 21 no 4 pp 787ndash802 1993

[102] I K O Cann and Y Ishino ldquoArchaeal DNA replication iden-tifying the pieces to solve a puzzlerdquo Genetics vol 152 no 4 pp1249ndash1267 1999

[103] G Lipps S Rother C Hart and G Krauss ldquoA novel typeof replicative enzyme harbouring ATpase primase and DNApolymerase activityrdquo The EMBO Journal vol 22 no 10 pp2516ndash2525 2003

[104] J Yamtich and J B Sweasy ldquoDNA polymerase family X func-tion structure and cellular rolesrdquoBiochimica et BiophysicaActavol 1804 no 5 pp 1136ndash1150 2010

[105] H Ohmori E C Friedberg R P P Fuchs et al ldquoThe Y-familyof DNA polymerasesrdquoMolecular Cell vol 8 no 1 pp 7ndash8 2001

[106] N Y Yao R E Georgescu J Finkelstein and M E OrsquoDonnellldquoSingle-molecule analysis reveals that the lagging strandincreases replisome processivity but slows replication forkprogressionrdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 106 no 32 pp 13236ndash132412009

[107] U Hubscher G Maga and S Spadari ldquoEukaryotic DNA poly-merasesrdquo Annual Review of Biochemistry vol 71 pp 133ndash1632002

[108] F Boudsocq S Iwai F Hanaoka and R Woodgate ldquoSulfolobussolfataricus P2 DNA polymerase IV (Dp04) an archaeal DinB-like DNA polymerase with lesion-bypass properties akin toeukaryotic pol120578rdquo Nucleic Acids Research vol 29 no 22 pp4607ndash4616 2001

[109] L-J Lin A Yoshinaga Y Lin et al ldquoMolecular analyses ofan unusual translesion DNA polymerase fromMethanosarcinaacetivorans C2Ardquo Journal of Molecular Biology vol 397 no 1pp 13ndash30 2010

[110] I K O Cann S Ishino NNomura Y Sako andY Ishino ldquoTwofamily B DNA polymerases from Aeropyrum pernix an aerobichyperthermophilic crenarchaeoterdquo Journal of Bacteriology vol181 no 19 pp 5984ndash5992 1999

[111] T Uemori Y Ishino H Doi and I Kato ldquoThe hyperther-mophilic archaeon Pyrodictium occultum has two 120572-like DNApolymerasesrdquo Journal of Bacteriology vol 177 no 8 pp 2164ndash2177 1995

[112] T Uemori Y Ishino H Toh K Asada and I Kato ldquoOrgani-zation and nucleotide sequence of the DNA polymerase genefrom the archaeon Pyrococcus furiosusrdquo Nucleic Acids Researchvol 21 no 2 pp 259ndash265 1993

[113] B A Connolly ldquoRecognition of deaminated bases by archaealfamily-B DNA polymerasesrdquo Biochemical Society Transactionsvol 37 no 1 pp 65ndash68 2009

[114] B A Connolly M J Fogg G Shuttleworth and B T WilsonldquoUracil recognition by archaeal family B DNA polymerasesrdquoBiochemical Society Transactions vol 31 no 3 pp 699ndash7022003

[115] T T Richardson X Wu B J Keith P Heslop A C Jones andB A Connolly ldquoUnwinding of primer-templates by archaealfamily-B DNA polymerases in response to template-stranduracilrdquo Nucleic Acids Research vol 41 no 4 pp 2466ndash24782013

[116] T Lindahl ldquoInstability and decay of the primary structure ofDNArdquo Nature vol 362 no 6422 pp 709ndash715 1993

[117] I B Rogozin K S Makarova Y I Pavlov and E V Koonin ldquoAhighly conserved family of inactivated archaeal B family DNApolymerasesrdquo Biology Direct vol 3 article 32 2008

[118] M Imamura T Uemori I Kato and Y Ishino ldquoA non-120572-like DNA polymerase from the hyperthermophilic archaeonPyrococcus furiosusrdquoBiological andPharmaceutical Bulletin vol18 no 12 pp 1647ndash1652 1995

[119] I K O Cann K Komori H Toh S Kanai and Y IshinoldquoA heterodimeric DNA polymerase evidence that members ofEuryarchaeota possess a distinct DNA polymeraserdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 95 no 24 pp 14250ndash14255 1998

[120] L Aravind D D Leipe and E V Koonin ldquoToprimmdasha con-served catalytic domain in type IA and II topoisomerases

14 Archaea

DnaG-type primases OLD family nucleases and RecR pro-teinsrdquo Nucleic Acids Research vol 26 no 18 pp 4205ndash42131998

[121] M Jokela A Eskelinen H Pospiech J Rouvinen and J ESyvaoja ldquoCharacterization of the 31015840 exonuclease subunit DP1of Methanococcus jannaschii replicative DNA polymerase DrdquoNucleic Acids Research vol 32 no 8 pp 2430ndash2440 2004

[122] T Uemori Y Sato I Kato H Doi and Y Ishino ldquoA novel DNApolymerase in the hyperthermophilic archaeon Pyrococcus fur-iosus gene cloning expression and characterizationrdquo Genes toCells vol 2 no 8 pp 499ndash512 1997

[123] Y Shen K Musti M Hiramoto H Kikuchi Y Kawarabayashiand I Matsui ldquoInvariant Asp-1122 and Asp-1124 are essentialresidues for polymerization catalysis of family D DNA poly-merase from Pyrococcus horikoshiirdquo The Journal of BiologicalChemistry vol 276 no 29 pp 27376ndash27383 2001

[124] G Henneke D Flament U Hubscher J Querellou and J-P Raffin ldquoThe hyperthermophilic euryarchaeota Pyrococcusabyssi likely requires the two DNA polymerases D and B forDNA replicationrdquo Journal of Molecular Biology vol 350 no 1pp 53ndash64 2005

[125] L Cubonova T Richardson B W Burkhart et al ldquoArchaealDNA polymerase D but not DNA polymerase B is required forgenome replication in Thermococcus kodakarensisrdquo Journal ofBacteriology vol 195 no 10 pp 2322ndash2328 2013

[126] C Rouillon G Henneke D Flament J Querellou and J-PRaffin ldquoDNA polymerase switching on homotrimeric PCNA atthe replication fork of the euryarchaea Pyrococcus abyssirdquo Jour-nal of Molecular Biology vol 369 no 2 pp 343ndash355 2007

[127] G Henneke ldquoIn vitro reconstitution of RNA primer removal inArchaea reveals the existence of two pathwaysrdquoTheBiochemicalJournal vol 447 no 2 pp 271ndash280 2012

[128] G-LMoldovan B Pfander and S Jentsch ldquoPCNA themaestroof the replication forkrdquo Cell vol 129 no 4 pp 665ndash679 2007

[129] X-P Kong R Onrust M OrsquoDonnell and J Kuriyan ldquoThree-dimensional structure of the 120573 subunit of E coli DNA poly-merase III holoenzyme a sliding DNA clamprdquo Cell vol 69 no3 pp 425ndash437 1992

[130] K Daimon Y Kawarabayasi H Kikuchi Y Sako and Y IshinoldquoThree proliferating cell nuclear antigen-like proteins foundin the hyperthermophilic archaeon Aeropyrum pemix interac-tions with the two DNA polymerasesrdquo Journal of Bacteriologyvol 184 no 3 pp 687ndash694 2002

[131] I Dionne R K Nookala S P Jackson A J Doherty andS D Bell ldquoA heterotrimeric PCNA in the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Cell vol 11 no 1pp 275ndash282 2003

[132] E Warbrick ldquoPCNA binding through a conserved motifrdquoBioEssays vol 20 no 3 pp 195ndash199 1998

[133] H Nishida K Mayanagi S Kiyonari et al ldquoStructural deter-minant for switching between the polymerase and exonucleasemodes in the PCNA-replicative DNA polymerase complexrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 106 no 49 pp 20693ndash20698 2009

[134] K Mayanagi S Kiyonari H Nishida et al ldquoArchitecture of theDNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complexrdquo Proceedings of the National Academy ofSciences of the United States of America vol 108 no 5 pp 1845ndash1849 2011

[135] B Castrec C Rouillon G Henneke D Flament J Querellouand J-P Raffin ldquoBinding to PCNA in Euryarchaeal DNA

replication requires two PIP motifs for DNA polymerase D andone PIP motif for DNA polymerase Brdquo Journal of MolecularBiology vol 394 no 2 pp 209ndash218 2009

[136] P F Pluchon T Fouqueau C Creze et al ldquoAn extendednetworkof genomic maintenance in the archaeon Pyrococcus abyssihighlights unexpected associations between eucaryotic homo-logsrdquo PLoS One vol 8 no 11 Article ID e79707 2013

[137] J E Ladner M Pan J Hurwitz and Z Kelman ldquoCrystalstructures of two active proliferating cell nuclear antigens(PCNAs) encoded byThermococcus kodakaraensisrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2711ndash2716 2011

[138] Y Kuba S Ishino T Yamagami et al ldquoComparative analyses ofthe two proliferating cell nuclear antigens from the hyperther-mophilic archaeonThermococcus kodakarensisrdquo Genes to Cellsvol 17 no 11 pp 923ndash937 2012

[139] T Fukui H Atomi T Kanai R Matsumi S Fujiwara andT Imanaka ldquoComplete genome sequence of the hyperther-mophilic archaeon Thermococcus kodakaraensis KOD1 andcomparison with Pyrococcus genomesrdquo Genome Research vol15 no 3 pp 352ndash363 2005

[140] D Jeruzalmi O Yurieva Y Zhao et al ldquoMechanism of proces-sivity clamp opening by the delta subunit wrench of the clamploader complex of E coliDNApolymerase IIIrdquoCell vol 106 no4 pp 417ndash428 2001

[141] Y Shiomi J Usukura Y Masamura et al ldquoATP-dependentstructural change of the eukaryotic clamp-loader protein repli-cation factor Crdquo Proceedings of the National Academy of Sciencesof the United States of America vol 97 no 26 pp 14127ndash141322000

[142] T Miyata T Oyama K Mayanagi S Ishino Y Ishino and KMorikawa ldquoThe clamp-loading complex for processive DNAreplicationrdquoNature Structural andMolecular Biology vol 11 no7 pp 632ndash636 2004

[143] T Oyama Y Ishino I K O Cann S Ishino and K MorikawaldquoAtomic structure of the clamp loader small subunit fromPyrococcus furiosusrdquo Molecular Cell vol 8 no 2 pp 455ndash4632001

[144] A Seybert D J Scott S Scaife M R Singleton and DB Wigley ldquoBiochemical characterisation of the clampclamploader proteins from the euryarchaeon Archaeoglobus fulgidusrdquoNucleic Acids Research vol 30 no 20 pp 4329ndash4338 2002

[145] Y-H Chen Y Lin A Yoshinaga et al ldquoMolecular analyses of athree-subunit euryarchaeal clamp loader complex from Meth-anosarcina acetivoransrdquo Journal of Bacteriology vol 191 no 21pp 6539ndash6549 2009

[146] Y-H Chen S A Kocherginskaya Y Lin et al ldquoBiochemicaland mutational analyses of a unique clamp loader complex inthe archaeon Methanosarcina acetivoransrdquo The Journal of Bio-logical Chemistry vol 280 no 51 pp 41852ndash41863 2005

[147] F Matsunaga C Norais P Forterre and H Myllykallio ldquoIden-tification of short ldquoeukaryoticrdquo Okazaki fragments synthesizedfrom a prokaryotic replication originrdquo EMBO Reports vol 4no 2 pp 154ndash158 2003

[148] H Kochiwa M Tomita and A Kanai ldquoEvolution of ribonucle-ase H genes in prokaryotes to avoid inheritance of redundantgenesrdquo BMC Evolutionary Biology vol 7 article 128 2007

[149] N OhtaniMHarukiMMorikawa and S Kanaya ldquoMoleculardiversities of RNases Hrdquo Journal of Bioscience and Bioengineer-ing vol 88 no 1 pp 12ndash19 1999

Archaea 15

[150] N Ohtani M Haruki M Morikawa R J Crouch M Itayaand S Kanaya ldquoIdentification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII fromBacillus subtilis classification of RNases H into three familiesrdquoBiochemistry vol 38 no 2 pp 605ndash618 1999

[151] N Ohtani H Yanagawa M Tomita and M Itaya ldquoIdentifi-cation of the first archaeal type 1 RNase H gene from Halobac-terium sp NRC-1 archaeal RNase HI can cleave an RNA-DNAjunctionrdquoThe Biochemical Journal vol 381 no 3 pp 795ndash8022004

[152] N Ohtani H Yanagawa M Tomita and M Itaya ldquoCleavage ofdouble-stranded RNA by RNase HI from a thermoacidophilicarchaeon Sulfolobus tokodaii 7rdquo Nucleic Acids Research vol 32no 19 pp 5809ndash5819 2004

[153] M A Nowak M C Boerlijst J Cooke and J M SmithldquoEvolution of genetic redundancyrdquo Nature vol 388 no 6638pp 167ndash170 1997

[154] A E Tomkinson S Vijayakumar J M Pascal and T Ellen-berger ldquoDNA ligases structure reactionmechanism and func-tionrdquo Chemical Reviews vol 106 no 2 pp 687ndash699 2006

[155] M Nakatani S Ezaki H Atomi and T Imanaka ldquoA DNAligase from a hyperthermophilic archaeon with unique cofactorspecificityrdquo Journal of Bacteriology vol 182 no 22 pp 6424ndash6433 2000

[156] Y Sun M S Seo J H Kim et al ldquoNovel DNA ligase with broadnucleotide cofactor specificity from the hyperthermophilic cre-narchaeon Sulfophobococcus zilligii influence of ancestral DNAligase on cofactor utilizationrdquo Environmental Microbiology vol10 no 12 pp 3212ndash3224 2008

[157] T R Beattie and S D Bell ldquoCoordination of multiple enzymeactivities by a single PCNA in archaeal Okazaki fragmentmaturationrdquo The EMBO Journal vol 31 no 6 pp 1556ndash15672012

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

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International Journal of

Volume 2014

Zoology

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Molecular Biology International

GenomicsInternational Journal of

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The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

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BioinformaticsAdvances in

Marine BiologyJournal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

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BioMed Research International

Evolutionary BiologyInternational Journal of

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ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

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International Journal of

Microbiology

4 Archaea

Methanohalobium evestigatum Z-7303 only possesses twoOrc1Cdc6 homologs Thus the ability to grow at extremelyhigh concentrations of salt and to maintain high intracellularsalt concentrations does not necessarily require a largenumber of Orc1Cdc6 homologsAlthoughmost members ofthe orderMethanomicrobiales possess two copies of this geneMethanoplanus petroleariusDSM 11571 possesses four copiesThus the number of Orc1Cdc6 homologs varies consider-ably among the euryarchaeotes In an extreme case repre-sentatives of the ordersMethanococcales andMethanopyralesdo not possess any recognizable homologs for the Orc1Cdc6protein [7 44] and the mechanics of replication initiation inthese archaea remain an intriguing unknown of the archaealreplication process

32 Initiation (DNA Unwinding and Primer Synthesis) AfterOrc1Cdc6 proteins bind to the origin of replication ahelicase is recruited to unwind the dsDNA In Bacteria thereplicative helicase is the homohexamer DnaB In eukaryotesthe most likely candidate for the replicative DNA helicase isthe MCM (minichromosome maintenance) complex whichis a heterohexamer that is activated when associated withother replicative proteins forming the CMG (Cdc45-MCM-GINS) complex [45ndash48] As in eukaryotes in Archaea themost probable candidate for the replicative helicase is theMCM complex Intriguingly theMCM complexes in eukary-otes and archaea possess a 31015840-51015840 unwinding polarity but thebacterialDnaBhelicase unwinds duplexDNAon the oppositedirection with a distinct 51015840-31015840 polarity [49ndash51]

Most archaeal genomes studied so far encode one MCMhomolog Its helicase activity has been demonstrated invitro for several archaea including Methanothermobacterthermautotrophicus ΔH where the MCM protein forms adimer of hexamers [52 53] The in vivo interaction betweenthe MCM complex and the Orc1Cdc6 proteins has beendemonstrated in other Archaea [54ndash56] Indeed through anin vitro recruiting assay Orc1CDC6 from P furiosus has beendemonstrated as the possible recruiter of the MCM complexto the origin of replication [57] A recent study identifiedthirteen species of archaeawithmultiplemcm genes encodingthe MCM complexes (Figure 1 [58]) The number of mcmhomologs is especially high in the order Methanococcaleswhere different representatives possess from 2 to 8 copies[59 60] For instance Methanococcus maripaludis S2 pos-sesses four homologs of the MCM protein [44] Through ashotgun proteomic study peptides for three of them havebeen detected [61] suggesting that multiple MCMs areexpressed and functional However a genome-wide surveyof gene functionality in M maripaludis demonstrated thatonly one of these genes MMP0030 was likely to be essentialfor growth [62] In addition coexpression of recombinantMCMs from M maripaludis S2 allowed copurification ofall four proteins [59] suggesting that M maripaludis mayform a heterologous multimeric MCM complex Howeverbecause MMP0030 protein is the only mcm gene essentialfor growth a homologous multimeric complex may alsobe possible Similar results have been found in Thermo-coccus kodakaraensis in which three MCM homologs arepresent but only one is essential [63] The T kodakaraensis

MCM system is suggested to form homologous multimericcomplexes [64] A recent study proposed that two of theMCMhomologs that are conserved among representatives ofthe order Methanococcales are a consequence of an ancientduplication that occurred prior to the divergence of thisgroup [59] It has also been proposed that the large numberof MCM homologs in the order Methanococcales is a directconsequence of mobile elements which may have takenadvantage of the ancient duplication of the MCM genes totake over the replication system by forming cellular MCMheterocomplexes [58] In any case the large number of MCMhomologs in the order Methanococcales may be a product ofan intricate and complex evolutionary history Whether ornot it is related to the absence of the replication initiationprotein Orc1Cdc6 is an interesting possibility [58]

In eukaryotes the MCM complex is not active on itsown and requires the association of two accessory factorsthe heterotetrameric GINS complex (from the Japanese go-ishi-ni-san meaning 5-1-2-3 after the four subunits Sld5Psf1 Psf2 and Psf3) and the Cdc45 protein This complexcalled CMG (Cdc45-MCM-GINS) is thought to be the activereplicative helicase [47] Homologs for GINS subunits havebeen identified in Archaea by bioinformatics analysis Onehomolog is most similar to the eukaryotic proteins Psf2and Psf3 (GINS23) and is common in the crenarchaeotesAnother homolog is most similar to the eukaryotic pro-teins Psf1 and Sld5 (GINS15) and is found largely in theeuryarchaeotes [65] The GINS complex is expected to beessential for DNA replication but the distribution of thesetwo different GINS homologs suggests that the presence ofone of them is sufficient for archaeal DNA replication SomeCrenarchaeota (S solfataricus) and some Euryarchaeota (Pfuriosus and T kodakaraensis) possess both homologs andform heterotetramers similar to the ones found in eukaryoteswith a ratio 2 2 [66ndash68] To find homologs of GINS15 andGINS23 in Archaea two known GINS15 (from Sulfolobussolfataricus P2 and Thermococcus gammatolerans EJ3) andthree known GINS23 (from Sulfolobus solfataricus P2 Pyro-coccus yayanosii CH1 andThermococcus gammatolerans EJ3)were used for homology searches These analyses failed toidentifyGINShomologs in several archaeal groups (Figure 1)These results suggest that there are other unknown GINShomologs in archaea or that the sequences have divergedenough between genera not to be recognized by homologysearches In any case a more comprehensive analysis of GINSproteins is necessary to fully understand their function anddistribution in Archaea

The detailed interactions of the GINS andMCM proteinsin archaea appear to be highly variable Although the Ssolfataricus GINS and MCM proteins physically interactin vitro MCM helicase activity was not stimulated in thecomplex [66] In contrast the MCM helicase activity of Tkodakaraensis and P furiosus is clearly stimulated by theirGINS complexes [64 67] The crystal structure of the GINScomplex of T kodakaraensis was recently determined Thebackbone structure and the assembly are similar to thehuman complex with some notable differences [68] Interest-ingly many other euryarchaeotes possess only the homologto GINS15 One of those Thermoplasma acidophilum forms

Archaea 5

a homotetrameric complex [68 69] Moreover in vitro the Tacidophilum MCM helicase activity was not affected by theGINS complex [69] These results suggest that other proteinsmay be involved in the formation of a stable helicase in manyArchaea M maripaludis S2 possesses a hypothetical proteinwhich may correspond to the gene encoding for GINS15which is probably essential for growth [60 62] No homologsof GINS23 are present in the genome ofM maripaludis

The replication related Cdc45 protein is ubiquitous ineukaryotes but its exact role has not yet been elucidatedInterestingly homologs of the Cdc45 protein are not presentin Archaea However a bioinformatics analysis revealed thatthe eukaryotic Cdc45 and the prokaryotic RecJ which is aconserved 51015840-31015840exonuclease in most bacteria and archaeapossess a common ancestry and share a homologous DHHdomain [70] These results suggest that the archaeal RecJmay substitute for the eukaryotic Cdc45 during replicationCircumstantial evidence supports this conclusion In S solfa-taricus a homolog of the DNA binding domain of RecJ waspurified together with a GINS protein [66] Similarly in Tkodakaraensis the RecJ homolog (TK1252p) copurified withproteins of theGINS complex [71] and formed a stable in vitroassociation with the GINS complex [72] Two RecJ homologsare found inM jannaschii (MJ0977 and 0831) and they par-tially complement a recJ mutation in E coliThe recombinantMJ0977 also possesses high levels of thermostable single-stranded DNA degrading activity similar to RecJ [73] In Mmaripaludis S2 four proteins possess the DHH domain withsimilarity to the M jannaschii RecJ homologs (MMP16820547 1078 and 1314) However none of them was essentialfor growth suggesting that the activities were redundant [62]Alternatively another protein which has a low similaritywith M jannaschii RecJ homolog (MMP0285) but possessesthe DHH domain was possibly essential for growth [62]However this protein possesses other domains related totransport which make it an unlikely candidate for RecJThese results are not definitive and more experimental datais needed to assign a function to this protein

As soon as the DNA is unwound ssDNA is protectedfromnucleases chemicalmodification and other disruptionsby ssDNA binding proteins These proteins are present in allthree domains of life and are called SSB in Bacteria wherethey form homotetramers or homodimers [74 75] and RPA(replication protein A) in eukaryotes where they form astable heterotrimer composed of 70 32 and 14 kDa proteins[76] Although all ssDNA binding proteins contain dif-ferent combinations of the oligonucleotideoligosaccharide-binding fold or OB-fold [77] the sequence similarity is lowamong RPA and the bacterial SSBs [43] In Archaea differ-ent types of ssDNA binding proteins have been reportedIn crenarchaeotes an ssDNA binding protein is only wellcharacterized in S solfataricus The S solfataricus ssDNAbinding protein contains only one OB-fold and can adopt aheterotetramer conformation [78] However the protein alsoappears to exist as a monomer [79] This protein appears tobe more similar to the bacterial proteins in sequence but itsstructure is more similar to that of the eukaryotic RPAs [4380] While homologs are recognizable in other members ofthe Sulfolobales andmost otherArchaea they are absent from

the genomes of many members of the closely related orderThermoproteales with some few exceptions (Figure 1) [81]

RPAs have been studied from different representativesof the euryarchaeotes revealing additional diversity M jan-naschii andM thermautotrophicus possess a single RPA sub-unit which shares amino acid similarity with the eukaryoticRPA70 and possesses four and five OB-folds respectively [8283] P furiosus possesses three different RPA subunits whichform a stable heterotrimer that is involved in homologousrecombination in vitro [84] The P furiosus RPA thereforeis similar in subunit organization to the eukaryotic RPATheother members of the Thermococcales genera also possessthree RPA homologs which likely form the homotrimericcomplex described for P furiosus (Figure 1) Methanosarcinaacetivorans also possesses three different RPAproteins (RPA1-3) with four two and two OB-folds respectively Howeverthey do not interact with each other and appear to functionas homodimers [85] This arrangement is common amongthe Methanosarcinales but is not found in the closely relatedmethanogen orders such as the Methanocellales (Figure 1)Members of the order Methanococcales possess two to fourRPA homologs The genome of M maripaludis S2 containsthree possible RPA homologs (MMP0122 0616 and 1032)[60] Only MMP0616 and 1032 were likely to be essential forgrowth [62] suggesting a possible different complex configu-ration for RPA proteins in this archaeon It has been hypoth-esized that the diversity in OB-folds in the archaeal RPAs is adirect consequence of homologous recombination [86]

DNA synthesis starts with the production of a RNAprimer since the DNA polymerases that replicate genomesare incapable of de novo DNA synthesis The RNA primeris synthesized by a DNA-dependent RNA polymerase orprimase DnaG a single subunit protein is the primase inBacteria In eukaryotes a two-subunit primase consisting ofa small catalytic subunit (PriS) and a large subunit (PriL)is found in a complex with DNA polymerase 120572 and itsaccessory B subunit [87] In Archaea the first biochemicallycharacterized primase was the eukaryotic primase-like smallsubunit PriS in M jannaschii [88] Later homologs of thePriS and PriL subunits were described in several Pyrococ-cus species [89ndash93] The eukaryotic-like DNA primase hasalso been characterized in the crenarchaeote S solfataricus[94 95] where it has been shown to interact with MCMthrough GINS23 [66] A unique polymerization activityacross discontinuous DNA templates has been characterizedin the PriSL of S solfataricus suggesting that this primasemay be involved in double-stranded break repair in Archaea[96] So far the eukaryotic-like primases found in archaeaexhibit similar properties PriS functions as the catalyticsubunit and PriL modulate its activity [87] In additionthe archaeal eukaryotic-like primase has the unique abilityto synthesize both DNA and RNA in vitro Indeed theP furiosus PriS synthesizes long DNA fragments but theaddition of PriL regulates the process by decreasing theDNA polymerase activity increasing the RNA polymeraseactivity and decreasing the product length [90] Additionallystudies of the P abyssi enzyme suggest that DNA primasemay also be involved in DNA repair because of the DNApolymerase gap filling and strand displacement activities

6 Archaea

also present in vitro [93] Interestingly the archaeal primasesmall subunit resembles DNA polymerases from the Pol Xfamily in sequence and structure suggesting a similarity intheir catalytic mechanism [96]

Homologs of the bacterial DnaG primase are also foundin archaea However in vitro studies of the P furiosusenzyme failed to detect primer synthesis activity and the TkodakaraensisDnaG was copurified with proteins of the exo-some [71] Also in S solfataricus DnaG primase was found tobe a core exosome subunit involved in RNA degradation [9798] However recent studies demonstrated that the S solfa-taricus DnaG homolog has limited primer synthesis activityand a dual primase system with PriSL has been proposed tofunction during DNA replication [99] Hu et al hypothesizedan interesting theory which suggests that LUCA employed adual-primase system comprisingDnaG and PriSL which alsoserved roles in RNA degradation and the nonhomologousend joining (NHEJ) pathwayThe system was inherited by allthree domains In theArchaea domain it retained its originalfunctions However in the Bacteria domain DnaG becamethe major replicative primase and PriSL evolved into the Poldomain of LigD involved in the NHEJ pathway In contrastDnaG was lost in the Eukaryota domain and PriSL becamethe only replicative primase In addition it also evolved intothe DNA Pol X family involved in NHEJ [96]

Like other ArchaeaM maripaludis S2 possesses both theeukaryotic- and bacterial-like primases A new genome-widesurvey of this methanoarchaea revealed that genes encodingboth subunits of the eukaryotic like primase PriS and PriL(MMP0009 and MMP0071) were likely to be essential forgrowth which is consistent with a role in replication Similarobservations have been demonstrated in other Archaea suchas Halobacterium sp NRC-1and Haloferax volcanii [93 100]In contrast the DnaG primase (MMP1286) was nonessentialwhich would be consistent with a role in the exosome [62]These results suggest that in M maripaludis and probablyother euryarchaeotes a dual primase system is not pre-sent

33 Elongation (Replicative DNA Polymerase) The primersynthesized by the primase is further extended by a replicativeDNA polymerase DNA polymerases have been classifiedinto seven families based on their amino acid sequencesimilarity (A B C D E X and Y) [101ndash105] In Bacteria Ecoli possesses five DNA polymerases Pol IndashV where the firstthree belong to families A B and C respectively and the lasttwo belong to the Y family The major replicative DNA poly-merase in E coli is Pol III a member of the C family whichsynthesizes DNA with high processivity when functioningwithin the holoenzyme [106] In eukaryotes a great diversityof DNA polymerases is also found but DNA replicationrequires three replicative DNA polymerases which belongto family B (Pol120572 Pol120575 and Pol120576) [107] In Archaea fewertypes of DNA polymerases are present but they have aninteresting evolutionary division Representatives of theDNApolymerase B family are found in all Archaea The D familyDNA polymerase is present in every phyla studied so farwith the exception of the Crenarchaeota (Figure 1) Lastly amember of theY family has been identified andbiochemically

characterized in S solfataricus [108] and the Methanosarci-nales in which several species harbor two homologs [109]Even though the activity of DNA polymerases belongingto the Y family in archaea is not fully understood they aresuggested to play an important role in DNA repair [109]

Representatives of the DNA polymerase family B havebeen identified in all Archaea The crenarchaeotes possess atleast two family B DNA polymerases (PolB I and PolB IIand in some cases PolB III) [102 110 111] The recombinantS solfataricus Pyrodictium occultum and A pernix enzymeshave been characterized [102] In contrast euryarchaeotesonly contain PolB I The recombinant P furiosus enzymehas been characterized [112] The PolB I enzymes havesimilar amino acid sequence and overall structure and theypossess a potent 31015840-51015840exonuclease proofreading activity [102]A unique property of the archaeal family B DNA polymeraseis the ability to stall DNA polymerization in the presenceof uracil or hypoxanthine deaminated bases [113 114] thisproperty helps to prevent the copy of template-strand uraciland the transmission of fixed mutations to progeny [115]Commonly cytosine deamination converts GC base pairsinto the promutagenic GU mismatches which result in50 of the offspring containing an AT transition mutationafter replication [116] In addition when A-U base pairs areformed the loss of the 5-methyl moiety upon replacementof thymine can exert a detrimental effect on protein DNAinteractions Interestingly in some crenarchaeotes and eur-yarchaeotes one of the B family DNA polymerase paralogspossesses disrupted versions of the sequence motifs thatare essential for catalysis Possibly these enzymes possess astructural role [117]

DNA polymerase family D (PolD) is a novel enzyme thatwas originally discovered in P furiosus [118] It has sincethen been identified in all euryarchaeotes [119] For a longtime this enzyme was considered a euryarchaeote-specificpolymerase but the three newly discovered archaeal phylawere also found to possess genes for PolD [14ndash16] PolD isa heterodimer with a small subunit (DP1) and a large subunit(DP2) It has been proposed that the large subunit harborsthe polymerase activity although its sequence is very differentfrom other hitherto described DNA polymerases The smallsubunit possesses high similarity with the noncatalytic B-subunits of the eukaryoticDNApolymerases120572 120575 and 120576 [120]Studies of the M jannaschii enzyme demonstrated that thesmall subunit possesses a strong 31015840-51015840exonuclease activitysuggesting that it may be involved in proofreading activity[7 121] Efficient polymerase and proofreading activity havealso been detected from a purified PolD of P furiosus andthe residues Asp-1122 and Asp-1124 are essential for thepolymerization reaction in P horikoshii [122 123] Everyeuryarchaeote examined possessed one homolog for DP1 andDP2 except forMethanococcoides burtoniiDSM 6242 whichpossesses two homologs for DP1 (Figure 1)

Because the crenarchaeotes only possess family B DNApolymerases one of themmust be the replicative polymeraseHowever in euryarchaeotes it was not clear which enzymewas involved in replication Studies in Halobacterium spNRC-1 showed that both PolB and PolD were essential forviability and it was proposed that they could be working

Archaea 7

together at the replication fork synthesizing the leading andlagging strand respectively [100 124] However in otherEuryarchaeota PolB does not appear to be essential Forinstance a recent report demonstrated that both subunits ofPolDwere essential but PolB was nonessential for the growthof M maripaludis S2 [62] Likewise in T kodakaraensisPolD can be coisolated with different proteins of the archaealreplication fork but PolB wasmainly coisolated with proteinsof unknown function [71] A deletion of the PolB in Tkodakaraensis also had no detectable effect on cell viability[125] Interestingly T kodakaraensis PolB mutants haveincreased sensitivity to UV radiation These results togethersuggest that PolD is the essential replicative DNA polymerasein these euryarchaeotes and not a PolB family polymeraseIn this scenario PolB may have some other crucial functionin Halobacterium and possibly other closely related specieswhich it is not conserved throughout the phylum Finallyit has been demonstrated that purified PolD from P abyssiis able to perform strand displacement and RNA primerextension in vitro Purified PolB on its own cannot performthese activities in vitro but in the presence of PCNA stranddisplacement activity is stimulated [124 126] A recent in vitrostudy in P abyssi demonstrated that RNase HII is required toinitiate strand displacement DNA synthesis by PolB [127]

34 Elongation (Other Accessory Proteins) Purified DNApolymerases possess low processivity however the addi-tion of an accessory factor the sliding clamp gives DNApolymerases the required processivity to replicate genomesThis factor whose structure resembles a doughnut functionsas a molecular platform which recruits several replication-associated enzymes and act together with DNA and thepolymerase to stabilize their interactions during replication[128] The structure of sliding clamps is conserved in thethree domains of life In Bacteria the sliding clamp or 120573-subunit is a homodimeric ring [129] In eukaryotes thesliding clamp or proliferating cell nuclear antigen (PCNA)is a homotrimeric ring [128] In Archaea the majority ofcrenarchaeotes have multiple PCNA homologs which formheterotrimeric rings [130 131] (Figure 1) In contrast mosteuryarchaeotes possess a single PCNA homolog (Figure 1)Interactions of DNA polymerase with the sliding clampare mediated through a common motif called the PCNAInteracting Protein (PIP) box [132] The three dimensionalstructures of PCNA-PolB and the PolB-PCNA-DNA complexfrom P furiosus have been solved shedding light on theinteractions between these molecules [133 134] In additiona study demonstrated that the PolDPCNA and PolBPCNAinteractions require two and one PIP boxes respectively[135] Recently through a protein-interaction network of Pabyssi a previously unknown protein with nuclease activity(Pab0431) and a PIP canonical motif was discovered tointeract with PCNA suggesting a possible involvement inDNA replication [136] T kodakaraensis is the only well-documented example of an euryarchaeotewith twohomologsfor PCNA TK0535 (PCNA1) and TK0582 (PCNA2) Recentwork demonstrated both proteins form stable homotrimericrings that interact with T kodakaraensis PolB in vitro [137]A more detailed study of the two homologs of PCNA in T

kodakaraensis demonstrated that both homologs stimulate invitro the primer extension activity of PolB but only PCNA1and not PCNA2 stimulates the same activity of PolD [138]Also the same report showed that the pcna2 gene can bedisrupted without causing growth deficiencies but it was notpossible to isolate mutants of pcna1 These results suggestthat PCNA1 but not PCNA2 is essential for DNA replication[138] It has been proposed that one of the PCNA geneswas acquired by lateral gene transfer [139] Members of theorderMethanococcales possess one PCNA homolog with twoexceptionsMmaripaludis S2 possesses twoPCNAhomologs(MMP1126 and 1711) [60] Both genes appeared to be essentialfor growth suggesting that they both play an importantrole in replication [62] The gene MMP1711 possesses highsimilarity to both T kodakaraensis genes and is likely thetrue methanococcal PCNA In contrast MMP1126 possessesonly low similarity to the T kodakaraensis genes and alsocontains an S-adenosylmethionine-dependent methyltrans-ferases domain Thus it is likely to possess some alternativefunction Methanotorris igneus Kol 5 also possesses twoPCNA homologs

For PCNA to assemble around DNA a specific loadingfactor is required In Bacteria the loading factor is knownas 120574-complex and comprises three different subunits ina 1205743-120575-1205751015840 stoichiometry [140] In eukaryotes the loading

factor is known as Replication Factor C (RFC) and is aheteropentameric complex comprising one large subunit andfour different small subunits [141] In contrast inArchaea theRFC consists of two different proteins a small subunit RFCSand a large subunit RFCLThey also form a heteropentamericcomplex in a 4 1 ratio (RFCS RFCL) Interestingly manycrenarchaeotes possess one homolog of RFCL and two orthree homologs of RFCS Alternatively most euryarchaeotespossess only one RFCL and RFCS homolog The exceptionsare somemembers of the ordersHalobacteriales Methanomi-crobiales and Methanosarcinales which possess two RFCShomologs (Figure 1) Structural and biochemical studies ofRFC have been conducted in several euryarchaeotes such asArchaeoglobus fulgidus and Pyrococcus species [142ndash144] Aninteresting case is observed in Methanosarcina acetivoransThis RFC possesses three subunits (RFC1 2 L) found ina ratio 3 1 1 [145] Homologs for these three subunits arealso present in most of the genomes of the haloarchaea[145] It is inferred that this type of RFC complex representsan intermediary form transitional between the canonicalarchaeal RFC complex of one small and one large subunit andthe eukaryotic RFC complex of four different small and onelarge subunit [146] The organization and spatial distributionexhibit a similarity to the E coliminimal 120574-complex but thefunction of the subunits is probably not conserved [145]

35 Maturation During DNA replication the lagging strandis discontinuously synthesized by extending the RNAprimersor Okazaki fragments This discontinuously synthesizedDNA strand requires maturation to form a single covalentlyclosed strand to end the replication process In ArchaeaOkazaki fragments were first demonstrated during replica-tion in P abyssi and Sulfolobus acidocaldarius [147] Duringreplication these RNA primers are replaced with DNA The

8 Archaea

removal of the primers is performed by the enzyme RNase Hwhich is ubiquitous in the three domains of life Accordingto their sequence similarity in prokaryotes the RNase Hproteins are classified into three groups RNase HI HII andHIII In eukaryotes they are classified as RNase H1 and H2[148] However phylogenetic analyses suggest that the RNaseH proteins can also be classified into two different groupsType 1 (prokaryotic RNaseHI eukaryotic RNaseH1 and viralRNase H) and Type 2 (prokaryotic RNase HII and HIII andeukaryotic RNase H2) [149] These two types of RNase Hpossess different specific activities metal ion preferences andcleavage sites [150] Originally it was thought that Archaeaonly possess type 2 RNase H [149] but several type 1 archaealRNase H enzymes have since then been discovered [151 152]Interestingly in eukaryotes RNaseH1 andH2 tend to coexistand different combinations of the three prokaryotic RNasesH(I II and III) are found except for the combination of RNasesHI and HIII This mutually exclusive evolution of some ofthe prokaryotic RNases seems to be related to functionalredundancy [148]

Another enzyme involved in primer replacement inDNA replication is the Flap endonuclease I (FEN-1) whichrecognizes double-strandedDNAwith an unannealed 51015840-flapand cleaves it A eukaryotic homolog of FEN-1 is found inevery archaeal member analyzed and one member of theThermoproteales Thermofilum pendens Hrk5 possesses twohomologs

M maripaludis S2 possesses genes for the prokaryoticRNase HI and HII and for FEN-1 but none are essentialsuggesting that they may be redundant in their functions[44 62] Possibly both RNase H proteins persist and areevolutionary stable in the genome The gene products mayperform the same function but one is less efficient than theother [153]

After the Okazaki fragments are replaced by DNA inthe lagging strand the nick between the newly synthesizedand the elongated DNA is repaired by a DNA ligase Thisenzyme uses a nucleotide cofactor to catalyze the formationof the phosphodiester bond in three well-characterized steps[154]The enzyme is common to all three domains but can begrouped into two families based on cofactor specificity (ATPor NAD+) The DNA ligases from several crenarchaeotes andeuryarchaeotes have been further characterized (reviewedin [43]) Many archaeal DNA ligases possess dual cofactorspecificity (ATPNAD+ or ATPADP) but every archaealDNA ligase characterized so far uses ATP A thermophilicDNA ligase from M thermautotrophicus which uses ATP assole cofactor was characterized in vitro [155] A characterizedDNA ligase from the crenarchaeote Sulfophobococcus zilligiidisplayed specificity for three cofactors (ATPNAD+GTP)[156]Major structuralwork in this enzymehas been achievedin P furiosus and S solfataricus and the findings have beenreviewed in detail [43] InM maripaludis S2 the DNA ligaseis likely to be essential for growth [44 62]

Understanding the maturation process in archaea hasbecome a focus of increasing research in recent years An invitro study reconstituted the Okazaki fragment maturationusing proteins derived from the crenarchaeote S solfataricusThey demonstrated that only six proteins are necessary for

coupled DNA synthesis RNA primer removal and DNAligation In this model a single PCNA (heterotrimeric ring)coordinates the activities of PolBI FEN-1 and DNA ligaseinto an efficient maturation complex [157] A different invitro study in P abyssi has demonstrated two different modelsfor Okazaki fragments maturation which differ in the RNAprimer removal process In the first model RNA primerelimination is executed by continuous PolD strand displace-ment DNA synthesis and 51015840RNA flap cleavage by FEN-1The resulting nicks are closed by DNA ligase Alternativelythe second model proposes that RNase HII cleaves theRNA primer followed by the action of FEN-1 and stranddisplacement DNA synthesis by polB or polD The nick isthen sealed by DNA ligase [127] Testing these models invivo is of great interest to complete the picture of how theseprocesses behave in the cell In addition other factors that canmodulate these processesmay be required for coordination ofthe in vivomaturation process

4 Conclusions

DNA replication in archaea possesses a dual nature wherethe machinery is structurally and functionally similar to theeukaryotic replication system but it is executed within abacterial context [11 25] Additionally unique archaeal fea-tures demonstrate the complexity of this process and it doesnot appear to be just a simplified version of the eukary-otic system For example the archaeal specific DNA poly-merase D is conserved across the Archaea domain with theexception of the Crenarchaeota phylumThe recent discoverythat it is the essential replicative polymerase in two differenteuryarchaeotic species demonstrates an unanticipated vari-ability in archaeal DNA replication and a fundamental differ-ence in the replication mechanism between crenarchaeotesand euryarchaeotes Interestingly the absence of PolD increnarchaeotes is not the only difference in DNA repli-cation These differences include the absence of histonesin crenarchaeotes [4] the presence of multiple origins ofreplication in crenarchaeotes and a single origin of repli-cation in most euryarchaeotes the absence of GINS23 inmost euryarchaeotes the absence of RPA protein in manycrenarchaeotes the presence of multiple MCM homologs inMethanococcales and the presence of one homolog of PCNAin euryarchaeotes compared to the multiple homologs increnarchaeotes These distinctive characteristics between thephyla highlight the complexity of archaeal DNA replicationand suggest a complex evolutionary history (Table 1)

Among the Euryarchaeota the ordersHalobacteriales andMethanococcales possess differences in the DNA replicationsystem that make them unique For instance Halobac-teriales possess many more origin recognition proteins(Orc1Cdc6) compared to the rest of the archaea On theother hand Methanococcales and Methanopyrales lack rec-ognizable homologs for the Orc1Cdc6 proteins suggestingthe presence of a very different mechanism for initiation ofreplication In addition the Methanococcales possess a largenumber of MCM protein homologs It has been proposedthat these distinctive features are connected and because ofthe absence of the Orc1Cdc6 proteins MCM proteins may

Archaea 9

Table1DNAreplicationproteins

andfeatures

inthed

omains

BacteriaEukaryotaand

thetwomajor

phylao

fthe

Archaeado

main

Mod

ified

from

[43]

DNAreplicationstage

Process

Bacteria

Eukaryota

Archaea

Crenarchaeota

Euryarchaeota

Preinitia

tion

Orig

inof

replication

Sing

leMultip

leMultip

leSing

lea

Orig

inrecogn

ition

DnaA

ORC

complex

(ORC

1-6)

Orc1C

dc6

Orc1C

dc6b

Initiation

DNAun

winding

(Helicase)

DnaB

MCM

complex

(MCM

2-7)

MCM

complex

MCM

complex

DNAun

winding

(Accessory

proteins)

DnaC

Cdc6

GIN

S23GIN

S15

GIN

S15c

Cdt1

GIN

Scomplex

(Sld5Psf1-3)

RecJho

molog

RecJho

molog

Cdc45

Prim

ersynthesis

DnaG

Pol120572

prim

asec

omplex

DNAprim

ase

(PriS

L)D

naG

dDNAprim

ase(PriSL)

Elon

gatio

n

DNAsynthesis

(polym

erase)

PolIII(Fam

ilyCDNApo

lymerase)

Pol120575and

Pol120576(Fam

ilyBDNA

polymerase)

Family

BDNApo

lymerase

Family

DDNA

polymerasee

DNAsynthesis

(Processivity

factors)

120574-com

plex

(clamploader)

RFC(clamploader)

RFC(clamploader)

RFC(clamploader)

120573-clamp(clamp)

PCNA(clamp)

PCNA(clamp)

PCNA(clamp)

Maturation

Maturation(O

kazaki

fragmentp

rocessing)

PolI

(family

ADNApo

lymerase)

Fen1D

na2

Fen1

Fen1

RNaseH

RNaseH

RNaseH

RNaseH

DNAligase

DNAligase

DNAligase

DNAligase

a Exceptio

ntheo

rder

Halobacteria

les

b Not

know

nform

embersof

theE

uryarchaeota

ordersMethanococcalesandMethanopyrales

c GIN

S23hasb

eenfoun

dedon

lyin

theo

rder

Thermococcales

oftheE

uryarchaeota

d Sulfolobu

ssolfataric

usdidshow

prim

asea

ctivity

invitro

e Fam

ilyBDNApo

lymeraseisa

lsoessentialinHalobacteriu

mB

ecause

itsfunctio

nhasn

otbeen

clearlyelu

cidateditmight

also

play

aroleinreplicationin

thisandclo

selyrelated

organism

s

10 Archaea

interact with other unknown initiation enzymes resultingin a complex phylogeny of the MCM homologs [49] Pre-sumably these differences also account for the inability torecognize the origin of replication in these microorganismsThis unique scenario for initiation of DNA replicationmay bea direct consequence of various processes such as duplicationmobile genetic elements and interactions with viruses [58]

The differences in DNA replication among archaealhigher taxa demonstrate an unexpected variability and sug-gest two alternative evolutionary models In the first modelDNA replication evolved late after the diversification ofthe archaeal lineages Because the replicative system wasnot fully formed it was possible to develop differentlybetween the lineages Once formed replication would thenbe highly conserved However this model is not consistentwith differences observed between lineages that must haveformed relatively late such as those between the orders oreven in some cases within certain orders The alternativemodel is that DNA replication has changed throughout theevolution of the archaea Thus differences in the replicativesystems may represent ancient as well as modern adaptationsto changing environments In this case differences in thereplicative systems may provide important insights into theevolutionary pressures in play during different episodes ofarchaeal evolution From this perspective the differencesbetween the eukaryotic and archaeal replicative systems maynot be evidence for an ancient origin of the eukaryotesInstead it is entirely plausible that the replicative system ineukaryotes could have evolved relatively late from a well-developed archaeal system

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] E F DeLong and N R Pace ldquoEnvironmental diversity ofbacteria and archaeardquo Systematic Biology vol 50 no 4 pp 470ndash478 2001

[2] B Chaban S Y M Ng and K F Jarrell ldquoArchaeal habitatsmdashfrom the extreme to the ordinaryrdquo Canadian Journal of Micro-biology vol 52 no 2 pp 73ndash116 2006

[3] M J Hanford and T L Peeples ldquoArchaeal tetraether lipidsunique structures and applicationsrdquo Applied Biochemistry andBiotechnology A vol 97 no 1 pp 45ndash62 2002

[4] K Sandman and J N Reeve ldquoArchaeal histones and the originof the histone foldrdquo Current Opinion in Microbiology vol 9 no5 pp 520ndash525 2006

[5] O Lecompte R Ripp J-C Thierry D Moras and O PochldquoComparative analysis of ribosomal proteins in complete gen-omes an example of reductive evolution at the domain scalerdquoNucleic Acids Research vol 30 no 24 pp 5382ndash5390 2002

[6] D R Edgell and W F Doolittle ldquoArchaea and the origin(s) ofDNA rplication poteinsrdquo Cell vol 89 no 7 pp 995ndash998 1997

[7] E R Barry and S D Bell ldquoDNA replication in the archaeardquoMicrobiology and Molecular Biology Reviews vol 70 no 4 pp876ndash887 2006

[8] S Gribaldo and C Brochier-Armanet ldquoThe origin and evolu-tion of archaea a state of the artrdquo Philosophical Transactions ofthe Royal Society B vol 361 no 1470 pp 1007ndash1022 2006

[9] P Londei ldquoEvolution of translational initiation new insightsfrom the archaeardquo FEMS Microbiology Reviews vol 29 no 2pp 185ndash200 2005

[10] B Grabowski and Z Kelman ldquoArchaeal DNA replicationeukaryal proteins in a bacterial contextrdquo Annual Review ofMicrobiology vol 57 pp 487ndash516 2003

[11] P Forterre J Filee and H Myllykallio ldquoOrigin and evolutionof DNA and DNA replication machineriesrdquo in The GeneticCode and the Origin of Life L Ribas Ed Landes BioscienceGeorgetown Tex USA 2007

[12] E V Koonin ldquoThe origin and early evolution of eukaryotesin the light of phylogenomicsrdquo Genome Biology vol 11 no 5article 209 2010

[13] M Konneke A E Bernhard J R de la Torre C B WalkerJ B Waterbury and D A Stahl ldquoIsolation of an autotrophicammonia-oxidizing marine archaeonrdquo Nature vol 437 no7058 pp 543ndash546 2005

[14] C Brochier-Armanet B Boussau S Gribaldo and P ForterreldquoMesophilic crenarchaeota proposal for a third archaeal phy-lum theThaumarchaeotardquoNature Reviews Microbiology vol 6no 3 pp 245ndash252 2008

[15] J G Elkins M Podar D E Graham et al ldquoA korarchaealgenome reveals insights into the evolution of the ArchaeardquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 105 no 23 pp 8102ndash8107 2008

[16] T Nunoura Y Takaki J Kakuta et al ldquoInsights into theevolution of Archaea and eukaryotic protein modifier systemsrevealed by the genome of a novel archaeal grouprdquoNucleic AcidsResearch vol 39 no 8 pp 3204ndash3223 2011

[17] HHuberM J Hohn R Rachel T Fuchs V CWimmer andKO Stetter ldquoAnewphylumofArchaea represented by a nanosizedhyperthermophilic symbiontrdquoNature vol 417 no 6884 pp 63ndash67 2002

[18] C Brochier S Gribaldo Y Zivanovic F Confalonieri and PForterre ldquoNanoarchaea representatives of a novel archaeal phy-lum or a fast-evolving euryarchaeal lineage related to Therm-ococcalesrdquo Genome Biology vol 6 no 5 article R42 2005

[19] S J Aves ldquoDNA replication initiationrdquo Methods in MolecularBiology vol 521 pp 3ndash17 2009

[20] N P Robinson I Dionne M Lundgren V L Marsh RBernander and S D Bell ldquoIdentification of two origins ofreplication in the single chromosome of the archaeon Sulfolobussolfataricusrdquo Cell vol 116 no 1 pp 25ndash38 2004

[21] M Lundgren A Andersson L Chen P Nilsson and RBernander ldquoThree replication origins in Sulfolobus speciessynchronous initiation of chromosome replication and asyn-chronous terminationrdquo Proceedings of the National Academy ofSciences of theUnited States of America vol 101 no 18 pp 7046ndash7051 2004

[22] N P Robinson and S D Bell ldquoExtrachromosomal element cap-ture and the evolution ofmultiple replication origins in archaealchromosomesrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 104 no 14 pp 5806ndash58112007

[23] E A Pelve A C Lindas A Knoppel A Mira and R Bernan-der ldquoFour chromosome replication origins in the archaeonPyrobaculum calidifontisrdquo Molecular Microbiology vol 85 no5 pp 986ndash995 2012

Archaea 11

[24] A F Andersson E A Pelve S LindebergM Lundgren P Nils-son and R Bernander ldquoReplication-biased genome organisa-tion in the crenarchaeon Sulfolobusrdquo BMCGenomics vol 11 no1 article 454 2010

[25] H Myllykallio P Lopez P Lopez-Garcıa et al ldquoBacterial modeof replication with eukaryotic-like machinery in a hyperther-mophilic archaeonrdquo Science vol 288 no 5474 pp 2212ndash22152000

[26] F Matsunaga P Forterre Y Ishino and H Myllykallio ldquoInvivo interactions of archaeal Cdc6Orc1 and minichromosomemaintenance proteins with the replication originrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 98 no 20 pp 11152ndash11157 2001

[27] S Maisnier-Patin L Malandrin N K Birkeland and RBernander ldquoChromosome replication patterns in the hyper-thermophilic euryarchaeaArchaeoglobus fulgidus andMethano-caldococcus (Methanococcus) jannaschiirdquo Molecular Microbiol-ogy vol 45 no 5 pp 1443ndash1450 2002

[28] R Zhang and C-T Zhang ldquoMultiple replication origins ofthe archaeon Halobacterium species NRC-1rdquo Biochemical andBiophysical Research Communications vol 302 no 4 pp 728ndash734 2003

[29] C Norais M Hawkins A L Hartman J A Eisen H Myl-lykallio and T Allers ldquoGenetic and physical mapping of DNAreplication origins in Haloferax volcaniirdquo PLoS Genetics vol 3no 5 article e77 2007

[30] J A Coker P DasSarma M Capes et al ldquoMultiple replicationorigins of Halobacterium sp strain NRC-1 properties of theconserved orc7-dependent oriC1rdquo Journal of Bacteriology vol191 no 16 pp 5253ndash5261 2009

[31] Z Wu J Liu H Yang H Liu and H Xiang ldquoMultiple repli-cation origins with diverse control mechanisms in Haloarculahispanicardquo Nucleic Acids Research 2013

[32] M Hawkins S Malla M J Blythe C A Nieduszynski and TAllers ldquoAccelerated growth in the absence of DNA replicationoriginsrdquo Nature vol 503 no 7477 pp 544ndash547 2013

[33] A I Majernık and J P J Chong ldquoA conserved mechanismfor replication origin recognition and binding in archaeardquo TheBiochemical Journal vol 409 no 2 pp 511ndash518 2008

[34] J E Galagan C Nusbaum A Roy et al ldquoThe genome of Macetivorans reveals extensive metabolic and physiological diver-sityrdquo Genome Research vol 12 no 4 pp 532ndash542 2002

[35] R Zhang and C-T Zhang ldquoIdentification of replication originsin archaeal genomes based on the Z-curve methodrdquo Archaeavol 1 no 5 pp 335ndash346 2005

[36] A Spang R Hatzenpichler C Brochier-Armanet et al ldquoDis-tinct gene set in two different lineages of ammonia-oxidizingarchaea supports the phylum Thaumarchaeotardquo Trends inMicrobiology vol 18 no 8 pp 331ndash340 2010

[37] K J Marians ldquoProkaryotic DNA replicationrdquo Annual Review ofBiochemistry vol 61 pp 673ndash719 1992

[38] S P Bell ldquoThe origin recognition complex from simple originsto complex functionsrdquo Genes and Development vol 16 no 6pp 659ndash672 2002

[39] V L Marsh and S D Bell ldquoDNA replication and the cell cyclerdquoin Archaea Evolution Physiology and Molecular Biology R AGarrett and H P Klenk Eds Blackwell Publishing HobokenNJ USA 2007

[40] F Matsunaga A Glatigny M-H Mucchielli-Giorgi et alldquoGenomewide and biochemical analyses of DNA-binding activ-ity of Cdc6Orc1 and Mcm proteins in Pyrococcus sprdquo NucleicAcids Research vol 35 no 10 pp 3214ndash3222 2007

[41] J Liu C L Smith D DeRyckere K DeAngelis G S Martinand J M Berger ldquoStructure and function of Cdc6Cdc18implications for origin recognition and checkpoint controlrdquoMolecular Cell vol 6 no 3 pp 637ndash648 2000

[42] M R Singleton R Morales I Grainge N Cook M NIsupov and D B Wigley ldquoConformational changes inducedby nucleotide binding in Cdc6ORC from Aeropyrum pernixrdquoJournal of Molecular Biology vol 343 no 3 pp 547ndash557 2004

[43] Y Ishino and S Ishino ldquoRapid progress of DNA replicationstudies in Archaea the third domain of liferdquo Science China LifeSciences vol 55 no 5 pp 386ndash403 2012

[44] E L Hendrickson R Kaul Y Zhou et al ldquoComplete genomesequence of the genetically tractable hydrogenotrophic meth-anogen Methanococcus maripaludisrdquo Journal of Bacteriologyvol 186 no 20 pp 6956ndash6969 2004

[45] B K Tye ldquoMCM proteins in DNA replicationrdquo Annual Reviewof Biochemistry vol 68 pp 649ndash686 1999

[46] K Labib and J F X Diffley ldquoIs the MCM2-7 complex theeukaryotic DNA replication fork helicaserdquo Current Opinion inGenetics amp Development vol 11 no 1 pp 64ndash70 2001

[47] I Ilves T Petojevic J J Pesavento and M R Botchan ldquoActi-vation of the MCM2-7 helicase by association with Cdc45 andGINS proteinsrdquoMolecular Cell vol 37 no 2 pp 247ndash258 2010

[48] M L Bochman andA Schwacha ldquoTheMcm complex unwind-ing the mechanism of a replicative helicaserdquo Microbiology andMolecular Biology Reviews vol 73 no 4 pp 652ndash683 2009

[49] Y Ishimi ldquoADNAhelicase activity is associated with anMCM4-6 and -7 protein complexrdquoThe Journal of Biological Chemistryvol 272 no 39 pp 24508ndash24513 1997

[50] Z Kelman and M F White ldquoArchaeal DNA replication andrepairrdquo Current Opinion in Microbiology vol 8 no 6 pp 669ndash676 2005

[51] J H LeBowitz and R McMacken ldquoThe Escherichia coli dnaBreplication protein is a DNA helicaserdquoThe Journal of BiologicalChemistry vol 261 no 10 pp 4738ndash4748 1986

[52] Z Kelman J-K Lee and J Hurwitz ldquoThe single minichro-mosome maintenance protein ofMethanobacterium thermoau-totrophicum ΔH contains DNA helicase activityrdquo Proceedings ofthe National Academy of Sciences of the United States of Americavol 96 no 26 pp 14783ndash14788 1999

[53] D F Shechter C Y Ying and J Gautier ldquoThe intrinsic DNAhelicase activity of Methanobacterium thermoautotrophicumΔH minichromosome maintenance proteinrdquo The Journal ofBiological Chemistry vol 275 no 20 pp 15049ndash15059 2000

[54] M de Felice L Esposito B Pucci M de Falco M Rossi andF M Pisani ldquoA CDC6-like factor from the archaea Sulfolobussolfataricus promotes binding of the mini-chromosome main-tenance complex to DNArdquoThe Journal of Biological Chemistryvol 279 no 41 pp 43008ndash43012 2004

[55] R Kasiviswanathan J-H Shin and Z Kelman ldquoInteractionsbetween the archaeal Cdc6 and MCM proteins modulate theirbiochemical propertiesrdquo Nucleic Acids Research vol 33 no 15pp 4940ndash4950 2005

[56] J-H Shin B Grabowski R Kasiviswanathan S D Bell andZ Kelman ldquoRegulation of minichromosomemaintenance heli-case activity by Cdc6rdquo The Journal of Biological Chemistry vol278 no 39 pp 38059ndash38067 2003

[57] M Akita A Adachi K Takemura T Yamagami F Matsunagaand Y Ishino ldquoCdc6Orc1 from Pyrococcus furiosus may actas the origin recognition protein and Mcm helicase recruiterrdquoGenes to Cells vol 15 no 5 pp 537ndash552 2010

12 Archaea

[58] M Krupovic S Gribaldo D H Bamford and P Forterre ldquoTheevolutionary history of archaeal MCM helicases a case study ofvertical evolution combined with hitchhiking of mobile geneticelementsrdquo Molecular Biology and Evolution vol 27 no 12 pp2716ndash2732 2010

[59] ADWalters and J P J Chong ldquoAn archaeal orderwithmultipleminichromosome maintenance genesrdquo Microbiology vol 156part 5 pp 1405ndash1414 2010

[60] A DWalters and J P J Chong ldquoMethanococcusmaripaludis anarchaeon with multiple functional MCM proteinsrdquo Biochemi-cal Society Transactions vol 37 no 1 pp 1ndash6 2009

[61] Q Xia E L Hendrickson Y Zhang et al ldquoQuantitative pro-teomics of the archaeon Methanococcus maripaludis validatedbymicroarray analysis and real time PCRrdquoMolecularampCellularProteomics vol 5 no 5 pp 868ndash881 2006

[62] F Sarmiento J Mrazek and W B Whitman ldquoGenome-scaleanalysis of gene function in the hydrogenotrophic methano-genic archaeon Methanococcus maripaludisrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 110 no 12 pp 4726ndash4731 2013

[63] M Pan T J Santangelo Z Li J N Reeve and Z KelmanldquoThermococcus kodakarensis encodes threeMCMhomologs butonly one is essentialrdquo Nucleic Acids Research vol 39 no 22 pp9671ndash9680 2011

[64] S Ishino S Fujino H Tomita et al ldquoBiochemical and geneticalanalyses of the three mcm genes from the hyperthermophilicarchaeon Thermococcus kodakarensisrdquo Genes to Cells vol 16no 12 pp 1176ndash1189 2011

[65] K S Makarova Y I Wolf S L Mekhedov B G Mirkin and EV Koonin ldquoAncestral paralogs and pseudoparalogs and theirrole in the emergence of the eukaryotic cellrdquo Nucleic AcidsResearch vol 33 no 14 pp 4626ndash4638 2005

[66] N Marinsek E R Barry K S Makarova I Dionne E VKoonin and S D Bell ldquoGINS a central nexus in the archaealDNA replication forkrdquo EMBOReports vol 7 no 5 pp 539ndash5452006

[67] T Yoshimochi R Fujikane M Kawanami F Matsunaga and YIshino ldquoTheGINS complex from Pyrococcus furiosus stimulatesthe MCM helicase activityrdquoThe Journal of Biological Chemistryvol 283 no 3 pp 1601ndash1609 2008

[68] T Oyama S Ishino S Fujino et al ldquoArchitectures of archaealGINS complexes essential DNA replication initiation factorsrdquoBMC Biology vol 9 article 28 2011

[69] H Ogino S Ishino K Mayanagi et al ldquoThe GINS com-plex from the thermophilic archaeon Thermoplasma aci-dophilummay function as a homotetramer inDNA replicationrdquoExtremophiles vol 15 no 4 pp 529ndash539 2011

[70] L Sanchez-Pulido and C P Ponting ldquoCdc45 the missing recjortholog in eukaryotesrdquoBioinformatics vol 27 no 14 pp 1885ndash1888 2011

[71] Z Li T J Santangelo L Cubonova J N Reeve and Z KelmanldquoAffinity purification of an archaeal DNA replication proteinnetworkrdquomBio vol 1 no 5 2010

[72] Z Li M Pan T J Santangelo et al ldquoA novel DNA nucleaseis stimulated by association with the GINS complexrdquo NucleicAcids Research vol 39 no 14 pp 6114ndash6123 2011

[73] L A Rajman and S T Lovett ldquoA thermostable single-strandDNase from Methanococcus jannaschii related to the RecJrecombination and repair exonuclease from Escherichia colirdquoJournal of Bacteriology vol 182 no 3 pp 607ndash612 2000

[74] K RWilliams J B Murphy and JW Chase ldquoCharacterizationof the structural and functional defect in the Escherichia colisingle-stranded DNA binding protein encoded by the ssb-1 mutant gene Expression of the ssb-1 gene under 120582p(L)regulationrdquoThe Journal of Biological Chemistry vol 259 no 19pp 11804ndash11811 1984

[75] S Dąbrowski M Olszewski R Pitek and J Kur ldquoNovel ther-mostable ssDNA-binding proteins fromThermus thermophilusand T aquaticus-expression and purificationrdquo Protein Expres-sion and Purification vol 26 no 1 pp 131ndash138 2002

[76] C Iftode Y Daniely and J A Borowiec ldquoReplication proteinA (RPA) the eukaryotic SSBrdquo Critical Reviews in Biochemistryand Molecular Biology vol 34 no 3 pp 141ndash180 1999

[77] A G Murzin ldquoOB(oligonucleotideoligosaccharide binding)-fold common structural and functional solution for non-hom-ologous sequencesrdquo The EMBO Journal vol 12 no 3 pp 861ndash867 1993

[78] C A Haseltine and S C Kowalczykowski ldquoA distinctive single-stranded DNA-binding protein from the Archaeon Sulfolobussolfataricusrdquo Molecular Microbiology vol 43 no 6 pp 1505ndash1515 2002

[79] R I M Wadsworth and M F White ldquoIdentification and pro-perties of the crenarchaeal single-stranded DNA binding pro-tein from Sulfolobus solfataricusrdquoNucleic Acids Research vol 29no 4 pp 914ndash920 2001

[80] I D Kerr R I M Wadsworth L Cubeddu W Blankenfeldt JHNaismith andM FWhite ldquoInsights into ssDNA recognitionby the OB fold from a structural and thermodynamic study ofSulfolobus SSB proteinrdquo The EMBO Journal vol 22 no 11 pp2561ndash2570 2003

[81] X Luo U Schwarz-Linek C H Botting R Hensel B Siebersand M F White ldquoCC1 a novel crenarchaeal DNA binding pro-teinrdquo Journal of Bacteriology vol 189 no 2 pp 403ndash409 2007

[82] T J Kelly P Simancek and G S Brush ldquoIdentification andcharacterization of a single-stranded DNA-binding proteinfrom the archaeonMethanococcus jannaschiirdquoProceedings of theNational Academy of Sciences of theUnited States of America vol95 no 25 pp 14634ndash14639 1998

[83] Z Kelman S Pietrokovski and J Hurwitz ldquoIsolation and cha-racterization of a split B-type DNA polymerase from the arch-aeonMethanobacterium thermoautotrophicumΔHrdquoTheJournalof Biological Chemistry vol 274 no 40 pp 28751ndash28761 1999

[84] K Komori and Y Ishino ldquoReplication protein A in Pyrococcusfuriosus is involved in homologous DNA recombinationrdquo TheJournal of Biological Chemistry vol 276 no 28 pp 25654ndash25660 2001

[85] J B Robbins M C Murphy B A White R I Mackie THa and I K O Cann ldquoFunctional analysis of multiple single-stranded DNA-binding proteins from Methanosarcina acetivo-rans and their effects on DNA synthesis by DNA polymeraseBIrdquoThe Journal of Biological Chemistry vol 279 no 8 pp 6315ndash6326 2004

[86] Y Lin L-J Lin P Sriratana et al ldquoEngineering of functionalreplication protein a homologs based on insights into the evolu-tion of oligonucleotideoligosaccharide-binding foldsrdquo Journalof Bacteriology vol 190 no 17 pp 5766ndash5780 2008

[87] D N Frick and C C Richardson ldquoDNA primasesrdquo AnnualReview of Biochemistry vol 70 pp 39ndash80 2001

[88] G Desogus S Onesti P Brick M Rossi and F M PisanildquoIdentification and characterization of a DNA primase fromthe hyperthermophilic archaeon Methanococcus jannaschiirdquoNucleic Acids Research vol 27 no 22 pp 4444ndash4450 1999

Archaea 13

[89] A A Bocquier L Liu I K O Cann K Komori D Kohda andY Ishino ldquoArchaeal primase bridging the gap between RNAand DNA polymerasesrdquo Current Biology vol 11 no 6 pp 452ndash456 2001

[90] L Liu K Komori S Ishino et al ldquoThe archaeal DNA primasebiochemical characterization of the p41-p46 complex fromPyrococcus furiosusrdquo The Journal of Biological Chemistry vol276 no 48 pp 45484ndash45490 2001

[91] E Matsui M Nishio H Yokoyama K Harata S Darnisand I Matsui ldquoDistinct domain functions regulating de novoDNA synthesis of thermostable DNA primase from hyperther-mophile Pyrococcus horikoshiirdquo Biochemistry vol 42 no 50 pp14968ndash14976 2003

[92] N Ito I Matsui and EMatsui ldquoMolecular basis for the subunitassembly of the primase from an archaeon Pyrococcus hori-koshiirdquoThe FEBS Journal vol 274 no 5 pp 1340ndash1351 2007

[93] M le Breton G Henneke C Norais et al ldquoThe heterodimericprimase from the euryarchaeon Pyrococcus abyssi a multifunc-tional enzyme for initiation and repairrdquo Journal of MolecularBiology vol 374 no 5 pp 1172ndash1185 2007

[94] S-H Lao-Sirieix and S D Bell ldquoThe heterodimeric primaseof the hyperthermophilic archaeon Sulfolobus solfataricus pos-sesses DNA and RNA primase polymerase and 31015840-terminalnucleotidyl transferase activitiesrdquo Journal of Molecular Biologyvol 344 no 5 pp 1251ndash1263 2004

[95] S-H Lao-Sirieix L Pellegrini and S D Bell ldquoThe promiscuousprimaserdquo Trends in Genetics vol 21 no 10 pp 568ndash572 2005

[96] J Hu L Guo K Wu B Liu S Lang and L Huang ldquoTemplate-dependent polymerization across discontinuous templatesby the heterodimeric primase from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquoNucleic Acids Research vol 40no 8 pp 3470ndash3483 2012

[97] E Evguenieva-Hackenberg P Walter E Hochleitner FLottspeich and G Klug ldquoAn exosome-like complex in Sulfolo-bus solfataricusrdquo EMBOReports vol 4 no 9 pp 889ndash893 2003

[98] P Walter F Klein E Lorentzen A Ilchmann G Klug andE Evguenieva-Hackenberg ldquoCharacterization of native andreconstituted exosome complexes from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Microbiology vol62 no 4 pp 1076ndash1089 2006

[99] Z Zuo C J Rodgers A L Mikheikin and M A Trak-selis ldquoCharacterization of a functional DnaG-type primase inarchaea implications for a dual-primase systemrdquo Journal ofMolecular Biology vol 397 no 3 pp 664ndash676 2010

[100] B R Berquist P DasSarma and S DasSarma ldquoEssential andnon-essential DNA replication genes in the model halophilicArchaeon Halobacterium sp NRC-1rdquo BMC Genetics vol 8article 31 2007

[101] D K Braithwaite and J Ito ldquoCompilation alignment andphylogenetic relationships of DNA polymerasesrdquo Nucleic AcidsResearch vol 21 no 4 pp 787ndash802 1993

[102] I K O Cann and Y Ishino ldquoArchaeal DNA replication iden-tifying the pieces to solve a puzzlerdquo Genetics vol 152 no 4 pp1249ndash1267 1999

[103] G Lipps S Rother C Hart and G Krauss ldquoA novel typeof replicative enzyme harbouring ATpase primase and DNApolymerase activityrdquo The EMBO Journal vol 22 no 10 pp2516ndash2525 2003

[104] J Yamtich and J B Sweasy ldquoDNA polymerase family X func-tion structure and cellular rolesrdquoBiochimica et BiophysicaActavol 1804 no 5 pp 1136ndash1150 2010

[105] H Ohmori E C Friedberg R P P Fuchs et al ldquoThe Y-familyof DNA polymerasesrdquoMolecular Cell vol 8 no 1 pp 7ndash8 2001

[106] N Y Yao R E Georgescu J Finkelstein and M E OrsquoDonnellldquoSingle-molecule analysis reveals that the lagging strandincreases replisome processivity but slows replication forkprogressionrdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 106 no 32 pp 13236ndash132412009

[107] U Hubscher G Maga and S Spadari ldquoEukaryotic DNA poly-merasesrdquo Annual Review of Biochemistry vol 71 pp 133ndash1632002

[108] F Boudsocq S Iwai F Hanaoka and R Woodgate ldquoSulfolobussolfataricus P2 DNA polymerase IV (Dp04) an archaeal DinB-like DNA polymerase with lesion-bypass properties akin toeukaryotic pol120578rdquo Nucleic Acids Research vol 29 no 22 pp4607ndash4616 2001

[109] L-J Lin A Yoshinaga Y Lin et al ldquoMolecular analyses ofan unusual translesion DNA polymerase fromMethanosarcinaacetivorans C2Ardquo Journal of Molecular Biology vol 397 no 1pp 13ndash30 2010

[110] I K O Cann S Ishino NNomura Y Sako andY Ishino ldquoTwofamily B DNA polymerases from Aeropyrum pernix an aerobichyperthermophilic crenarchaeoterdquo Journal of Bacteriology vol181 no 19 pp 5984ndash5992 1999

[111] T Uemori Y Ishino H Doi and I Kato ldquoThe hyperther-mophilic archaeon Pyrodictium occultum has two 120572-like DNApolymerasesrdquo Journal of Bacteriology vol 177 no 8 pp 2164ndash2177 1995

[112] T Uemori Y Ishino H Toh K Asada and I Kato ldquoOrgani-zation and nucleotide sequence of the DNA polymerase genefrom the archaeon Pyrococcus furiosusrdquo Nucleic Acids Researchvol 21 no 2 pp 259ndash265 1993

[113] B A Connolly ldquoRecognition of deaminated bases by archaealfamily-B DNA polymerasesrdquo Biochemical Society Transactionsvol 37 no 1 pp 65ndash68 2009

[114] B A Connolly M J Fogg G Shuttleworth and B T WilsonldquoUracil recognition by archaeal family B DNA polymerasesrdquoBiochemical Society Transactions vol 31 no 3 pp 699ndash7022003

[115] T T Richardson X Wu B J Keith P Heslop A C Jones andB A Connolly ldquoUnwinding of primer-templates by archaealfamily-B DNA polymerases in response to template-stranduracilrdquo Nucleic Acids Research vol 41 no 4 pp 2466ndash24782013

[116] T Lindahl ldquoInstability and decay of the primary structure ofDNArdquo Nature vol 362 no 6422 pp 709ndash715 1993

[117] I B Rogozin K S Makarova Y I Pavlov and E V Koonin ldquoAhighly conserved family of inactivated archaeal B family DNApolymerasesrdquo Biology Direct vol 3 article 32 2008

[118] M Imamura T Uemori I Kato and Y Ishino ldquoA non-120572-like DNA polymerase from the hyperthermophilic archaeonPyrococcus furiosusrdquoBiological andPharmaceutical Bulletin vol18 no 12 pp 1647ndash1652 1995

[119] I K O Cann K Komori H Toh S Kanai and Y IshinoldquoA heterodimeric DNA polymerase evidence that members ofEuryarchaeota possess a distinct DNA polymeraserdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 95 no 24 pp 14250ndash14255 1998

[120] L Aravind D D Leipe and E V Koonin ldquoToprimmdasha con-served catalytic domain in type IA and II topoisomerases

14 Archaea

DnaG-type primases OLD family nucleases and RecR pro-teinsrdquo Nucleic Acids Research vol 26 no 18 pp 4205ndash42131998

[121] M Jokela A Eskelinen H Pospiech J Rouvinen and J ESyvaoja ldquoCharacterization of the 31015840 exonuclease subunit DP1of Methanococcus jannaschii replicative DNA polymerase DrdquoNucleic Acids Research vol 32 no 8 pp 2430ndash2440 2004

[122] T Uemori Y Sato I Kato H Doi and Y Ishino ldquoA novel DNApolymerase in the hyperthermophilic archaeon Pyrococcus fur-iosus gene cloning expression and characterizationrdquo Genes toCells vol 2 no 8 pp 499ndash512 1997

[123] Y Shen K Musti M Hiramoto H Kikuchi Y Kawarabayashiand I Matsui ldquoInvariant Asp-1122 and Asp-1124 are essentialresidues for polymerization catalysis of family D DNA poly-merase from Pyrococcus horikoshiirdquo The Journal of BiologicalChemistry vol 276 no 29 pp 27376ndash27383 2001

[124] G Henneke D Flament U Hubscher J Querellou and J-P Raffin ldquoThe hyperthermophilic euryarchaeota Pyrococcusabyssi likely requires the two DNA polymerases D and B forDNA replicationrdquo Journal of Molecular Biology vol 350 no 1pp 53ndash64 2005

[125] L Cubonova T Richardson B W Burkhart et al ldquoArchaealDNA polymerase D but not DNA polymerase B is required forgenome replication in Thermococcus kodakarensisrdquo Journal ofBacteriology vol 195 no 10 pp 2322ndash2328 2013

[126] C Rouillon G Henneke D Flament J Querellou and J-PRaffin ldquoDNA polymerase switching on homotrimeric PCNA atthe replication fork of the euryarchaea Pyrococcus abyssirdquo Jour-nal of Molecular Biology vol 369 no 2 pp 343ndash355 2007

[127] G Henneke ldquoIn vitro reconstitution of RNA primer removal inArchaea reveals the existence of two pathwaysrdquoTheBiochemicalJournal vol 447 no 2 pp 271ndash280 2012

[128] G-LMoldovan B Pfander and S Jentsch ldquoPCNA themaestroof the replication forkrdquo Cell vol 129 no 4 pp 665ndash679 2007

[129] X-P Kong R Onrust M OrsquoDonnell and J Kuriyan ldquoThree-dimensional structure of the 120573 subunit of E coli DNA poly-merase III holoenzyme a sliding DNA clamprdquo Cell vol 69 no3 pp 425ndash437 1992

[130] K Daimon Y Kawarabayasi H Kikuchi Y Sako and Y IshinoldquoThree proliferating cell nuclear antigen-like proteins foundin the hyperthermophilic archaeon Aeropyrum pemix interac-tions with the two DNA polymerasesrdquo Journal of Bacteriologyvol 184 no 3 pp 687ndash694 2002

[131] I Dionne R K Nookala S P Jackson A J Doherty andS D Bell ldquoA heterotrimeric PCNA in the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Cell vol 11 no 1pp 275ndash282 2003

[132] E Warbrick ldquoPCNA binding through a conserved motifrdquoBioEssays vol 20 no 3 pp 195ndash199 1998

[133] H Nishida K Mayanagi S Kiyonari et al ldquoStructural deter-minant for switching between the polymerase and exonucleasemodes in the PCNA-replicative DNA polymerase complexrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 106 no 49 pp 20693ndash20698 2009

[134] K Mayanagi S Kiyonari H Nishida et al ldquoArchitecture of theDNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complexrdquo Proceedings of the National Academy ofSciences of the United States of America vol 108 no 5 pp 1845ndash1849 2011

[135] B Castrec C Rouillon G Henneke D Flament J Querellouand J-P Raffin ldquoBinding to PCNA in Euryarchaeal DNA

replication requires two PIP motifs for DNA polymerase D andone PIP motif for DNA polymerase Brdquo Journal of MolecularBiology vol 394 no 2 pp 209ndash218 2009

[136] P F Pluchon T Fouqueau C Creze et al ldquoAn extendednetworkof genomic maintenance in the archaeon Pyrococcus abyssihighlights unexpected associations between eucaryotic homo-logsrdquo PLoS One vol 8 no 11 Article ID e79707 2013

[137] J E Ladner M Pan J Hurwitz and Z Kelman ldquoCrystalstructures of two active proliferating cell nuclear antigens(PCNAs) encoded byThermococcus kodakaraensisrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2711ndash2716 2011

[138] Y Kuba S Ishino T Yamagami et al ldquoComparative analyses ofthe two proliferating cell nuclear antigens from the hyperther-mophilic archaeonThermococcus kodakarensisrdquo Genes to Cellsvol 17 no 11 pp 923ndash937 2012

[139] T Fukui H Atomi T Kanai R Matsumi S Fujiwara andT Imanaka ldquoComplete genome sequence of the hyperther-mophilic archaeon Thermococcus kodakaraensis KOD1 andcomparison with Pyrococcus genomesrdquo Genome Research vol15 no 3 pp 352ndash363 2005

[140] D Jeruzalmi O Yurieva Y Zhao et al ldquoMechanism of proces-sivity clamp opening by the delta subunit wrench of the clamploader complex of E coliDNApolymerase IIIrdquoCell vol 106 no4 pp 417ndash428 2001

[141] Y Shiomi J Usukura Y Masamura et al ldquoATP-dependentstructural change of the eukaryotic clamp-loader protein repli-cation factor Crdquo Proceedings of the National Academy of Sciencesof the United States of America vol 97 no 26 pp 14127ndash141322000

[142] T Miyata T Oyama K Mayanagi S Ishino Y Ishino and KMorikawa ldquoThe clamp-loading complex for processive DNAreplicationrdquoNature Structural andMolecular Biology vol 11 no7 pp 632ndash636 2004

[143] T Oyama Y Ishino I K O Cann S Ishino and K MorikawaldquoAtomic structure of the clamp loader small subunit fromPyrococcus furiosusrdquo Molecular Cell vol 8 no 2 pp 455ndash4632001

[144] A Seybert D J Scott S Scaife M R Singleton and DB Wigley ldquoBiochemical characterisation of the clampclamploader proteins from the euryarchaeon Archaeoglobus fulgidusrdquoNucleic Acids Research vol 30 no 20 pp 4329ndash4338 2002

[145] Y-H Chen Y Lin A Yoshinaga et al ldquoMolecular analyses of athree-subunit euryarchaeal clamp loader complex from Meth-anosarcina acetivoransrdquo Journal of Bacteriology vol 191 no 21pp 6539ndash6549 2009

[146] Y-H Chen S A Kocherginskaya Y Lin et al ldquoBiochemicaland mutational analyses of a unique clamp loader complex inthe archaeon Methanosarcina acetivoransrdquo The Journal of Bio-logical Chemistry vol 280 no 51 pp 41852ndash41863 2005

[147] F Matsunaga C Norais P Forterre and H Myllykallio ldquoIden-tification of short ldquoeukaryoticrdquo Okazaki fragments synthesizedfrom a prokaryotic replication originrdquo EMBO Reports vol 4no 2 pp 154ndash158 2003

[148] H Kochiwa M Tomita and A Kanai ldquoEvolution of ribonucle-ase H genes in prokaryotes to avoid inheritance of redundantgenesrdquo BMC Evolutionary Biology vol 7 article 128 2007

[149] N OhtaniMHarukiMMorikawa and S Kanaya ldquoMoleculardiversities of RNases Hrdquo Journal of Bioscience and Bioengineer-ing vol 88 no 1 pp 12ndash19 1999

Archaea 15

[150] N Ohtani M Haruki M Morikawa R J Crouch M Itayaand S Kanaya ldquoIdentification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII fromBacillus subtilis classification of RNases H into three familiesrdquoBiochemistry vol 38 no 2 pp 605ndash618 1999

[151] N Ohtani H Yanagawa M Tomita and M Itaya ldquoIdentifi-cation of the first archaeal type 1 RNase H gene from Halobac-terium sp NRC-1 archaeal RNase HI can cleave an RNA-DNAjunctionrdquoThe Biochemical Journal vol 381 no 3 pp 795ndash8022004

[152] N Ohtani H Yanagawa M Tomita and M Itaya ldquoCleavage ofdouble-stranded RNA by RNase HI from a thermoacidophilicarchaeon Sulfolobus tokodaii 7rdquo Nucleic Acids Research vol 32no 19 pp 5809ndash5819 2004

[153] M A Nowak M C Boerlijst J Cooke and J M SmithldquoEvolution of genetic redundancyrdquo Nature vol 388 no 6638pp 167ndash170 1997

[154] A E Tomkinson S Vijayakumar J M Pascal and T Ellen-berger ldquoDNA ligases structure reactionmechanism and func-tionrdquo Chemical Reviews vol 106 no 2 pp 687ndash699 2006

[155] M Nakatani S Ezaki H Atomi and T Imanaka ldquoA DNAligase from a hyperthermophilic archaeon with unique cofactorspecificityrdquo Journal of Bacteriology vol 182 no 22 pp 6424ndash6433 2000

[156] Y Sun M S Seo J H Kim et al ldquoNovel DNA ligase with broadnucleotide cofactor specificity from the hyperthermophilic cre-narchaeon Sulfophobococcus zilligii influence of ancestral DNAligase on cofactor utilizationrdquo Environmental Microbiology vol10 no 12 pp 3212ndash3224 2008

[157] T R Beattie and S D Bell ldquoCoordination of multiple enzymeactivities by a single PCNA in archaeal Okazaki fragmentmaturationrdquo The EMBO Journal vol 31 no 6 pp 1556ndash15672012

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

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Molecular Biology International

GenomicsInternational Journal of

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The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

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BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

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Nucleic AcidsJournal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Archaea 5

a homotetrameric complex [68 69] Moreover in vitro the Tacidophilum MCM helicase activity was not affected by theGINS complex [69] These results suggest that other proteinsmay be involved in the formation of a stable helicase in manyArchaea M maripaludis S2 possesses a hypothetical proteinwhich may correspond to the gene encoding for GINS15which is probably essential for growth [60 62] No homologsof GINS23 are present in the genome ofM maripaludis

The replication related Cdc45 protein is ubiquitous ineukaryotes but its exact role has not yet been elucidatedInterestingly homologs of the Cdc45 protein are not presentin Archaea However a bioinformatics analysis revealed thatthe eukaryotic Cdc45 and the prokaryotic RecJ which is aconserved 51015840-31015840exonuclease in most bacteria and archaeapossess a common ancestry and share a homologous DHHdomain [70] These results suggest that the archaeal RecJmay substitute for the eukaryotic Cdc45 during replicationCircumstantial evidence supports this conclusion In S solfa-taricus a homolog of the DNA binding domain of RecJ waspurified together with a GINS protein [66] Similarly in Tkodakaraensis the RecJ homolog (TK1252p) copurified withproteins of theGINS complex [71] and formed a stable in vitroassociation with the GINS complex [72] Two RecJ homologsare found inM jannaschii (MJ0977 and 0831) and they par-tially complement a recJ mutation in E coliThe recombinantMJ0977 also possesses high levels of thermostable single-stranded DNA degrading activity similar to RecJ [73] In Mmaripaludis S2 four proteins possess the DHH domain withsimilarity to the M jannaschii RecJ homologs (MMP16820547 1078 and 1314) However none of them was essentialfor growth suggesting that the activities were redundant [62]Alternatively another protein which has a low similaritywith M jannaschii RecJ homolog (MMP0285) but possessesthe DHH domain was possibly essential for growth [62]However this protein possesses other domains related totransport which make it an unlikely candidate for RecJThese results are not definitive and more experimental datais needed to assign a function to this protein

As soon as the DNA is unwound ssDNA is protectedfromnucleases chemicalmodification and other disruptionsby ssDNA binding proteins These proteins are present in allthree domains of life and are called SSB in Bacteria wherethey form homotetramers or homodimers [74 75] and RPA(replication protein A) in eukaryotes where they form astable heterotrimer composed of 70 32 and 14 kDa proteins[76] Although all ssDNA binding proteins contain dif-ferent combinations of the oligonucleotideoligosaccharide-binding fold or OB-fold [77] the sequence similarity is lowamong RPA and the bacterial SSBs [43] In Archaea differ-ent types of ssDNA binding proteins have been reportedIn crenarchaeotes an ssDNA binding protein is only wellcharacterized in S solfataricus The S solfataricus ssDNAbinding protein contains only one OB-fold and can adopt aheterotetramer conformation [78] However the protein alsoappears to exist as a monomer [79] This protein appears tobe more similar to the bacterial proteins in sequence but itsstructure is more similar to that of the eukaryotic RPAs [4380] While homologs are recognizable in other members ofthe Sulfolobales andmost otherArchaea they are absent from

the genomes of many members of the closely related orderThermoproteales with some few exceptions (Figure 1) [81]

RPAs have been studied from different representativesof the euryarchaeotes revealing additional diversity M jan-naschii andM thermautotrophicus possess a single RPA sub-unit which shares amino acid similarity with the eukaryoticRPA70 and possesses four and five OB-folds respectively [8283] P furiosus possesses three different RPA subunits whichform a stable heterotrimer that is involved in homologousrecombination in vitro [84] The P furiosus RPA thereforeis similar in subunit organization to the eukaryotic RPATheother members of the Thermococcales genera also possessthree RPA homologs which likely form the homotrimericcomplex described for P furiosus (Figure 1) Methanosarcinaacetivorans also possesses three different RPAproteins (RPA1-3) with four two and two OB-folds respectively Howeverthey do not interact with each other and appear to functionas homodimers [85] This arrangement is common amongthe Methanosarcinales but is not found in the closely relatedmethanogen orders such as the Methanocellales (Figure 1)Members of the order Methanococcales possess two to fourRPA homologs The genome of M maripaludis S2 containsthree possible RPA homologs (MMP0122 0616 and 1032)[60] Only MMP0616 and 1032 were likely to be essential forgrowth [62] suggesting a possible different complex configu-ration for RPA proteins in this archaeon It has been hypoth-esized that the diversity in OB-folds in the archaeal RPAs is adirect consequence of homologous recombination [86]

DNA synthesis starts with the production of a RNAprimer since the DNA polymerases that replicate genomesare incapable of de novo DNA synthesis The RNA primeris synthesized by a DNA-dependent RNA polymerase orprimase DnaG a single subunit protein is the primase inBacteria In eukaryotes a two-subunit primase consisting ofa small catalytic subunit (PriS) and a large subunit (PriL)is found in a complex with DNA polymerase 120572 and itsaccessory B subunit [87] In Archaea the first biochemicallycharacterized primase was the eukaryotic primase-like smallsubunit PriS in M jannaschii [88] Later homologs of thePriS and PriL subunits were described in several Pyrococ-cus species [89ndash93] The eukaryotic-like DNA primase hasalso been characterized in the crenarchaeote S solfataricus[94 95] where it has been shown to interact with MCMthrough GINS23 [66] A unique polymerization activityacross discontinuous DNA templates has been characterizedin the PriSL of S solfataricus suggesting that this primasemay be involved in double-stranded break repair in Archaea[96] So far the eukaryotic-like primases found in archaeaexhibit similar properties PriS functions as the catalyticsubunit and PriL modulate its activity [87] In additionthe archaeal eukaryotic-like primase has the unique abilityto synthesize both DNA and RNA in vitro Indeed theP furiosus PriS synthesizes long DNA fragments but theaddition of PriL regulates the process by decreasing theDNA polymerase activity increasing the RNA polymeraseactivity and decreasing the product length [90] Additionallystudies of the P abyssi enzyme suggest that DNA primasemay also be involved in DNA repair because of the DNApolymerase gap filling and strand displacement activities

6 Archaea

also present in vitro [93] Interestingly the archaeal primasesmall subunit resembles DNA polymerases from the Pol Xfamily in sequence and structure suggesting a similarity intheir catalytic mechanism [96]

Homologs of the bacterial DnaG primase are also foundin archaea However in vitro studies of the P furiosusenzyme failed to detect primer synthesis activity and the TkodakaraensisDnaG was copurified with proteins of the exo-some [71] Also in S solfataricus DnaG primase was found tobe a core exosome subunit involved in RNA degradation [9798] However recent studies demonstrated that the S solfa-taricus DnaG homolog has limited primer synthesis activityand a dual primase system with PriSL has been proposed tofunction during DNA replication [99] Hu et al hypothesizedan interesting theory which suggests that LUCA employed adual-primase system comprisingDnaG and PriSL which alsoserved roles in RNA degradation and the nonhomologousend joining (NHEJ) pathwayThe system was inherited by allthree domains In theArchaea domain it retained its originalfunctions However in the Bacteria domain DnaG becamethe major replicative primase and PriSL evolved into the Poldomain of LigD involved in the NHEJ pathway In contrastDnaG was lost in the Eukaryota domain and PriSL becamethe only replicative primase In addition it also evolved intothe DNA Pol X family involved in NHEJ [96]

Like other ArchaeaM maripaludis S2 possesses both theeukaryotic- and bacterial-like primases A new genome-widesurvey of this methanoarchaea revealed that genes encodingboth subunits of the eukaryotic like primase PriS and PriL(MMP0009 and MMP0071) were likely to be essential forgrowth which is consistent with a role in replication Similarobservations have been demonstrated in other Archaea suchas Halobacterium sp NRC-1and Haloferax volcanii [93 100]In contrast the DnaG primase (MMP1286) was nonessentialwhich would be consistent with a role in the exosome [62]These results suggest that in M maripaludis and probablyother euryarchaeotes a dual primase system is not pre-sent

33 Elongation (Replicative DNA Polymerase) The primersynthesized by the primase is further extended by a replicativeDNA polymerase DNA polymerases have been classifiedinto seven families based on their amino acid sequencesimilarity (A B C D E X and Y) [101ndash105] In Bacteria Ecoli possesses five DNA polymerases Pol IndashV where the firstthree belong to families A B and C respectively and the lasttwo belong to the Y family The major replicative DNA poly-merase in E coli is Pol III a member of the C family whichsynthesizes DNA with high processivity when functioningwithin the holoenzyme [106] In eukaryotes a great diversityof DNA polymerases is also found but DNA replicationrequires three replicative DNA polymerases which belongto family B (Pol120572 Pol120575 and Pol120576) [107] In Archaea fewertypes of DNA polymerases are present but they have aninteresting evolutionary division Representatives of theDNApolymerase B family are found in all Archaea The D familyDNA polymerase is present in every phyla studied so farwith the exception of the Crenarchaeota (Figure 1) Lastly amember of theY family has been identified andbiochemically

characterized in S solfataricus [108] and the Methanosarci-nales in which several species harbor two homologs [109]Even though the activity of DNA polymerases belongingto the Y family in archaea is not fully understood they aresuggested to play an important role in DNA repair [109]

Representatives of the DNA polymerase family B havebeen identified in all Archaea The crenarchaeotes possess atleast two family B DNA polymerases (PolB I and PolB IIand in some cases PolB III) [102 110 111] The recombinantS solfataricus Pyrodictium occultum and A pernix enzymeshave been characterized [102] In contrast euryarchaeotesonly contain PolB I The recombinant P furiosus enzymehas been characterized [112] The PolB I enzymes havesimilar amino acid sequence and overall structure and theypossess a potent 31015840-51015840exonuclease proofreading activity [102]A unique property of the archaeal family B DNA polymeraseis the ability to stall DNA polymerization in the presenceof uracil or hypoxanthine deaminated bases [113 114] thisproperty helps to prevent the copy of template-strand uraciland the transmission of fixed mutations to progeny [115]Commonly cytosine deamination converts GC base pairsinto the promutagenic GU mismatches which result in50 of the offspring containing an AT transition mutationafter replication [116] In addition when A-U base pairs areformed the loss of the 5-methyl moiety upon replacementof thymine can exert a detrimental effect on protein DNAinteractions Interestingly in some crenarchaeotes and eur-yarchaeotes one of the B family DNA polymerase paralogspossesses disrupted versions of the sequence motifs thatare essential for catalysis Possibly these enzymes possess astructural role [117]

DNA polymerase family D (PolD) is a novel enzyme thatwas originally discovered in P furiosus [118] It has sincethen been identified in all euryarchaeotes [119] For a longtime this enzyme was considered a euryarchaeote-specificpolymerase but the three newly discovered archaeal phylawere also found to possess genes for PolD [14ndash16] PolD isa heterodimer with a small subunit (DP1) and a large subunit(DP2) It has been proposed that the large subunit harborsthe polymerase activity although its sequence is very differentfrom other hitherto described DNA polymerases The smallsubunit possesses high similarity with the noncatalytic B-subunits of the eukaryoticDNApolymerases120572 120575 and 120576 [120]Studies of the M jannaschii enzyme demonstrated that thesmall subunit possesses a strong 31015840-51015840exonuclease activitysuggesting that it may be involved in proofreading activity[7 121] Efficient polymerase and proofreading activity havealso been detected from a purified PolD of P furiosus andthe residues Asp-1122 and Asp-1124 are essential for thepolymerization reaction in P horikoshii [122 123] Everyeuryarchaeote examined possessed one homolog for DP1 andDP2 except forMethanococcoides burtoniiDSM 6242 whichpossesses two homologs for DP1 (Figure 1)

Because the crenarchaeotes only possess family B DNApolymerases one of themmust be the replicative polymeraseHowever in euryarchaeotes it was not clear which enzymewas involved in replication Studies in Halobacterium spNRC-1 showed that both PolB and PolD were essential forviability and it was proposed that they could be working

Archaea 7

together at the replication fork synthesizing the leading andlagging strand respectively [100 124] However in otherEuryarchaeota PolB does not appear to be essential Forinstance a recent report demonstrated that both subunits ofPolDwere essential but PolB was nonessential for the growthof M maripaludis S2 [62] Likewise in T kodakaraensisPolD can be coisolated with different proteins of the archaealreplication fork but PolB wasmainly coisolated with proteinsof unknown function [71] A deletion of the PolB in Tkodakaraensis also had no detectable effect on cell viability[125] Interestingly T kodakaraensis PolB mutants haveincreased sensitivity to UV radiation These results togethersuggest that PolD is the essential replicative DNA polymerasein these euryarchaeotes and not a PolB family polymeraseIn this scenario PolB may have some other crucial functionin Halobacterium and possibly other closely related specieswhich it is not conserved throughout the phylum Finallyit has been demonstrated that purified PolD from P abyssiis able to perform strand displacement and RNA primerextension in vitro Purified PolB on its own cannot performthese activities in vitro but in the presence of PCNA stranddisplacement activity is stimulated [124 126] A recent in vitrostudy in P abyssi demonstrated that RNase HII is required toinitiate strand displacement DNA synthesis by PolB [127]

34 Elongation (Other Accessory Proteins) Purified DNApolymerases possess low processivity however the addi-tion of an accessory factor the sliding clamp gives DNApolymerases the required processivity to replicate genomesThis factor whose structure resembles a doughnut functionsas a molecular platform which recruits several replication-associated enzymes and act together with DNA and thepolymerase to stabilize their interactions during replication[128] The structure of sliding clamps is conserved in thethree domains of life In Bacteria the sliding clamp or 120573-subunit is a homodimeric ring [129] In eukaryotes thesliding clamp or proliferating cell nuclear antigen (PCNA)is a homotrimeric ring [128] In Archaea the majority ofcrenarchaeotes have multiple PCNA homologs which formheterotrimeric rings [130 131] (Figure 1) In contrast mosteuryarchaeotes possess a single PCNA homolog (Figure 1)Interactions of DNA polymerase with the sliding clampare mediated through a common motif called the PCNAInteracting Protein (PIP) box [132] The three dimensionalstructures of PCNA-PolB and the PolB-PCNA-DNA complexfrom P furiosus have been solved shedding light on theinteractions between these molecules [133 134] In additiona study demonstrated that the PolDPCNA and PolBPCNAinteractions require two and one PIP boxes respectively[135] Recently through a protein-interaction network of Pabyssi a previously unknown protein with nuclease activity(Pab0431) and a PIP canonical motif was discovered tointeract with PCNA suggesting a possible involvement inDNA replication [136] T kodakaraensis is the only well-documented example of an euryarchaeotewith twohomologsfor PCNA TK0535 (PCNA1) and TK0582 (PCNA2) Recentwork demonstrated both proteins form stable homotrimericrings that interact with T kodakaraensis PolB in vitro [137]A more detailed study of the two homologs of PCNA in T

kodakaraensis demonstrated that both homologs stimulate invitro the primer extension activity of PolB but only PCNA1and not PCNA2 stimulates the same activity of PolD [138]Also the same report showed that the pcna2 gene can bedisrupted without causing growth deficiencies but it was notpossible to isolate mutants of pcna1 These results suggestthat PCNA1 but not PCNA2 is essential for DNA replication[138] It has been proposed that one of the PCNA geneswas acquired by lateral gene transfer [139] Members of theorderMethanococcales possess one PCNA homolog with twoexceptionsMmaripaludis S2 possesses twoPCNAhomologs(MMP1126 and 1711) [60] Both genes appeared to be essentialfor growth suggesting that they both play an importantrole in replication [62] The gene MMP1711 possesses highsimilarity to both T kodakaraensis genes and is likely thetrue methanococcal PCNA In contrast MMP1126 possessesonly low similarity to the T kodakaraensis genes and alsocontains an S-adenosylmethionine-dependent methyltrans-ferases domain Thus it is likely to possess some alternativefunction Methanotorris igneus Kol 5 also possesses twoPCNA homologs

For PCNA to assemble around DNA a specific loadingfactor is required In Bacteria the loading factor is knownas 120574-complex and comprises three different subunits ina 1205743-120575-1205751015840 stoichiometry [140] In eukaryotes the loading

factor is known as Replication Factor C (RFC) and is aheteropentameric complex comprising one large subunit andfour different small subunits [141] In contrast inArchaea theRFC consists of two different proteins a small subunit RFCSand a large subunit RFCLThey also form a heteropentamericcomplex in a 4 1 ratio (RFCS RFCL) Interestingly manycrenarchaeotes possess one homolog of RFCL and two orthree homologs of RFCS Alternatively most euryarchaeotespossess only one RFCL and RFCS homolog The exceptionsare somemembers of the ordersHalobacteriales Methanomi-crobiales and Methanosarcinales which possess two RFCShomologs (Figure 1) Structural and biochemical studies ofRFC have been conducted in several euryarchaeotes such asArchaeoglobus fulgidus and Pyrococcus species [142ndash144] Aninteresting case is observed in Methanosarcina acetivoransThis RFC possesses three subunits (RFC1 2 L) found ina ratio 3 1 1 [145] Homologs for these three subunits arealso present in most of the genomes of the haloarchaea[145] It is inferred that this type of RFC complex representsan intermediary form transitional between the canonicalarchaeal RFC complex of one small and one large subunit andthe eukaryotic RFC complex of four different small and onelarge subunit [146] The organization and spatial distributionexhibit a similarity to the E coliminimal 120574-complex but thefunction of the subunits is probably not conserved [145]

35 Maturation During DNA replication the lagging strandis discontinuously synthesized by extending the RNAprimersor Okazaki fragments This discontinuously synthesizedDNA strand requires maturation to form a single covalentlyclosed strand to end the replication process In ArchaeaOkazaki fragments were first demonstrated during replica-tion in P abyssi and Sulfolobus acidocaldarius [147] Duringreplication these RNA primers are replaced with DNA The

8 Archaea

removal of the primers is performed by the enzyme RNase Hwhich is ubiquitous in the three domains of life Accordingto their sequence similarity in prokaryotes the RNase Hproteins are classified into three groups RNase HI HII andHIII In eukaryotes they are classified as RNase H1 and H2[148] However phylogenetic analyses suggest that the RNaseH proteins can also be classified into two different groupsType 1 (prokaryotic RNaseHI eukaryotic RNaseH1 and viralRNase H) and Type 2 (prokaryotic RNase HII and HIII andeukaryotic RNase H2) [149] These two types of RNase Hpossess different specific activities metal ion preferences andcleavage sites [150] Originally it was thought that Archaeaonly possess type 2 RNase H [149] but several type 1 archaealRNase H enzymes have since then been discovered [151 152]Interestingly in eukaryotes RNaseH1 andH2 tend to coexistand different combinations of the three prokaryotic RNasesH(I II and III) are found except for the combination of RNasesHI and HIII This mutually exclusive evolution of some ofthe prokaryotic RNases seems to be related to functionalredundancy [148]

Another enzyme involved in primer replacement inDNA replication is the Flap endonuclease I (FEN-1) whichrecognizes double-strandedDNAwith an unannealed 51015840-flapand cleaves it A eukaryotic homolog of FEN-1 is found inevery archaeal member analyzed and one member of theThermoproteales Thermofilum pendens Hrk5 possesses twohomologs

M maripaludis S2 possesses genes for the prokaryoticRNase HI and HII and for FEN-1 but none are essentialsuggesting that they may be redundant in their functions[44 62] Possibly both RNase H proteins persist and areevolutionary stable in the genome The gene products mayperform the same function but one is less efficient than theother [153]

After the Okazaki fragments are replaced by DNA inthe lagging strand the nick between the newly synthesizedand the elongated DNA is repaired by a DNA ligase Thisenzyme uses a nucleotide cofactor to catalyze the formationof the phosphodiester bond in three well-characterized steps[154]The enzyme is common to all three domains but can begrouped into two families based on cofactor specificity (ATPor NAD+) The DNA ligases from several crenarchaeotes andeuryarchaeotes have been further characterized (reviewedin [43]) Many archaeal DNA ligases possess dual cofactorspecificity (ATPNAD+ or ATPADP) but every archaealDNA ligase characterized so far uses ATP A thermophilicDNA ligase from M thermautotrophicus which uses ATP assole cofactor was characterized in vitro [155] A characterizedDNA ligase from the crenarchaeote Sulfophobococcus zilligiidisplayed specificity for three cofactors (ATPNAD+GTP)[156]Major structuralwork in this enzymehas been achievedin P furiosus and S solfataricus and the findings have beenreviewed in detail [43] InM maripaludis S2 the DNA ligaseis likely to be essential for growth [44 62]

Understanding the maturation process in archaea hasbecome a focus of increasing research in recent years An invitro study reconstituted the Okazaki fragment maturationusing proteins derived from the crenarchaeote S solfataricusThey demonstrated that only six proteins are necessary for

coupled DNA synthesis RNA primer removal and DNAligation In this model a single PCNA (heterotrimeric ring)coordinates the activities of PolBI FEN-1 and DNA ligaseinto an efficient maturation complex [157] A different invitro study in P abyssi has demonstrated two different modelsfor Okazaki fragments maturation which differ in the RNAprimer removal process In the first model RNA primerelimination is executed by continuous PolD strand displace-ment DNA synthesis and 51015840RNA flap cleavage by FEN-1The resulting nicks are closed by DNA ligase Alternativelythe second model proposes that RNase HII cleaves theRNA primer followed by the action of FEN-1 and stranddisplacement DNA synthesis by polB or polD The nick isthen sealed by DNA ligase [127] Testing these models invivo is of great interest to complete the picture of how theseprocesses behave in the cell In addition other factors that canmodulate these processesmay be required for coordination ofthe in vivomaturation process

4 Conclusions

DNA replication in archaea possesses a dual nature wherethe machinery is structurally and functionally similar to theeukaryotic replication system but it is executed within abacterial context [11 25] Additionally unique archaeal fea-tures demonstrate the complexity of this process and it doesnot appear to be just a simplified version of the eukary-otic system For example the archaeal specific DNA poly-merase D is conserved across the Archaea domain with theexception of the Crenarchaeota phylumThe recent discoverythat it is the essential replicative polymerase in two differenteuryarchaeotic species demonstrates an unanticipated vari-ability in archaeal DNA replication and a fundamental differ-ence in the replication mechanism between crenarchaeotesand euryarchaeotes Interestingly the absence of PolD increnarchaeotes is not the only difference in DNA repli-cation These differences include the absence of histonesin crenarchaeotes [4] the presence of multiple origins ofreplication in crenarchaeotes and a single origin of repli-cation in most euryarchaeotes the absence of GINS23 inmost euryarchaeotes the absence of RPA protein in manycrenarchaeotes the presence of multiple MCM homologs inMethanococcales and the presence of one homolog of PCNAin euryarchaeotes compared to the multiple homologs increnarchaeotes These distinctive characteristics between thephyla highlight the complexity of archaeal DNA replicationand suggest a complex evolutionary history (Table 1)

Among the Euryarchaeota the ordersHalobacteriales andMethanococcales possess differences in the DNA replicationsystem that make them unique For instance Halobac-teriales possess many more origin recognition proteins(Orc1Cdc6) compared to the rest of the archaea On theother hand Methanococcales and Methanopyrales lack rec-ognizable homologs for the Orc1Cdc6 proteins suggestingthe presence of a very different mechanism for initiation ofreplication In addition the Methanococcales possess a largenumber of MCM protein homologs It has been proposedthat these distinctive features are connected and because ofthe absence of the Orc1Cdc6 proteins MCM proteins may

Archaea 9

Table1DNAreplicationproteins

andfeatures

inthed

omains

BacteriaEukaryotaand

thetwomajor

phylao

fthe

Archaeado

main

Mod

ified

from

[43]

DNAreplicationstage

Process

Bacteria

Eukaryota

Archaea

Crenarchaeota

Euryarchaeota

Preinitia

tion

Orig

inof

replication

Sing

leMultip

leMultip

leSing

lea

Orig

inrecogn

ition

DnaA

ORC

complex

(ORC

1-6)

Orc1C

dc6

Orc1C

dc6b

Initiation

DNAun

winding

(Helicase)

DnaB

MCM

complex

(MCM

2-7)

MCM

complex

MCM

complex

DNAun

winding

(Accessory

proteins)

DnaC

Cdc6

GIN

S23GIN

S15

GIN

S15c

Cdt1

GIN

Scomplex

(Sld5Psf1-3)

RecJho

molog

RecJho

molog

Cdc45

Prim

ersynthesis

DnaG

Pol120572

prim

asec

omplex

DNAprim

ase

(PriS

L)D

naG

dDNAprim

ase(PriSL)

Elon

gatio

n

DNAsynthesis

(polym

erase)

PolIII(Fam

ilyCDNApo

lymerase)

Pol120575and

Pol120576(Fam

ilyBDNA

polymerase)

Family

BDNApo

lymerase

Family

DDNA

polymerasee

DNAsynthesis

(Processivity

factors)

120574-com

plex

(clamploader)

RFC(clamploader)

RFC(clamploader)

RFC(clamploader)

120573-clamp(clamp)

PCNA(clamp)

PCNA(clamp)

PCNA(clamp)

Maturation

Maturation(O

kazaki

fragmentp

rocessing)

PolI

(family

ADNApo

lymerase)

Fen1D

na2

Fen1

Fen1

RNaseH

RNaseH

RNaseH

RNaseH

DNAligase

DNAligase

DNAligase

DNAligase

a Exceptio

ntheo

rder

Halobacteria

les

b Not

know

nform

embersof

theE

uryarchaeota

ordersMethanococcalesandMethanopyrales

c GIN

S23hasb

eenfoun

dedon

lyin

theo

rder

Thermococcales

oftheE

uryarchaeota

d Sulfolobu

ssolfataric

usdidshow

prim

asea

ctivity

invitro

e Fam

ilyBDNApo

lymeraseisa

lsoessentialinHalobacteriu

mB

ecause

itsfunctio

nhasn

otbeen

clearlyelu

cidateditmight

also

play

aroleinreplicationin

thisandclo

selyrelated

organism

s

10 Archaea

interact with other unknown initiation enzymes resultingin a complex phylogeny of the MCM homologs [49] Pre-sumably these differences also account for the inability torecognize the origin of replication in these microorganismsThis unique scenario for initiation of DNA replicationmay bea direct consequence of various processes such as duplicationmobile genetic elements and interactions with viruses [58]

The differences in DNA replication among archaealhigher taxa demonstrate an unexpected variability and sug-gest two alternative evolutionary models In the first modelDNA replication evolved late after the diversification ofthe archaeal lineages Because the replicative system wasnot fully formed it was possible to develop differentlybetween the lineages Once formed replication would thenbe highly conserved However this model is not consistentwith differences observed between lineages that must haveformed relatively late such as those between the orders oreven in some cases within certain orders The alternativemodel is that DNA replication has changed throughout theevolution of the archaea Thus differences in the replicativesystems may represent ancient as well as modern adaptationsto changing environments In this case differences in thereplicative systems may provide important insights into theevolutionary pressures in play during different episodes ofarchaeal evolution From this perspective the differencesbetween the eukaryotic and archaeal replicative systems maynot be evidence for an ancient origin of the eukaryotesInstead it is entirely plausible that the replicative system ineukaryotes could have evolved relatively late from a well-developed archaeal system

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] E F DeLong and N R Pace ldquoEnvironmental diversity ofbacteria and archaeardquo Systematic Biology vol 50 no 4 pp 470ndash478 2001

[2] B Chaban S Y M Ng and K F Jarrell ldquoArchaeal habitatsmdashfrom the extreme to the ordinaryrdquo Canadian Journal of Micro-biology vol 52 no 2 pp 73ndash116 2006

[3] M J Hanford and T L Peeples ldquoArchaeal tetraether lipidsunique structures and applicationsrdquo Applied Biochemistry andBiotechnology A vol 97 no 1 pp 45ndash62 2002

[4] K Sandman and J N Reeve ldquoArchaeal histones and the originof the histone foldrdquo Current Opinion in Microbiology vol 9 no5 pp 520ndash525 2006

[5] O Lecompte R Ripp J-C Thierry D Moras and O PochldquoComparative analysis of ribosomal proteins in complete gen-omes an example of reductive evolution at the domain scalerdquoNucleic Acids Research vol 30 no 24 pp 5382ndash5390 2002

[6] D R Edgell and W F Doolittle ldquoArchaea and the origin(s) ofDNA rplication poteinsrdquo Cell vol 89 no 7 pp 995ndash998 1997

[7] E R Barry and S D Bell ldquoDNA replication in the archaeardquoMicrobiology and Molecular Biology Reviews vol 70 no 4 pp876ndash887 2006

[8] S Gribaldo and C Brochier-Armanet ldquoThe origin and evolu-tion of archaea a state of the artrdquo Philosophical Transactions ofthe Royal Society B vol 361 no 1470 pp 1007ndash1022 2006

[9] P Londei ldquoEvolution of translational initiation new insightsfrom the archaeardquo FEMS Microbiology Reviews vol 29 no 2pp 185ndash200 2005

[10] B Grabowski and Z Kelman ldquoArchaeal DNA replicationeukaryal proteins in a bacterial contextrdquo Annual Review ofMicrobiology vol 57 pp 487ndash516 2003

[11] P Forterre J Filee and H Myllykallio ldquoOrigin and evolutionof DNA and DNA replication machineriesrdquo in The GeneticCode and the Origin of Life L Ribas Ed Landes BioscienceGeorgetown Tex USA 2007

[12] E V Koonin ldquoThe origin and early evolution of eukaryotesin the light of phylogenomicsrdquo Genome Biology vol 11 no 5article 209 2010

[13] M Konneke A E Bernhard J R de la Torre C B WalkerJ B Waterbury and D A Stahl ldquoIsolation of an autotrophicammonia-oxidizing marine archaeonrdquo Nature vol 437 no7058 pp 543ndash546 2005

[14] C Brochier-Armanet B Boussau S Gribaldo and P ForterreldquoMesophilic crenarchaeota proposal for a third archaeal phy-lum theThaumarchaeotardquoNature Reviews Microbiology vol 6no 3 pp 245ndash252 2008

[15] J G Elkins M Podar D E Graham et al ldquoA korarchaealgenome reveals insights into the evolution of the ArchaeardquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 105 no 23 pp 8102ndash8107 2008

[16] T Nunoura Y Takaki J Kakuta et al ldquoInsights into theevolution of Archaea and eukaryotic protein modifier systemsrevealed by the genome of a novel archaeal grouprdquoNucleic AcidsResearch vol 39 no 8 pp 3204ndash3223 2011

[17] HHuberM J Hohn R Rachel T Fuchs V CWimmer andKO Stetter ldquoAnewphylumofArchaea represented by a nanosizedhyperthermophilic symbiontrdquoNature vol 417 no 6884 pp 63ndash67 2002

[18] C Brochier S Gribaldo Y Zivanovic F Confalonieri and PForterre ldquoNanoarchaea representatives of a novel archaeal phy-lum or a fast-evolving euryarchaeal lineage related to Therm-ococcalesrdquo Genome Biology vol 6 no 5 article R42 2005

[19] S J Aves ldquoDNA replication initiationrdquo Methods in MolecularBiology vol 521 pp 3ndash17 2009

[20] N P Robinson I Dionne M Lundgren V L Marsh RBernander and S D Bell ldquoIdentification of two origins ofreplication in the single chromosome of the archaeon Sulfolobussolfataricusrdquo Cell vol 116 no 1 pp 25ndash38 2004

[21] M Lundgren A Andersson L Chen P Nilsson and RBernander ldquoThree replication origins in Sulfolobus speciessynchronous initiation of chromosome replication and asyn-chronous terminationrdquo Proceedings of the National Academy ofSciences of theUnited States of America vol 101 no 18 pp 7046ndash7051 2004

[22] N P Robinson and S D Bell ldquoExtrachromosomal element cap-ture and the evolution ofmultiple replication origins in archaealchromosomesrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 104 no 14 pp 5806ndash58112007

[23] E A Pelve A C Lindas A Knoppel A Mira and R Bernan-der ldquoFour chromosome replication origins in the archaeonPyrobaculum calidifontisrdquo Molecular Microbiology vol 85 no5 pp 986ndash995 2012

Archaea 11

[24] A F Andersson E A Pelve S LindebergM Lundgren P Nils-son and R Bernander ldquoReplication-biased genome organisa-tion in the crenarchaeon Sulfolobusrdquo BMCGenomics vol 11 no1 article 454 2010

[25] H Myllykallio P Lopez P Lopez-Garcıa et al ldquoBacterial modeof replication with eukaryotic-like machinery in a hyperther-mophilic archaeonrdquo Science vol 288 no 5474 pp 2212ndash22152000

[26] F Matsunaga P Forterre Y Ishino and H Myllykallio ldquoInvivo interactions of archaeal Cdc6Orc1 and minichromosomemaintenance proteins with the replication originrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 98 no 20 pp 11152ndash11157 2001

[27] S Maisnier-Patin L Malandrin N K Birkeland and RBernander ldquoChromosome replication patterns in the hyper-thermophilic euryarchaeaArchaeoglobus fulgidus andMethano-caldococcus (Methanococcus) jannaschiirdquo Molecular Microbiol-ogy vol 45 no 5 pp 1443ndash1450 2002

[28] R Zhang and C-T Zhang ldquoMultiple replication origins ofthe archaeon Halobacterium species NRC-1rdquo Biochemical andBiophysical Research Communications vol 302 no 4 pp 728ndash734 2003

[29] C Norais M Hawkins A L Hartman J A Eisen H Myl-lykallio and T Allers ldquoGenetic and physical mapping of DNAreplication origins in Haloferax volcaniirdquo PLoS Genetics vol 3no 5 article e77 2007

[30] J A Coker P DasSarma M Capes et al ldquoMultiple replicationorigins of Halobacterium sp strain NRC-1 properties of theconserved orc7-dependent oriC1rdquo Journal of Bacteriology vol191 no 16 pp 5253ndash5261 2009

[31] Z Wu J Liu H Yang H Liu and H Xiang ldquoMultiple repli-cation origins with diverse control mechanisms in Haloarculahispanicardquo Nucleic Acids Research 2013

[32] M Hawkins S Malla M J Blythe C A Nieduszynski and TAllers ldquoAccelerated growth in the absence of DNA replicationoriginsrdquo Nature vol 503 no 7477 pp 544ndash547 2013

[33] A I Majernık and J P J Chong ldquoA conserved mechanismfor replication origin recognition and binding in archaeardquo TheBiochemical Journal vol 409 no 2 pp 511ndash518 2008

[34] J E Galagan C Nusbaum A Roy et al ldquoThe genome of Macetivorans reveals extensive metabolic and physiological diver-sityrdquo Genome Research vol 12 no 4 pp 532ndash542 2002

[35] R Zhang and C-T Zhang ldquoIdentification of replication originsin archaeal genomes based on the Z-curve methodrdquo Archaeavol 1 no 5 pp 335ndash346 2005

[36] A Spang R Hatzenpichler C Brochier-Armanet et al ldquoDis-tinct gene set in two different lineages of ammonia-oxidizingarchaea supports the phylum Thaumarchaeotardquo Trends inMicrobiology vol 18 no 8 pp 331ndash340 2010

[37] K J Marians ldquoProkaryotic DNA replicationrdquo Annual Review ofBiochemistry vol 61 pp 673ndash719 1992

[38] S P Bell ldquoThe origin recognition complex from simple originsto complex functionsrdquo Genes and Development vol 16 no 6pp 659ndash672 2002

[39] V L Marsh and S D Bell ldquoDNA replication and the cell cyclerdquoin Archaea Evolution Physiology and Molecular Biology R AGarrett and H P Klenk Eds Blackwell Publishing HobokenNJ USA 2007

[40] F Matsunaga A Glatigny M-H Mucchielli-Giorgi et alldquoGenomewide and biochemical analyses of DNA-binding activ-ity of Cdc6Orc1 and Mcm proteins in Pyrococcus sprdquo NucleicAcids Research vol 35 no 10 pp 3214ndash3222 2007

[41] J Liu C L Smith D DeRyckere K DeAngelis G S Martinand J M Berger ldquoStructure and function of Cdc6Cdc18implications for origin recognition and checkpoint controlrdquoMolecular Cell vol 6 no 3 pp 637ndash648 2000

[42] M R Singleton R Morales I Grainge N Cook M NIsupov and D B Wigley ldquoConformational changes inducedby nucleotide binding in Cdc6ORC from Aeropyrum pernixrdquoJournal of Molecular Biology vol 343 no 3 pp 547ndash557 2004

[43] Y Ishino and S Ishino ldquoRapid progress of DNA replicationstudies in Archaea the third domain of liferdquo Science China LifeSciences vol 55 no 5 pp 386ndash403 2012

[44] E L Hendrickson R Kaul Y Zhou et al ldquoComplete genomesequence of the genetically tractable hydrogenotrophic meth-anogen Methanococcus maripaludisrdquo Journal of Bacteriologyvol 186 no 20 pp 6956ndash6969 2004

[45] B K Tye ldquoMCM proteins in DNA replicationrdquo Annual Reviewof Biochemistry vol 68 pp 649ndash686 1999

[46] K Labib and J F X Diffley ldquoIs the MCM2-7 complex theeukaryotic DNA replication fork helicaserdquo Current Opinion inGenetics amp Development vol 11 no 1 pp 64ndash70 2001

[47] I Ilves T Petojevic J J Pesavento and M R Botchan ldquoActi-vation of the MCM2-7 helicase by association with Cdc45 andGINS proteinsrdquoMolecular Cell vol 37 no 2 pp 247ndash258 2010

[48] M L Bochman andA Schwacha ldquoTheMcm complex unwind-ing the mechanism of a replicative helicaserdquo Microbiology andMolecular Biology Reviews vol 73 no 4 pp 652ndash683 2009

[49] Y Ishimi ldquoADNAhelicase activity is associated with anMCM4-6 and -7 protein complexrdquoThe Journal of Biological Chemistryvol 272 no 39 pp 24508ndash24513 1997

[50] Z Kelman and M F White ldquoArchaeal DNA replication andrepairrdquo Current Opinion in Microbiology vol 8 no 6 pp 669ndash676 2005

[51] J H LeBowitz and R McMacken ldquoThe Escherichia coli dnaBreplication protein is a DNA helicaserdquoThe Journal of BiologicalChemistry vol 261 no 10 pp 4738ndash4748 1986

[52] Z Kelman J-K Lee and J Hurwitz ldquoThe single minichro-mosome maintenance protein ofMethanobacterium thermoau-totrophicum ΔH contains DNA helicase activityrdquo Proceedings ofthe National Academy of Sciences of the United States of Americavol 96 no 26 pp 14783ndash14788 1999

[53] D F Shechter C Y Ying and J Gautier ldquoThe intrinsic DNAhelicase activity of Methanobacterium thermoautotrophicumΔH minichromosome maintenance proteinrdquo The Journal ofBiological Chemistry vol 275 no 20 pp 15049ndash15059 2000

[54] M de Felice L Esposito B Pucci M de Falco M Rossi andF M Pisani ldquoA CDC6-like factor from the archaea Sulfolobussolfataricus promotes binding of the mini-chromosome main-tenance complex to DNArdquoThe Journal of Biological Chemistryvol 279 no 41 pp 43008ndash43012 2004

[55] R Kasiviswanathan J-H Shin and Z Kelman ldquoInteractionsbetween the archaeal Cdc6 and MCM proteins modulate theirbiochemical propertiesrdquo Nucleic Acids Research vol 33 no 15pp 4940ndash4950 2005

[56] J-H Shin B Grabowski R Kasiviswanathan S D Bell andZ Kelman ldquoRegulation of minichromosomemaintenance heli-case activity by Cdc6rdquo The Journal of Biological Chemistry vol278 no 39 pp 38059ndash38067 2003

[57] M Akita A Adachi K Takemura T Yamagami F Matsunagaand Y Ishino ldquoCdc6Orc1 from Pyrococcus furiosus may actas the origin recognition protein and Mcm helicase recruiterrdquoGenes to Cells vol 15 no 5 pp 537ndash552 2010

12 Archaea

[58] M Krupovic S Gribaldo D H Bamford and P Forterre ldquoTheevolutionary history of archaeal MCM helicases a case study ofvertical evolution combined with hitchhiking of mobile geneticelementsrdquo Molecular Biology and Evolution vol 27 no 12 pp2716ndash2732 2010

[59] ADWalters and J P J Chong ldquoAn archaeal orderwithmultipleminichromosome maintenance genesrdquo Microbiology vol 156part 5 pp 1405ndash1414 2010

[60] A DWalters and J P J Chong ldquoMethanococcusmaripaludis anarchaeon with multiple functional MCM proteinsrdquo Biochemi-cal Society Transactions vol 37 no 1 pp 1ndash6 2009

[61] Q Xia E L Hendrickson Y Zhang et al ldquoQuantitative pro-teomics of the archaeon Methanococcus maripaludis validatedbymicroarray analysis and real time PCRrdquoMolecularampCellularProteomics vol 5 no 5 pp 868ndash881 2006

[62] F Sarmiento J Mrazek and W B Whitman ldquoGenome-scaleanalysis of gene function in the hydrogenotrophic methano-genic archaeon Methanococcus maripaludisrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 110 no 12 pp 4726ndash4731 2013

[63] M Pan T J Santangelo Z Li J N Reeve and Z KelmanldquoThermococcus kodakarensis encodes threeMCMhomologs butonly one is essentialrdquo Nucleic Acids Research vol 39 no 22 pp9671ndash9680 2011

[64] S Ishino S Fujino H Tomita et al ldquoBiochemical and geneticalanalyses of the three mcm genes from the hyperthermophilicarchaeon Thermococcus kodakarensisrdquo Genes to Cells vol 16no 12 pp 1176ndash1189 2011

[65] K S Makarova Y I Wolf S L Mekhedov B G Mirkin and EV Koonin ldquoAncestral paralogs and pseudoparalogs and theirrole in the emergence of the eukaryotic cellrdquo Nucleic AcidsResearch vol 33 no 14 pp 4626ndash4638 2005

[66] N Marinsek E R Barry K S Makarova I Dionne E VKoonin and S D Bell ldquoGINS a central nexus in the archaealDNA replication forkrdquo EMBOReports vol 7 no 5 pp 539ndash5452006

[67] T Yoshimochi R Fujikane M Kawanami F Matsunaga and YIshino ldquoTheGINS complex from Pyrococcus furiosus stimulatesthe MCM helicase activityrdquoThe Journal of Biological Chemistryvol 283 no 3 pp 1601ndash1609 2008

[68] T Oyama S Ishino S Fujino et al ldquoArchitectures of archaealGINS complexes essential DNA replication initiation factorsrdquoBMC Biology vol 9 article 28 2011

[69] H Ogino S Ishino K Mayanagi et al ldquoThe GINS com-plex from the thermophilic archaeon Thermoplasma aci-dophilummay function as a homotetramer inDNA replicationrdquoExtremophiles vol 15 no 4 pp 529ndash539 2011

[70] L Sanchez-Pulido and C P Ponting ldquoCdc45 the missing recjortholog in eukaryotesrdquoBioinformatics vol 27 no 14 pp 1885ndash1888 2011

[71] Z Li T J Santangelo L Cubonova J N Reeve and Z KelmanldquoAffinity purification of an archaeal DNA replication proteinnetworkrdquomBio vol 1 no 5 2010

[72] Z Li M Pan T J Santangelo et al ldquoA novel DNA nucleaseis stimulated by association with the GINS complexrdquo NucleicAcids Research vol 39 no 14 pp 6114ndash6123 2011

[73] L A Rajman and S T Lovett ldquoA thermostable single-strandDNase from Methanococcus jannaschii related to the RecJrecombination and repair exonuclease from Escherichia colirdquoJournal of Bacteriology vol 182 no 3 pp 607ndash612 2000

[74] K RWilliams J B Murphy and JW Chase ldquoCharacterizationof the structural and functional defect in the Escherichia colisingle-stranded DNA binding protein encoded by the ssb-1 mutant gene Expression of the ssb-1 gene under 120582p(L)regulationrdquoThe Journal of Biological Chemistry vol 259 no 19pp 11804ndash11811 1984

[75] S Dąbrowski M Olszewski R Pitek and J Kur ldquoNovel ther-mostable ssDNA-binding proteins fromThermus thermophilusand T aquaticus-expression and purificationrdquo Protein Expres-sion and Purification vol 26 no 1 pp 131ndash138 2002

[76] C Iftode Y Daniely and J A Borowiec ldquoReplication proteinA (RPA) the eukaryotic SSBrdquo Critical Reviews in Biochemistryand Molecular Biology vol 34 no 3 pp 141ndash180 1999

[77] A G Murzin ldquoOB(oligonucleotideoligosaccharide binding)-fold common structural and functional solution for non-hom-ologous sequencesrdquo The EMBO Journal vol 12 no 3 pp 861ndash867 1993

[78] C A Haseltine and S C Kowalczykowski ldquoA distinctive single-stranded DNA-binding protein from the Archaeon Sulfolobussolfataricusrdquo Molecular Microbiology vol 43 no 6 pp 1505ndash1515 2002

[79] R I M Wadsworth and M F White ldquoIdentification and pro-perties of the crenarchaeal single-stranded DNA binding pro-tein from Sulfolobus solfataricusrdquoNucleic Acids Research vol 29no 4 pp 914ndash920 2001

[80] I D Kerr R I M Wadsworth L Cubeddu W Blankenfeldt JHNaismith andM FWhite ldquoInsights into ssDNA recognitionby the OB fold from a structural and thermodynamic study ofSulfolobus SSB proteinrdquo The EMBO Journal vol 22 no 11 pp2561ndash2570 2003

[81] X Luo U Schwarz-Linek C H Botting R Hensel B Siebersand M F White ldquoCC1 a novel crenarchaeal DNA binding pro-teinrdquo Journal of Bacteriology vol 189 no 2 pp 403ndash409 2007

[82] T J Kelly P Simancek and G S Brush ldquoIdentification andcharacterization of a single-stranded DNA-binding proteinfrom the archaeonMethanococcus jannaschiirdquoProceedings of theNational Academy of Sciences of theUnited States of America vol95 no 25 pp 14634ndash14639 1998

[83] Z Kelman S Pietrokovski and J Hurwitz ldquoIsolation and cha-racterization of a split B-type DNA polymerase from the arch-aeonMethanobacterium thermoautotrophicumΔHrdquoTheJournalof Biological Chemistry vol 274 no 40 pp 28751ndash28761 1999

[84] K Komori and Y Ishino ldquoReplication protein A in Pyrococcusfuriosus is involved in homologous DNA recombinationrdquo TheJournal of Biological Chemistry vol 276 no 28 pp 25654ndash25660 2001

[85] J B Robbins M C Murphy B A White R I Mackie THa and I K O Cann ldquoFunctional analysis of multiple single-stranded DNA-binding proteins from Methanosarcina acetivo-rans and their effects on DNA synthesis by DNA polymeraseBIrdquoThe Journal of Biological Chemistry vol 279 no 8 pp 6315ndash6326 2004

[86] Y Lin L-J Lin P Sriratana et al ldquoEngineering of functionalreplication protein a homologs based on insights into the evolu-tion of oligonucleotideoligosaccharide-binding foldsrdquo Journalof Bacteriology vol 190 no 17 pp 5766ndash5780 2008

[87] D N Frick and C C Richardson ldquoDNA primasesrdquo AnnualReview of Biochemistry vol 70 pp 39ndash80 2001

[88] G Desogus S Onesti P Brick M Rossi and F M PisanildquoIdentification and characterization of a DNA primase fromthe hyperthermophilic archaeon Methanococcus jannaschiirdquoNucleic Acids Research vol 27 no 22 pp 4444ndash4450 1999

Archaea 13

[89] A A Bocquier L Liu I K O Cann K Komori D Kohda andY Ishino ldquoArchaeal primase bridging the gap between RNAand DNA polymerasesrdquo Current Biology vol 11 no 6 pp 452ndash456 2001

[90] L Liu K Komori S Ishino et al ldquoThe archaeal DNA primasebiochemical characterization of the p41-p46 complex fromPyrococcus furiosusrdquo The Journal of Biological Chemistry vol276 no 48 pp 45484ndash45490 2001

[91] E Matsui M Nishio H Yokoyama K Harata S Darnisand I Matsui ldquoDistinct domain functions regulating de novoDNA synthesis of thermostable DNA primase from hyperther-mophile Pyrococcus horikoshiirdquo Biochemistry vol 42 no 50 pp14968ndash14976 2003

[92] N Ito I Matsui and EMatsui ldquoMolecular basis for the subunitassembly of the primase from an archaeon Pyrococcus hori-koshiirdquoThe FEBS Journal vol 274 no 5 pp 1340ndash1351 2007

[93] M le Breton G Henneke C Norais et al ldquoThe heterodimericprimase from the euryarchaeon Pyrococcus abyssi a multifunc-tional enzyme for initiation and repairrdquo Journal of MolecularBiology vol 374 no 5 pp 1172ndash1185 2007

[94] S-H Lao-Sirieix and S D Bell ldquoThe heterodimeric primaseof the hyperthermophilic archaeon Sulfolobus solfataricus pos-sesses DNA and RNA primase polymerase and 31015840-terminalnucleotidyl transferase activitiesrdquo Journal of Molecular Biologyvol 344 no 5 pp 1251ndash1263 2004

[95] S-H Lao-Sirieix L Pellegrini and S D Bell ldquoThe promiscuousprimaserdquo Trends in Genetics vol 21 no 10 pp 568ndash572 2005

[96] J Hu L Guo K Wu B Liu S Lang and L Huang ldquoTemplate-dependent polymerization across discontinuous templatesby the heterodimeric primase from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquoNucleic Acids Research vol 40no 8 pp 3470ndash3483 2012

[97] E Evguenieva-Hackenberg P Walter E Hochleitner FLottspeich and G Klug ldquoAn exosome-like complex in Sulfolo-bus solfataricusrdquo EMBOReports vol 4 no 9 pp 889ndash893 2003

[98] P Walter F Klein E Lorentzen A Ilchmann G Klug andE Evguenieva-Hackenberg ldquoCharacterization of native andreconstituted exosome complexes from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Microbiology vol62 no 4 pp 1076ndash1089 2006

[99] Z Zuo C J Rodgers A L Mikheikin and M A Trak-selis ldquoCharacterization of a functional DnaG-type primase inarchaea implications for a dual-primase systemrdquo Journal ofMolecular Biology vol 397 no 3 pp 664ndash676 2010

[100] B R Berquist P DasSarma and S DasSarma ldquoEssential andnon-essential DNA replication genes in the model halophilicArchaeon Halobacterium sp NRC-1rdquo BMC Genetics vol 8article 31 2007

[101] D K Braithwaite and J Ito ldquoCompilation alignment andphylogenetic relationships of DNA polymerasesrdquo Nucleic AcidsResearch vol 21 no 4 pp 787ndash802 1993

[102] I K O Cann and Y Ishino ldquoArchaeal DNA replication iden-tifying the pieces to solve a puzzlerdquo Genetics vol 152 no 4 pp1249ndash1267 1999

[103] G Lipps S Rother C Hart and G Krauss ldquoA novel typeof replicative enzyme harbouring ATpase primase and DNApolymerase activityrdquo The EMBO Journal vol 22 no 10 pp2516ndash2525 2003

[104] J Yamtich and J B Sweasy ldquoDNA polymerase family X func-tion structure and cellular rolesrdquoBiochimica et BiophysicaActavol 1804 no 5 pp 1136ndash1150 2010

[105] H Ohmori E C Friedberg R P P Fuchs et al ldquoThe Y-familyof DNA polymerasesrdquoMolecular Cell vol 8 no 1 pp 7ndash8 2001

[106] N Y Yao R E Georgescu J Finkelstein and M E OrsquoDonnellldquoSingle-molecule analysis reveals that the lagging strandincreases replisome processivity but slows replication forkprogressionrdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 106 no 32 pp 13236ndash132412009

[107] U Hubscher G Maga and S Spadari ldquoEukaryotic DNA poly-merasesrdquo Annual Review of Biochemistry vol 71 pp 133ndash1632002

[108] F Boudsocq S Iwai F Hanaoka and R Woodgate ldquoSulfolobussolfataricus P2 DNA polymerase IV (Dp04) an archaeal DinB-like DNA polymerase with lesion-bypass properties akin toeukaryotic pol120578rdquo Nucleic Acids Research vol 29 no 22 pp4607ndash4616 2001

[109] L-J Lin A Yoshinaga Y Lin et al ldquoMolecular analyses ofan unusual translesion DNA polymerase fromMethanosarcinaacetivorans C2Ardquo Journal of Molecular Biology vol 397 no 1pp 13ndash30 2010

[110] I K O Cann S Ishino NNomura Y Sako andY Ishino ldquoTwofamily B DNA polymerases from Aeropyrum pernix an aerobichyperthermophilic crenarchaeoterdquo Journal of Bacteriology vol181 no 19 pp 5984ndash5992 1999

[111] T Uemori Y Ishino H Doi and I Kato ldquoThe hyperther-mophilic archaeon Pyrodictium occultum has two 120572-like DNApolymerasesrdquo Journal of Bacteriology vol 177 no 8 pp 2164ndash2177 1995

[112] T Uemori Y Ishino H Toh K Asada and I Kato ldquoOrgani-zation and nucleotide sequence of the DNA polymerase genefrom the archaeon Pyrococcus furiosusrdquo Nucleic Acids Researchvol 21 no 2 pp 259ndash265 1993

[113] B A Connolly ldquoRecognition of deaminated bases by archaealfamily-B DNA polymerasesrdquo Biochemical Society Transactionsvol 37 no 1 pp 65ndash68 2009

[114] B A Connolly M J Fogg G Shuttleworth and B T WilsonldquoUracil recognition by archaeal family B DNA polymerasesrdquoBiochemical Society Transactions vol 31 no 3 pp 699ndash7022003

[115] T T Richardson X Wu B J Keith P Heslop A C Jones andB A Connolly ldquoUnwinding of primer-templates by archaealfamily-B DNA polymerases in response to template-stranduracilrdquo Nucleic Acids Research vol 41 no 4 pp 2466ndash24782013

[116] T Lindahl ldquoInstability and decay of the primary structure ofDNArdquo Nature vol 362 no 6422 pp 709ndash715 1993

[117] I B Rogozin K S Makarova Y I Pavlov and E V Koonin ldquoAhighly conserved family of inactivated archaeal B family DNApolymerasesrdquo Biology Direct vol 3 article 32 2008

[118] M Imamura T Uemori I Kato and Y Ishino ldquoA non-120572-like DNA polymerase from the hyperthermophilic archaeonPyrococcus furiosusrdquoBiological andPharmaceutical Bulletin vol18 no 12 pp 1647ndash1652 1995

[119] I K O Cann K Komori H Toh S Kanai and Y IshinoldquoA heterodimeric DNA polymerase evidence that members ofEuryarchaeota possess a distinct DNA polymeraserdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 95 no 24 pp 14250ndash14255 1998

[120] L Aravind D D Leipe and E V Koonin ldquoToprimmdasha con-served catalytic domain in type IA and II topoisomerases

14 Archaea

DnaG-type primases OLD family nucleases and RecR pro-teinsrdquo Nucleic Acids Research vol 26 no 18 pp 4205ndash42131998

[121] M Jokela A Eskelinen H Pospiech J Rouvinen and J ESyvaoja ldquoCharacterization of the 31015840 exonuclease subunit DP1of Methanococcus jannaschii replicative DNA polymerase DrdquoNucleic Acids Research vol 32 no 8 pp 2430ndash2440 2004

[122] T Uemori Y Sato I Kato H Doi and Y Ishino ldquoA novel DNApolymerase in the hyperthermophilic archaeon Pyrococcus fur-iosus gene cloning expression and characterizationrdquo Genes toCells vol 2 no 8 pp 499ndash512 1997

[123] Y Shen K Musti M Hiramoto H Kikuchi Y Kawarabayashiand I Matsui ldquoInvariant Asp-1122 and Asp-1124 are essentialresidues for polymerization catalysis of family D DNA poly-merase from Pyrococcus horikoshiirdquo The Journal of BiologicalChemistry vol 276 no 29 pp 27376ndash27383 2001

[124] G Henneke D Flament U Hubscher J Querellou and J-P Raffin ldquoThe hyperthermophilic euryarchaeota Pyrococcusabyssi likely requires the two DNA polymerases D and B forDNA replicationrdquo Journal of Molecular Biology vol 350 no 1pp 53ndash64 2005

[125] L Cubonova T Richardson B W Burkhart et al ldquoArchaealDNA polymerase D but not DNA polymerase B is required forgenome replication in Thermococcus kodakarensisrdquo Journal ofBacteriology vol 195 no 10 pp 2322ndash2328 2013

[126] C Rouillon G Henneke D Flament J Querellou and J-PRaffin ldquoDNA polymerase switching on homotrimeric PCNA atthe replication fork of the euryarchaea Pyrococcus abyssirdquo Jour-nal of Molecular Biology vol 369 no 2 pp 343ndash355 2007

[127] G Henneke ldquoIn vitro reconstitution of RNA primer removal inArchaea reveals the existence of two pathwaysrdquoTheBiochemicalJournal vol 447 no 2 pp 271ndash280 2012

[128] G-LMoldovan B Pfander and S Jentsch ldquoPCNA themaestroof the replication forkrdquo Cell vol 129 no 4 pp 665ndash679 2007

[129] X-P Kong R Onrust M OrsquoDonnell and J Kuriyan ldquoThree-dimensional structure of the 120573 subunit of E coli DNA poly-merase III holoenzyme a sliding DNA clamprdquo Cell vol 69 no3 pp 425ndash437 1992

[130] K Daimon Y Kawarabayasi H Kikuchi Y Sako and Y IshinoldquoThree proliferating cell nuclear antigen-like proteins foundin the hyperthermophilic archaeon Aeropyrum pemix interac-tions with the two DNA polymerasesrdquo Journal of Bacteriologyvol 184 no 3 pp 687ndash694 2002

[131] I Dionne R K Nookala S P Jackson A J Doherty andS D Bell ldquoA heterotrimeric PCNA in the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Cell vol 11 no 1pp 275ndash282 2003

[132] E Warbrick ldquoPCNA binding through a conserved motifrdquoBioEssays vol 20 no 3 pp 195ndash199 1998

[133] H Nishida K Mayanagi S Kiyonari et al ldquoStructural deter-minant for switching between the polymerase and exonucleasemodes in the PCNA-replicative DNA polymerase complexrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 106 no 49 pp 20693ndash20698 2009

[134] K Mayanagi S Kiyonari H Nishida et al ldquoArchitecture of theDNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complexrdquo Proceedings of the National Academy ofSciences of the United States of America vol 108 no 5 pp 1845ndash1849 2011

[135] B Castrec C Rouillon G Henneke D Flament J Querellouand J-P Raffin ldquoBinding to PCNA in Euryarchaeal DNA

replication requires two PIP motifs for DNA polymerase D andone PIP motif for DNA polymerase Brdquo Journal of MolecularBiology vol 394 no 2 pp 209ndash218 2009

[136] P F Pluchon T Fouqueau C Creze et al ldquoAn extendednetworkof genomic maintenance in the archaeon Pyrococcus abyssihighlights unexpected associations between eucaryotic homo-logsrdquo PLoS One vol 8 no 11 Article ID e79707 2013

[137] J E Ladner M Pan J Hurwitz and Z Kelman ldquoCrystalstructures of two active proliferating cell nuclear antigens(PCNAs) encoded byThermococcus kodakaraensisrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2711ndash2716 2011

[138] Y Kuba S Ishino T Yamagami et al ldquoComparative analyses ofthe two proliferating cell nuclear antigens from the hyperther-mophilic archaeonThermococcus kodakarensisrdquo Genes to Cellsvol 17 no 11 pp 923ndash937 2012

[139] T Fukui H Atomi T Kanai R Matsumi S Fujiwara andT Imanaka ldquoComplete genome sequence of the hyperther-mophilic archaeon Thermococcus kodakaraensis KOD1 andcomparison with Pyrococcus genomesrdquo Genome Research vol15 no 3 pp 352ndash363 2005

[140] D Jeruzalmi O Yurieva Y Zhao et al ldquoMechanism of proces-sivity clamp opening by the delta subunit wrench of the clamploader complex of E coliDNApolymerase IIIrdquoCell vol 106 no4 pp 417ndash428 2001

[141] Y Shiomi J Usukura Y Masamura et al ldquoATP-dependentstructural change of the eukaryotic clamp-loader protein repli-cation factor Crdquo Proceedings of the National Academy of Sciencesof the United States of America vol 97 no 26 pp 14127ndash141322000

[142] T Miyata T Oyama K Mayanagi S Ishino Y Ishino and KMorikawa ldquoThe clamp-loading complex for processive DNAreplicationrdquoNature Structural andMolecular Biology vol 11 no7 pp 632ndash636 2004

[143] T Oyama Y Ishino I K O Cann S Ishino and K MorikawaldquoAtomic structure of the clamp loader small subunit fromPyrococcus furiosusrdquo Molecular Cell vol 8 no 2 pp 455ndash4632001

[144] A Seybert D J Scott S Scaife M R Singleton and DB Wigley ldquoBiochemical characterisation of the clampclamploader proteins from the euryarchaeon Archaeoglobus fulgidusrdquoNucleic Acids Research vol 30 no 20 pp 4329ndash4338 2002

[145] Y-H Chen Y Lin A Yoshinaga et al ldquoMolecular analyses of athree-subunit euryarchaeal clamp loader complex from Meth-anosarcina acetivoransrdquo Journal of Bacteriology vol 191 no 21pp 6539ndash6549 2009

[146] Y-H Chen S A Kocherginskaya Y Lin et al ldquoBiochemicaland mutational analyses of a unique clamp loader complex inthe archaeon Methanosarcina acetivoransrdquo The Journal of Bio-logical Chemistry vol 280 no 51 pp 41852ndash41863 2005

[147] F Matsunaga C Norais P Forterre and H Myllykallio ldquoIden-tification of short ldquoeukaryoticrdquo Okazaki fragments synthesizedfrom a prokaryotic replication originrdquo EMBO Reports vol 4no 2 pp 154ndash158 2003

[148] H Kochiwa M Tomita and A Kanai ldquoEvolution of ribonucle-ase H genes in prokaryotes to avoid inheritance of redundantgenesrdquo BMC Evolutionary Biology vol 7 article 128 2007

[149] N OhtaniMHarukiMMorikawa and S Kanaya ldquoMoleculardiversities of RNases Hrdquo Journal of Bioscience and Bioengineer-ing vol 88 no 1 pp 12ndash19 1999

Archaea 15

[150] N Ohtani M Haruki M Morikawa R J Crouch M Itayaand S Kanaya ldquoIdentification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII fromBacillus subtilis classification of RNases H into three familiesrdquoBiochemistry vol 38 no 2 pp 605ndash618 1999

[151] N Ohtani H Yanagawa M Tomita and M Itaya ldquoIdentifi-cation of the first archaeal type 1 RNase H gene from Halobac-terium sp NRC-1 archaeal RNase HI can cleave an RNA-DNAjunctionrdquoThe Biochemical Journal vol 381 no 3 pp 795ndash8022004

[152] N Ohtani H Yanagawa M Tomita and M Itaya ldquoCleavage ofdouble-stranded RNA by RNase HI from a thermoacidophilicarchaeon Sulfolobus tokodaii 7rdquo Nucleic Acids Research vol 32no 19 pp 5809ndash5819 2004

[153] M A Nowak M C Boerlijst J Cooke and J M SmithldquoEvolution of genetic redundancyrdquo Nature vol 388 no 6638pp 167ndash170 1997

[154] A E Tomkinson S Vijayakumar J M Pascal and T Ellen-berger ldquoDNA ligases structure reactionmechanism and func-tionrdquo Chemical Reviews vol 106 no 2 pp 687ndash699 2006

[155] M Nakatani S Ezaki H Atomi and T Imanaka ldquoA DNAligase from a hyperthermophilic archaeon with unique cofactorspecificityrdquo Journal of Bacteriology vol 182 no 22 pp 6424ndash6433 2000

[156] Y Sun M S Seo J H Kim et al ldquoNovel DNA ligase with broadnucleotide cofactor specificity from the hyperthermophilic cre-narchaeon Sulfophobococcus zilligii influence of ancestral DNAligase on cofactor utilizationrdquo Environmental Microbiology vol10 no 12 pp 3212ndash3224 2008

[157] T R Beattie and S D Bell ldquoCoordination of multiple enzymeactivities by a single PCNA in archaeal Okazaki fragmentmaturationrdquo The EMBO Journal vol 31 no 6 pp 1556ndash15672012

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

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BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

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Nucleic AcidsJournal of

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Enzyme Research

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International Journal of

Microbiology

6 Archaea

also present in vitro [93] Interestingly the archaeal primasesmall subunit resembles DNA polymerases from the Pol Xfamily in sequence and structure suggesting a similarity intheir catalytic mechanism [96]

Homologs of the bacterial DnaG primase are also foundin archaea However in vitro studies of the P furiosusenzyme failed to detect primer synthesis activity and the TkodakaraensisDnaG was copurified with proteins of the exo-some [71] Also in S solfataricus DnaG primase was found tobe a core exosome subunit involved in RNA degradation [9798] However recent studies demonstrated that the S solfa-taricus DnaG homolog has limited primer synthesis activityand a dual primase system with PriSL has been proposed tofunction during DNA replication [99] Hu et al hypothesizedan interesting theory which suggests that LUCA employed adual-primase system comprisingDnaG and PriSL which alsoserved roles in RNA degradation and the nonhomologousend joining (NHEJ) pathwayThe system was inherited by allthree domains In theArchaea domain it retained its originalfunctions However in the Bacteria domain DnaG becamethe major replicative primase and PriSL evolved into the Poldomain of LigD involved in the NHEJ pathway In contrastDnaG was lost in the Eukaryota domain and PriSL becamethe only replicative primase In addition it also evolved intothe DNA Pol X family involved in NHEJ [96]

Like other ArchaeaM maripaludis S2 possesses both theeukaryotic- and bacterial-like primases A new genome-widesurvey of this methanoarchaea revealed that genes encodingboth subunits of the eukaryotic like primase PriS and PriL(MMP0009 and MMP0071) were likely to be essential forgrowth which is consistent with a role in replication Similarobservations have been demonstrated in other Archaea suchas Halobacterium sp NRC-1and Haloferax volcanii [93 100]In contrast the DnaG primase (MMP1286) was nonessentialwhich would be consistent with a role in the exosome [62]These results suggest that in M maripaludis and probablyother euryarchaeotes a dual primase system is not pre-sent

33 Elongation (Replicative DNA Polymerase) The primersynthesized by the primase is further extended by a replicativeDNA polymerase DNA polymerases have been classifiedinto seven families based on their amino acid sequencesimilarity (A B C D E X and Y) [101ndash105] In Bacteria Ecoli possesses five DNA polymerases Pol IndashV where the firstthree belong to families A B and C respectively and the lasttwo belong to the Y family The major replicative DNA poly-merase in E coli is Pol III a member of the C family whichsynthesizes DNA with high processivity when functioningwithin the holoenzyme [106] In eukaryotes a great diversityof DNA polymerases is also found but DNA replicationrequires three replicative DNA polymerases which belongto family B (Pol120572 Pol120575 and Pol120576) [107] In Archaea fewertypes of DNA polymerases are present but they have aninteresting evolutionary division Representatives of theDNApolymerase B family are found in all Archaea The D familyDNA polymerase is present in every phyla studied so farwith the exception of the Crenarchaeota (Figure 1) Lastly amember of theY family has been identified andbiochemically

characterized in S solfataricus [108] and the Methanosarci-nales in which several species harbor two homologs [109]Even though the activity of DNA polymerases belongingto the Y family in archaea is not fully understood they aresuggested to play an important role in DNA repair [109]

Representatives of the DNA polymerase family B havebeen identified in all Archaea The crenarchaeotes possess atleast two family B DNA polymerases (PolB I and PolB IIand in some cases PolB III) [102 110 111] The recombinantS solfataricus Pyrodictium occultum and A pernix enzymeshave been characterized [102] In contrast euryarchaeotesonly contain PolB I The recombinant P furiosus enzymehas been characterized [112] The PolB I enzymes havesimilar amino acid sequence and overall structure and theypossess a potent 31015840-51015840exonuclease proofreading activity [102]A unique property of the archaeal family B DNA polymeraseis the ability to stall DNA polymerization in the presenceof uracil or hypoxanthine deaminated bases [113 114] thisproperty helps to prevent the copy of template-strand uraciland the transmission of fixed mutations to progeny [115]Commonly cytosine deamination converts GC base pairsinto the promutagenic GU mismatches which result in50 of the offspring containing an AT transition mutationafter replication [116] In addition when A-U base pairs areformed the loss of the 5-methyl moiety upon replacementof thymine can exert a detrimental effect on protein DNAinteractions Interestingly in some crenarchaeotes and eur-yarchaeotes one of the B family DNA polymerase paralogspossesses disrupted versions of the sequence motifs thatare essential for catalysis Possibly these enzymes possess astructural role [117]

DNA polymerase family D (PolD) is a novel enzyme thatwas originally discovered in P furiosus [118] It has sincethen been identified in all euryarchaeotes [119] For a longtime this enzyme was considered a euryarchaeote-specificpolymerase but the three newly discovered archaeal phylawere also found to possess genes for PolD [14ndash16] PolD isa heterodimer with a small subunit (DP1) and a large subunit(DP2) It has been proposed that the large subunit harborsthe polymerase activity although its sequence is very differentfrom other hitherto described DNA polymerases The smallsubunit possesses high similarity with the noncatalytic B-subunits of the eukaryoticDNApolymerases120572 120575 and 120576 [120]Studies of the M jannaschii enzyme demonstrated that thesmall subunit possesses a strong 31015840-51015840exonuclease activitysuggesting that it may be involved in proofreading activity[7 121] Efficient polymerase and proofreading activity havealso been detected from a purified PolD of P furiosus andthe residues Asp-1122 and Asp-1124 are essential for thepolymerization reaction in P horikoshii [122 123] Everyeuryarchaeote examined possessed one homolog for DP1 andDP2 except forMethanococcoides burtoniiDSM 6242 whichpossesses two homologs for DP1 (Figure 1)

Because the crenarchaeotes only possess family B DNApolymerases one of themmust be the replicative polymeraseHowever in euryarchaeotes it was not clear which enzymewas involved in replication Studies in Halobacterium spNRC-1 showed that both PolB and PolD were essential forviability and it was proposed that they could be working

Archaea 7

together at the replication fork synthesizing the leading andlagging strand respectively [100 124] However in otherEuryarchaeota PolB does not appear to be essential Forinstance a recent report demonstrated that both subunits ofPolDwere essential but PolB was nonessential for the growthof M maripaludis S2 [62] Likewise in T kodakaraensisPolD can be coisolated with different proteins of the archaealreplication fork but PolB wasmainly coisolated with proteinsof unknown function [71] A deletion of the PolB in Tkodakaraensis also had no detectable effect on cell viability[125] Interestingly T kodakaraensis PolB mutants haveincreased sensitivity to UV radiation These results togethersuggest that PolD is the essential replicative DNA polymerasein these euryarchaeotes and not a PolB family polymeraseIn this scenario PolB may have some other crucial functionin Halobacterium and possibly other closely related specieswhich it is not conserved throughout the phylum Finallyit has been demonstrated that purified PolD from P abyssiis able to perform strand displacement and RNA primerextension in vitro Purified PolB on its own cannot performthese activities in vitro but in the presence of PCNA stranddisplacement activity is stimulated [124 126] A recent in vitrostudy in P abyssi demonstrated that RNase HII is required toinitiate strand displacement DNA synthesis by PolB [127]

34 Elongation (Other Accessory Proteins) Purified DNApolymerases possess low processivity however the addi-tion of an accessory factor the sliding clamp gives DNApolymerases the required processivity to replicate genomesThis factor whose structure resembles a doughnut functionsas a molecular platform which recruits several replication-associated enzymes and act together with DNA and thepolymerase to stabilize their interactions during replication[128] The structure of sliding clamps is conserved in thethree domains of life In Bacteria the sliding clamp or 120573-subunit is a homodimeric ring [129] In eukaryotes thesliding clamp or proliferating cell nuclear antigen (PCNA)is a homotrimeric ring [128] In Archaea the majority ofcrenarchaeotes have multiple PCNA homologs which formheterotrimeric rings [130 131] (Figure 1) In contrast mosteuryarchaeotes possess a single PCNA homolog (Figure 1)Interactions of DNA polymerase with the sliding clampare mediated through a common motif called the PCNAInteracting Protein (PIP) box [132] The three dimensionalstructures of PCNA-PolB and the PolB-PCNA-DNA complexfrom P furiosus have been solved shedding light on theinteractions between these molecules [133 134] In additiona study demonstrated that the PolDPCNA and PolBPCNAinteractions require two and one PIP boxes respectively[135] Recently through a protein-interaction network of Pabyssi a previously unknown protein with nuclease activity(Pab0431) and a PIP canonical motif was discovered tointeract with PCNA suggesting a possible involvement inDNA replication [136] T kodakaraensis is the only well-documented example of an euryarchaeotewith twohomologsfor PCNA TK0535 (PCNA1) and TK0582 (PCNA2) Recentwork demonstrated both proteins form stable homotrimericrings that interact with T kodakaraensis PolB in vitro [137]A more detailed study of the two homologs of PCNA in T

kodakaraensis demonstrated that both homologs stimulate invitro the primer extension activity of PolB but only PCNA1and not PCNA2 stimulates the same activity of PolD [138]Also the same report showed that the pcna2 gene can bedisrupted without causing growth deficiencies but it was notpossible to isolate mutants of pcna1 These results suggestthat PCNA1 but not PCNA2 is essential for DNA replication[138] It has been proposed that one of the PCNA geneswas acquired by lateral gene transfer [139] Members of theorderMethanococcales possess one PCNA homolog with twoexceptionsMmaripaludis S2 possesses twoPCNAhomologs(MMP1126 and 1711) [60] Both genes appeared to be essentialfor growth suggesting that they both play an importantrole in replication [62] The gene MMP1711 possesses highsimilarity to both T kodakaraensis genes and is likely thetrue methanococcal PCNA In contrast MMP1126 possessesonly low similarity to the T kodakaraensis genes and alsocontains an S-adenosylmethionine-dependent methyltrans-ferases domain Thus it is likely to possess some alternativefunction Methanotorris igneus Kol 5 also possesses twoPCNA homologs

For PCNA to assemble around DNA a specific loadingfactor is required In Bacteria the loading factor is knownas 120574-complex and comprises three different subunits ina 1205743-120575-1205751015840 stoichiometry [140] In eukaryotes the loading

factor is known as Replication Factor C (RFC) and is aheteropentameric complex comprising one large subunit andfour different small subunits [141] In contrast inArchaea theRFC consists of two different proteins a small subunit RFCSand a large subunit RFCLThey also form a heteropentamericcomplex in a 4 1 ratio (RFCS RFCL) Interestingly manycrenarchaeotes possess one homolog of RFCL and two orthree homologs of RFCS Alternatively most euryarchaeotespossess only one RFCL and RFCS homolog The exceptionsare somemembers of the ordersHalobacteriales Methanomi-crobiales and Methanosarcinales which possess two RFCShomologs (Figure 1) Structural and biochemical studies ofRFC have been conducted in several euryarchaeotes such asArchaeoglobus fulgidus and Pyrococcus species [142ndash144] Aninteresting case is observed in Methanosarcina acetivoransThis RFC possesses three subunits (RFC1 2 L) found ina ratio 3 1 1 [145] Homologs for these three subunits arealso present in most of the genomes of the haloarchaea[145] It is inferred that this type of RFC complex representsan intermediary form transitional between the canonicalarchaeal RFC complex of one small and one large subunit andthe eukaryotic RFC complex of four different small and onelarge subunit [146] The organization and spatial distributionexhibit a similarity to the E coliminimal 120574-complex but thefunction of the subunits is probably not conserved [145]

35 Maturation During DNA replication the lagging strandis discontinuously synthesized by extending the RNAprimersor Okazaki fragments This discontinuously synthesizedDNA strand requires maturation to form a single covalentlyclosed strand to end the replication process In ArchaeaOkazaki fragments were first demonstrated during replica-tion in P abyssi and Sulfolobus acidocaldarius [147] Duringreplication these RNA primers are replaced with DNA The

8 Archaea

removal of the primers is performed by the enzyme RNase Hwhich is ubiquitous in the three domains of life Accordingto their sequence similarity in prokaryotes the RNase Hproteins are classified into three groups RNase HI HII andHIII In eukaryotes they are classified as RNase H1 and H2[148] However phylogenetic analyses suggest that the RNaseH proteins can also be classified into two different groupsType 1 (prokaryotic RNaseHI eukaryotic RNaseH1 and viralRNase H) and Type 2 (prokaryotic RNase HII and HIII andeukaryotic RNase H2) [149] These two types of RNase Hpossess different specific activities metal ion preferences andcleavage sites [150] Originally it was thought that Archaeaonly possess type 2 RNase H [149] but several type 1 archaealRNase H enzymes have since then been discovered [151 152]Interestingly in eukaryotes RNaseH1 andH2 tend to coexistand different combinations of the three prokaryotic RNasesH(I II and III) are found except for the combination of RNasesHI and HIII This mutually exclusive evolution of some ofthe prokaryotic RNases seems to be related to functionalredundancy [148]

Another enzyme involved in primer replacement inDNA replication is the Flap endonuclease I (FEN-1) whichrecognizes double-strandedDNAwith an unannealed 51015840-flapand cleaves it A eukaryotic homolog of FEN-1 is found inevery archaeal member analyzed and one member of theThermoproteales Thermofilum pendens Hrk5 possesses twohomologs

M maripaludis S2 possesses genes for the prokaryoticRNase HI and HII and for FEN-1 but none are essentialsuggesting that they may be redundant in their functions[44 62] Possibly both RNase H proteins persist and areevolutionary stable in the genome The gene products mayperform the same function but one is less efficient than theother [153]

After the Okazaki fragments are replaced by DNA inthe lagging strand the nick between the newly synthesizedand the elongated DNA is repaired by a DNA ligase Thisenzyme uses a nucleotide cofactor to catalyze the formationof the phosphodiester bond in three well-characterized steps[154]The enzyme is common to all three domains but can begrouped into two families based on cofactor specificity (ATPor NAD+) The DNA ligases from several crenarchaeotes andeuryarchaeotes have been further characterized (reviewedin [43]) Many archaeal DNA ligases possess dual cofactorspecificity (ATPNAD+ or ATPADP) but every archaealDNA ligase characterized so far uses ATP A thermophilicDNA ligase from M thermautotrophicus which uses ATP assole cofactor was characterized in vitro [155] A characterizedDNA ligase from the crenarchaeote Sulfophobococcus zilligiidisplayed specificity for three cofactors (ATPNAD+GTP)[156]Major structuralwork in this enzymehas been achievedin P furiosus and S solfataricus and the findings have beenreviewed in detail [43] InM maripaludis S2 the DNA ligaseis likely to be essential for growth [44 62]

Understanding the maturation process in archaea hasbecome a focus of increasing research in recent years An invitro study reconstituted the Okazaki fragment maturationusing proteins derived from the crenarchaeote S solfataricusThey demonstrated that only six proteins are necessary for

coupled DNA synthesis RNA primer removal and DNAligation In this model a single PCNA (heterotrimeric ring)coordinates the activities of PolBI FEN-1 and DNA ligaseinto an efficient maturation complex [157] A different invitro study in P abyssi has demonstrated two different modelsfor Okazaki fragments maturation which differ in the RNAprimer removal process In the first model RNA primerelimination is executed by continuous PolD strand displace-ment DNA synthesis and 51015840RNA flap cleavage by FEN-1The resulting nicks are closed by DNA ligase Alternativelythe second model proposes that RNase HII cleaves theRNA primer followed by the action of FEN-1 and stranddisplacement DNA synthesis by polB or polD The nick isthen sealed by DNA ligase [127] Testing these models invivo is of great interest to complete the picture of how theseprocesses behave in the cell In addition other factors that canmodulate these processesmay be required for coordination ofthe in vivomaturation process

4 Conclusions

DNA replication in archaea possesses a dual nature wherethe machinery is structurally and functionally similar to theeukaryotic replication system but it is executed within abacterial context [11 25] Additionally unique archaeal fea-tures demonstrate the complexity of this process and it doesnot appear to be just a simplified version of the eukary-otic system For example the archaeal specific DNA poly-merase D is conserved across the Archaea domain with theexception of the Crenarchaeota phylumThe recent discoverythat it is the essential replicative polymerase in two differenteuryarchaeotic species demonstrates an unanticipated vari-ability in archaeal DNA replication and a fundamental differ-ence in the replication mechanism between crenarchaeotesand euryarchaeotes Interestingly the absence of PolD increnarchaeotes is not the only difference in DNA repli-cation These differences include the absence of histonesin crenarchaeotes [4] the presence of multiple origins ofreplication in crenarchaeotes and a single origin of repli-cation in most euryarchaeotes the absence of GINS23 inmost euryarchaeotes the absence of RPA protein in manycrenarchaeotes the presence of multiple MCM homologs inMethanococcales and the presence of one homolog of PCNAin euryarchaeotes compared to the multiple homologs increnarchaeotes These distinctive characteristics between thephyla highlight the complexity of archaeal DNA replicationand suggest a complex evolutionary history (Table 1)

Among the Euryarchaeota the ordersHalobacteriales andMethanococcales possess differences in the DNA replicationsystem that make them unique For instance Halobac-teriales possess many more origin recognition proteins(Orc1Cdc6) compared to the rest of the archaea On theother hand Methanococcales and Methanopyrales lack rec-ognizable homologs for the Orc1Cdc6 proteins suggestingthe presence of a very different mechanism for initiation ofreplication In addition the Methanococcales possess a largenumber of MCM protein homologs It has been proposedthat these distinctive features are connected and because ofthe absence of the Orc1Cdc6 proteins MCM proteins may

Archaea 9

Table1DNAreplicationproteins

andfeatures

inthed

omains

BacteriaEukaryotaand

thetwomajor

phylao

fthe

Archaeado

main

Mod

ified

from

[43]

DNAreplicationstage

Process

Bacteria

Eukaryota

Archaea

Crenarchaeota

Euryarchaeota

Preinitia

tion

Orig

inof

replication

Sing

leMultip

leMultip

leSing

lea

Orig

inrecogn

ition

DnaA

ORC

complex

(ORC

1-6)

Orc1C

dc6

Orc1C

dc6b

Initiation

DNAun

winding

(Helicase)

DnaB

MCM

complex

(MCM

2-7)

MCM

complex

MCM

complex

DNAun

winding

(Accessory

proteins)

DnaC

Cdc6

GIN

S23GIN

S15

GIN

S15c

Cdt1

GIN

Scomplex

(Sld5Psf1-3)

RecJho

molog

RecJho

molog

Cdc45

Prim

ersynthesis

DnaG

Pol120572

prim

asec

omplex

DNAprim

ase

(PriS

L)D

naG

dDNAprim

ase(PriSL)

Elon

gatio

n

DNAsynthesis

(polym

erase)

PolIII(Fam

ilyCDNApo

lymerase)

Pol120575and

Pol120576(Fam

ilyBDNA

polymerase)

Family

BDNApo

lymerase

Family

DDNA

polymerasee

DNAsynthesis

(Processivity

factors)

120574-com

plex

(clamploader)

RFC(clamploader)

RFC(clamploader)

RFC(clamploader)

120573-clamp(clamp)

PCNA(clamp)

PCNA(clamp)

PCNA(clamp)

Maturation

Maturation(O

kazaki

fragmentp

rocessing)

PolI

(family

ADNApo

lymerase)

Fen1D

na2

Fen1

Fen1

RNaseH

RNaseH

RNaseH

RNaseH

DNAligase

DNAligase

DNAligase

DNAligase

a Exceptio

ntheo

rder

Halobacteria

les

b Not

know

nform

embersof

theE

uryarchaeota

ordersMethanococcalesandMethanopyrales

c GIN

S23hasb

eenfoun

dedon

lyin

theo

rder

Thermococcales

oftheE

uryarchaeota

d Sulfolobu

ssolfataric

usdidshow

prim

asea

ctivity

invitro

e Fam

ilyBDNApo

lymeraseisa

lsoessentialinHalobacteriu

mB

ecause

itsfunctio

nhasn

otbeen

clearlyelu

cidateditmight

also

play

aroleinreplicationin

thisandclo

selyrelated

organism

s

10 Archaea

interact with other unknown initiation enzymes resultingin a complex phylogeny of the MCM homologs [49] Pre-sumably these differences also account for the inability torecognize the origin of replication in these microorganismsThis unique scenario for initiation of DNA replicationmay bea direct consequence of various processes such as duplicationmobile genetic elements and interactions with viruses [58]

The differences in DNA replication among archaealhigher taxa demonstrate an unexpected variability and sug-gest two alternative evolutionary models In the first modelDNA replication evolved late after the diversification ofthe archaeal lineages Because the replicative system wasnot fully formed it was possible to develop differentlybetween the lineages Once formed replication would thenbe highly conserved However this model is not consistentwith differences observed between lineages that must haveformed relatively late such as those between the orders oreven in some cases within certain orders The alternativemodel is that DNA replication has changed throughout theevolution of the archaea Thus differences in the replicativesystems may represent ancient as well as modern adaptationsto changing environments In this case differences in thereplicative systems may provide important insights into theevolutionary pressures in play during different episodes ofarchaeal evolution From this perspective the differencesbetween the eukaryotic and archaeal replicative systems maynot be evidence for an ancient origin of the eukaryotesInstead it is entirely plausible that the replicative system ineukaryotes could have evolved relatively late from a well-developed archaeal system

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] E F DeLong and N R Pace ldquoEnvironmental diversity ofbacteria and archaeardquo Systematic Biology vol 50 no 4 pp 470ndash478 2001

[2] B Chaban S Y M Ng and K F Jarrell ldquoArchaeal habitatsmdashfrom the extreme to the ordinaryrdquo Canadian Journal of Micro-biology vol 52 no 2 pp 73ndash116 2006

[3] M J Hanford and T L Peeples ldquoArchaeal tetraether lipidsunique structures and applicationsrdquo Applied Biochemistry andBiotechnology A vol 97 no 1 pp 45ndash62 2002

[4] K Sandman and J N Reeve ldquoArchaeal histones and the originof the histone foldrdquo Current Opinion in Microbiology vol 9 no5 pp 520ndash525 2006

[5] O Lecompte R Ripp J-C Thierry D Moras and O PochldquoComparative analysis of ribosomal proteins in complete gen-omes an example of reductive evolution at the domain scalerdquoNucleic Acids Research vol 30 no 24 pp 5382ndash5390 2002

[6] D R Edgell and W F Doolittle ldquoArchaea and the origin(s) ofDNA rplication poteinsrdquo Cell vol 89 no 7 pp 995ndash998 1997

[7] E R Barry and S D Bell ldquoDNA replication in the archaeardquoMicrobiology and Molecular Biology Reviews vol 70 no 4 pp876ndash887 2006

[8] S Gribaldo and C Brochier-Armanet ldquoThe origin and evolu-tion of archaea a state of the artrdquo Philosophical Transactions ofthe Royal Society B vol 361 no 1470 pp 1007ndash1022 2006

[9] P Londei ldquoEvolution of translational initiation new insightsfrom the archaeardquo FEMS Microbiology Reviews vol 29 no 2pp 185ndash200 2005

[10] B Grabowski and Z Kelman ldquoArchaeal DNA replicationeukaryal proteins in a bacterial contextrdquo Annual Review ofMicrobiology vol 57 pp 487ndash516 2003

[11] P Forterre J Filee and H Myllykallio ldquoOrigin and evolutionof DNA and DNA replication machineriesrdquo in The GeneticCode and the Origin of Life L Ribas Ed Landes BioscienceGeorgetown Tex USA 2007

[12] E V Koonin ldquoThe origin and early evolution of eukaryotesin the light of phylogenomicsrdquo Genome Biology vol 11 no 5article 209 2010

[13] M Konneke A E Bernhard J R de la Torre C B WalkerJ B Waterbury and D A Stahl ldquoIsolation of an autotrophicammonia-oxidizing marine archaeonrdquo Nature vol 437 no7058 pp 543ndash546 2005

[14] C Brochier-Armanet B Boussau S Gribaldo and P ForterreldquoMesophilic crenarchaeota proposal for a third archaeal phy-lum theThaumarchaeotardquoNature Reviews Microbiology vol 6no 3 pp 245ndash252 2008

[15] J G Elkins M Podar D E Graham et al ldquoA korarchaealgenome reveals insights into the evolution of the ArchaeardquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 105 no 23 pp 8102ndash8107 2008

[16] T Nunoura Y Takaki J Kakuta et al ldquoInsights into theevolution of Archaea and eukaryotic protein modifier systemsrevealed by the genome of a novel archaeal grouprdquoNucleic AcidsResearch vol 39 no 8 pp 3204ndash3223 2011

[17] HHuberM J Hohn R Rachel T Fuchs V CWimmer andKO Stetter ldquoAnewphylumofArchaea represented by a nanosizedhyperthermophilic symbiontrdquoNature vol 417 no 6884 pp 63ndash67 2002

[18] C Brochier S Gribaldo Y Zivanovic F Confalonieri and PForterre ldquoNanoarchaea representatives of a novel archaeal phy-lum or a fast-evolving euryarchaeal lineage related to Therm-ococcalesrdquo Genome Biology vol 6 no 5 article R42 2005

[19] S J Aves ldquoDNA replication initiationrdquo Methods in MolecularBiology vol 521 pp 3ndash17 2009

[20] N P Robinson I Dionne M Lundgren V L Marsh RBernander and S D Bell ldquoIdentification of two origins ofreplication in the single chromosome of the archaeon Sulfolobussolfataricusrdquo Cell vol 116 no 1 pp 25ndash38 2004

[21] M Lundgren A Andersson L Chen P Nilsson and RBernander ldquoThree replication origins in Sulfolobus speciessynchronous initiation of chromosome replication and asyn-chronous terminationrdquo Proceedings of the National Academy ofSciences of theUnited States of America vol 101 no 18 pp 7046ndash7051 2004

[22] N P Robinson and S D Bell ldquoExtrachromosomal element cap-ture and the evolution ofmultiple replication origins in archaealchromosomesrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 104 no 14 pp 5806ndash58112007

[23] E A Pelve A C Lindas A Knoppel A Mira and R Bernan-der ldquoFour chromosome replication origins in the archaeonPyrobaculum calidifontisrdquo Molecular Microbiology vol 85 no5 pp 986ndash995 2012

Archaea 11

[24] A F Andersson E A Pelve S LindebergM Lundgren P Nils-son and R Bernander ldquoReplication-biased genome organisa-tion in the crenarchaeon Sulfolobusrdquo BMCGenomics vol 11 no1 article 454 2010

[25] H Myllykallio P Lopez P Lopez-Garcıa et al ldquoBacterial modeof replication with eukaryotic-like machinery in a hyperther-mophilic archaeonrdquo Science vol 288 no 5474 pp 2212ndash22152000

[26] F Matsunaga P Forterre Y Ishino and H Myllykallio ldquoInvivo interactions of archaeal Cdc6Orc1 and minichromosomemaintenance proteins with the replication originrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 98 no 20 pp 11152ndash11157 2001

[27] S Maisnier-Patin L Malandrin N K Birkeland and RBernander ldquoChromosome replication patterns in the hyper-thermophilic euryarchaeaArchaeoglobus fulgidus andMethano-caldococcus (Methanococcus) jannaschiirdquo Molecular Microbiol-ogy vol 45 no 5 pp 1443ndash1450 2002

[28] R Zhang and C-T Zhang ldquoMultiple replication origins ofthe archaeon Halobacterium species NRC-1rdquo Biochemical andBiophysical Research Communications vol 302 no 4 pp 728ndash734 2003

[29] C Norais M Hawkins A L Hartman J A Eisen H Myl-lykallio and T Allers ldquoGenetic and physical mapping of DNAreplication origins in Haloferax volcaniirdquo PLoS Genetics vol 3no 5 article e77 2007

[30] J A Coker P DasSarma M Capes et al ldquoMultiple replicationorigins of Halobacterium sp strain NRC-1 properties of theconserved orc7-dependent oriC1rdquo Journal of Bacteriology vol191 no 16 pp 5253ndash5261 2009

[31] Z Wu J Liu H Yang H Liu and H Xiang ldquoMultiple repli-cation origins with diverse control mechanisms in Haloarculahispanicardquo Nucleic Acids Research 2013

[32] M Hawkins S Malla M J Blythe C A Nieduszynski and TAllers ldquoAccelerated growth in the absence of DNA replicationoriginsrdquo Nature vol 503 no 7477 pp 544ndash547 2013

[33] A I Majernık and J P J Chong ldquoA conserved mechanismfor replication origin recognition and binding in archaeardquo TheBiochemical Journal vol 409 no 2 pp 511ndash518 2008

[34] J E Galagan C Nusbaum A Roy et al ldquoThe genome of Macetivorans reveals extensive metabolic and physiological diver-sityrdquo Genome Research vol 12 no 4 pp 532ndash542 2002

[35] R Zhang and C-T Zhang ldquoIdentification of replication originsin archaeal genomes based on the Z-curve methodrdquo Archaeavol 1 no 5 pp 335ndash346 2005

[36] A Spang R Hatzenpichler C Brochier-Armanet et al ldquoDis-tinct gene set in two different lineages of ammonia-oxidizingarchaea supports the phylum Thaumarchaeotardquo Trends inMicrobiology vol 18 no 8 pp 331ndash340 2010

[37] K J Marians ldquoProkaryotic DNA replicationrdquo Annual Review ofBiochemistry vol 61 pp 673ndash719 1992

[38] S P Bell ldquoThe origin recognition complex from simple originsto complex functionsrdquo Genes and Development vol 16 no 6pp 659ndash672 2002

[39] V L Marsh and S D Bell ldquoDNA replication and the cell cyclerdquoin Archaea Evolution Physiology and Molecular Biology R AGarrett and H P Klenk Eds Blackwell Publishing HobokenNJ USA 2007

[40] F Matsunaga A Glatigny M-H Mucchielli-Giorgi et alldquoGenomewide and biochemical analyses of DNA-binding activ-ity of Cdc6Orc1 and Mcm proteins in Pyrococcus sprdquo NucleicAcids Research vol 35 no 10 pp 3214ndash3222 2007

[41] J Liu C L Smith D DeRyckere K DeAngelis G S Martinand J M Berger ldquoStructure and function of Cdc6Cdc18implications for origin recognition and checkpoint controlrdquoMolecular Cell vol 6 no 3 pp 637ndash648 2000

[42] M R Singleton R Morales I Grainge N Cook M NIsupov and D B Wigley ldquoConformational changes inducedby nucleotide binding in Cdc6ORC from Aeropyrum pernixrdquoJournal of Molecular Biology vol 343 no 3 pp 547ndash557 2004

[43] Y Ishino and S Ishino ldquoRapid progress of DNA replicationstudies in Archaea the third domain of liferdquo Science China LifeSciences vol 55 no 5 pp 386ndash403 2012

[44] E L Hendrickson R Kaul Y Zhou et al ldquoComplete genomesequence of the genetically tractable hydrogenotrophic meth-anogen Methanococcus maripaludisrdquo Journal of Bacteriologyvol 186 no 20 pp 6956ndash6969 2004

[45] B K Tye ldquoMCM proteins in DNA replicationrdquo Annual Reviewof Biochemistry vol 68 pp 649ndash686 1999

[46] K Labib and J F X Diffley ldquoIs the MCM2-7 complex theeukaryotic DNA replication fork helicaserdquo Current Opinion inGenetics amp Development vol 11 no 1 pp 64ndash70 2001

[47] I Ilves T Petojevic J J Pesavento and M R Botchan ldquoActi-vation of the MCM2-7 helicase by association with Cdc45 andGINS proteinsrdquoMolecular Cell vol 37 no 2 pp 247ndash258 2010

[48] M L Bochman andA Schwacha ldquoTheMcm complex unwind-ing the mechanism of a replicative helicaserdquo Microbiology andMolecular Biology Reviews vol 73 no 4 pp 652ndash683 2009

[49] Y Ishimi ldquoADNAhelicase activity is associated with anMCM4-6 and -7 protein complexrdquoThe Journal of Biological Chemistryvol 272 no 39 pp 24508ndash24513 1997

[50] Z Kelman and M F White ldquoArchaeal DNA replication andrepairrdquo Current Opinion in Microbiology vol 8 no 6 pp 669ndash676 2005

[51] J H LeBowitz and R McMacken ldquoThe Escherichia coli dnaBreplication protein is a DNA helicaserdquoThe Journal of BiologicalChemistry vol 261 no 10 pp 4738ndash4748 1986

[52] Z Kelman J-K Lee and J Hurwitz ldquoThe single minichro-mosome maintenance protein ofMethanobacterium thermoau-totrophicum ΔH contains DNA helicase activityrdquo Proceedings ofthe National Academy of Sciences of the United States of Americavol 96 no 26 pp 14783ndash14788 1999

[53] D F Shechter C Y Ying and J Gautier ldquoThe intrinsic DNAhelicase activity of Methanobacterium thermoautotrophicumΔH minichromosome maintenance proteinrdquo The Journal ofBiological Chemistry vol 275 no 20 pp 15049ndash15059 2000

[54] M de Felice L Esposito B Pucci M de Falco M Rossi andF M Pisani ldquoA CDC6-like factor from the archaea Sulfolobussolfataricus promotes binding of the mini-chromosome main-tenance complex to DNArdquoThe Journal of Biological Chemistryvol 279 no 41 pp 43008ndash43012 2004

[55] R Kasiviswanathan J-H Shin and Z Kelman ldquoInteractionsbetween the archaeal Cdc6 and MCM proteins modulate theirbiochemical propertiesrdquo Nucleic Acids Research vol 33 no 15pp 4940ndash4950 2005

[56] J-H Shin B Grabowski R Kasiviswanathan S D Bell andZ Kelman ldquoRegulation of minichromosomemaintenance heli-case activity by Cdc6rdquo The Journal of Biological Chemistry vol278 no 39 pp 38059ndash38067 2003

[57] M Akita A Adachi K Takemura T Yamagami F Matsunagaand Y Ishino ldquoCdc6Orc1 from Pyrococcus furiosus may actas the origin recognition protein and Mcm helicase recruiterrdquoGenes to Cells vol 15 no 5 pp 537ndash552 2010

12 Archaea

[58] M Krupovic S Gribaldo D H Bamford and P Forterre ldquoTheevolutionary history of archaeal MCM helicases a case study ofvertical evolution combined with hitchhiking of mobile geneticelementsrdquo Molecular Biology and Evolution vol 27 no 12 pp2716ndash2732 2010

[59] ADWalters and J P J Chong ldquoAn archaeal orderwithmultipleminichromosome maintenance genesrdquo Microbiology vol 156part 5 pp 1405ndash1414 2010

[60] A DWalters and J P J Chong ldquoMethanococcusmaripaludis anarchaeon with multiple functional MCM proteinsrdquo Biochemi-cal Society Transactions vol 37 no 1 pp 1ndash6 2009

[61] Q Xia E L Hendrickson Y Zhang et al ldquoQuantitative pro-teomics of the archaeon Methanococcus maripaludis validatedbymicroarray analysis and real time PCRrdquoMolecularampCellularProteomics vol 5 no 5 pp 868ndash881 2006

[62] F Sarmiento J Mrazek and W B Whitman ldquoGenome-scaleanalysis of gene function in the hydrogenotrophic methano-genic archaeon Methanococcus maripaludisrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 110 no 12 pp 4726ndash4731 2013

[63] M Pan T J Santangelo Z Li J N Reeve and Z KelmanldquoThermococcus kodakarensis encodes threeMCMhomologs butonly one is essentialrdquo Nucleic Acids Research vol 39 no 22 pp9671ndash9680 2011

[64] S Ishino S Fujino H Tomita et al ldquoBiochemical and geneticalanalyses of the three mcm genes from the hyperthermophilicarchaeon Thermococcus kodakarensisrdquo Genes to Cells vol 16no 12 pp 1176ndash1189 2011

[65] K S Makarova Y I Wolf S L Mekhedov B G Mirkin and EV Koonin ldquoAncestral paralogs and pseudoparalogs and theirrole in the emergence of the eukaryotic cellrdquo Nucleic AcidsResearch vol 33 no 14 pp 4626ndash4638 2005

[66] N Marinsek E R Barry K S Makarova I Dionne E VKoonin and S D Bell ldquoGINS a central nexus in the archaealDNA replication forkrdquo EMBOReports vol 7 no 5 pp 539ndash5452006

[67] T Yoshimochi R Fujikane M Kawanami F Matsunaga and YIshino ldquoTheGINS complex from Pyrococcus furiosus stimulatesthe MCM helicase activityrdquoThe Journal of Biological Chemistryvol 283 no 3 pp 1601ndash1609 2008

[68] T Oyama S Ishino S Fujino et al ldquoArchitectures of archaealGINS complexes essential DNA replication initiation factorsrdquoBMC Biology vol 9 article 28 2011

[69] H Ogino S Ishino K Mayanagi et al ldquoThe GINS com-plex from the thermophilic archaeon Thermoplasma aci-dophilummay function as a homotetramer inDNA replicationrdquoExtremophiles vol 15 no 4 pp 529ndash539 2011

[70] L Sanchez-Pulido and C P Ponting ldquoCdc45 the missing recjortholog in eukaryotesrdquoBioinformatics vol 27 no 14 pp 1885ndash1888 2011

[71] Z Li T J Santangelo L Cubonova J N Reeve and Z KelmanldquoAffinity purification of an archaeal DNA replication proteinnetworkrdquomBio vol 1 no 5 2010

[72] Z Li M Pan T J Santangelo et al ldquoA novel DNA nucleaseis stimulated by association with the GINS complexrdquo NucleicAcids Research vol 39 no 14 pp 6114ndash6123 2011

[73] L A Rajman and S T Lovett ldquoA thermostable single-strandDNase from Methanococcus jannaschii related to the RecJrecombination and repair exonuclease from Escherichia colirdquoJournal of Bacteriology vol 182 no 3 pp 607ndash612 2000

[74] K RWilliams J B Murphy and JW Chase ldquoCharacterizationof the structural and functional defect in the Escherichia colisingle-stranded DNA binding protein encoded by the ssb-1 mutant gene Expression of the ssb-1 gene under 120582p(L)regulationrdquoThe Journal of Biological Chemistry vol 259 no 19pp 11804ndash11811 1984

[75] S Dąbrowski M Olszewski R Pitek and J Kur ldquoNovel ther-mostable ssDNA-binding proteins fromThermus thermophilusand T aquaticus-expression and purificationrdquo Protein Expres-sion and Purification vol 26 no 1 pp 131ndash138 2002

[76] C Iftode Y Daniely and J A Borowiec ldquoReplication proteinA (RPA) the eukaryotic SSBrdquo Critical Reviews in Biochemistryand Molecular Biology vol 34 no 3 pp 141ndash180 1999

[77] A G Murzin ldquoOB(oligonucleotideoligosaccharide binding)-fold common structural and functional solution for non-hom-ologous sequencesrdquo The EMBO Journal vol 12 no 3 pp 861ndash867 1993

[78] C A Haseltine and S C Kowalczykowski ldquoA distinctive single-stranded DNA-binding protein from the Archaeon Sulfolobussolfataricusrdquo Molecular Microbiology vol 43 no 6 pp 1505ndash1515 2002

[79] R I M Wadsworth and M F White ldquoIdentification and pro-perties of the crenarchaeal single-stranded DNA binding pro-tein from Sulfolobus solfataricusrdquoNucleic Acids Research vol 29no 4 pp 914ndash920 2001

[80] I D Kerr R I M Wadsworth L Cubeddu W Blankenfeldt JHNaismith andM FWhite ldquoInsights into ssDNA recognitionby the OB fold from a structural and thermodynamic study ofSulfolobus SSB proteinrdquo The EMBO Journal vol 22 no 11 pp2561ndash2570 2003

[81] X Luo U Schwarz-Linek C H Botting R Hensel B Siebersand M F White ldquoCC1 a novel crenarchaeal DNA binding pro-teinrdquo Journal of Bacteriology vol 189 no 2 pp 403ndash409 2007

[82] T J Kelly P Simancek and G S Brush ldquoIdentification andcharacterization of a single-stranded DNA-binding proteinfrom the archaeonMethanococcus jannaschiirdquoProceedings of theNational Academy of Sciences of theUnited States of America vol95 no 25 pp 14634ndash14639 1998

[83] Z Kelman S Pietrokovski and J Hurwitz ldquoIsolation and cha-racterization of a split B-type DNA polymerase from the arch-aeonMethanobacterium thermoautotrophicumΔHrdquoTheJournalof Biological Chemistry vol 274 no 40 pp 28751ndash28761 1999

[84] K Komori and Y Ishino ldquoReplication protein A in Pyrococcusfuriosus is involved in homologous DNA recombinationrdquo TheJournal of Biological Chemistry vol 276 no 28 pp 25654ndash25660 2001

[85] J B Robbins M C Murphy B A White R I Mackie THa and I K O Cann ldquoFunctional analysis of multiple single-stranded DNA-binding proteins from Methanosarcina acetivo-rans and their effects on DNA synthesis by DNA polymeraseBIrdquoThe Journal of Biological Chemistry vol 279 no 8 pp 6315ndash6326 2004

[86] Y Lin L-J Lin P Sriratana et al ldquoEngineering of functionalreplication protein a homologs based on insights into the evolu-tion of oligonucleotideoligosaccharide-binding foldsrdquo Journalof Bacteriology vol 190 no 17 pp 5766ndash5780 2008

[87] D N Frick and C C Richardson ldquoDNA primasesrdquo AnnualReview of Biochemistry vol 70 pp 39ndash80 2001

[88] G Desogus S Onesti P Brick M Rossi and F M PisanildquoIdentification and characterization of a DNA primase fromthe hyperthermophilic archaeon Methanococcus jannaschiirdquoNucleic Acids Research vol 27 no 22 pp 4444ndash4450 1999

Archaea 13

[89] A A Bocquier L Liu I K O Cann K Komori D Kohda andY Ishino ldquoArchaeal primase bridging the gap between RNAand DNA polymerasesrdquo Current Biology vol 11 no 6 pp 452ndash456 2001

[90] L Liu K Komori S Ishino et al ldquoThe archaeal DNA primasebiochemical characterization of the p41-p46 complex fromPyrococcus furiosusrdquo The Journal of Biological Chemistry vol276 no 48 pp 45484ndash45490 2001

[91] E Matsui M Nishio H Yokoyama K Harata S Darnisand I Matsui ldquoDistinct domain functions regulating de novoDNA synthesis of thermostable DNA primase from hyperther-mophile Pyrococcus horikoshiirdquo Biochemistry vol 42 no 50 pp14968ndash14976 2003

[92] N Ito I Matsui and EMatsui ldquoMolecular basis for the subunitassembly of the primase from an archaeon Pyrococcus hori-koshiirdquoThe FEBS Journal vol 274 no 5 pp 1340ndash1351 2007

[93] M le Breton G Henneke C Norais et al ldquoThe heterodimericprimase from the euryarchaeon Pyrococcus abyssi a multifunc-tional enzyme for initiation and repairrdquo Journal of MolecularBiology vol 374 no 5 pp 1172ndash1185 2007

[94] S-H Lao-Sirieix and S D Bell ldquoThe heterodimeric primaseof the hyperthermophilic archaeon Sulfolobus solfataricus pos-sesses DNA and RNA primase polymerase and 31015840-terminalnucleotidyl transferase activitiesrdquo Journal of Molecular Biologyvol 344 no 5 pp 1251ndash1263 2004

[95] S-H Lao-Sirieix L Pellegrini and S D Bell ldquoThe promiscuousprimaserdquo Trends in Genetics vol 21 no 10 pp 568ndash572 2005

[96] J Hu L Guo K Wu B Liu S Lang and L Huang ldquoTemplate-dependent polymerization across discontinuous templatesby the heterodimeric primase from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquoNucleic Acids Research vol 40no 8 pp 3470ndash3483 2012

[97] E Evguenieva-Hackenberg P Walter E Hochleitner FLottspeich and G Klug ldquoAn exosome-like complex in Sulfolo-bus solfataricusrdquo EMBOReports vol 4 no 9 pp 889ndash893 2003

[98] P Walter F Klein E Lorentzen A Ilchmann G Klug andE Evguenieva-Hackenberg ldquoCharacterization of native andreconstituted exosome complexes from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Microbiology vol62 no 4 pp 1076ndash1089 2006

[99] Z Zuo C J Rodgers A L Mikheikin and M A Trak-selis ldquoCharacterization of a functional DnaG-type primase inarchaea implications for a dual-primase systemrdquo Journal ofMolecular Biology vol 397 no 3 pp 664ndash676 2010

[100] B R Berquist P DasSarma and S DasSarma ldquoEssential andnon-essential DNA replication genes in the model halophilicArchaeon Halobacterium sp NRC-1rdquo BMC Genetics vol 8article 31 2007

[101] D K Braithwaite and J Ito ldquoCompilation alignment andphylogenetic relationships of DNA polymerasesrdquo Nucleic AcidsResearch vol 21 no 4 pp 787ndash802 1993

[102] I K O Cann and Y Ishino ldquoArchaeal DNA replication iden-tifying the pieces to solve a puzzlerdquo Genetics vol 152 no 4 pp1249ndash1267 1999

[103] G Lipps S Rother C Hart and G Krauss ldquoA novel typeof replicative enzyme harbouring ATpase primase and DNApolymerase activityrdquo The EMBO Journal vol 22 no 10 pp2516ndash2525 2003

[104] J Yamtich and J B Sweasy ldquoDNA polymerase family X func-tion structure and cellular rolesrdquoBiochimica et BiophysicaActavol 1804 no 5 pp 1136ndash1150 2010

[105] H Ohmori E C Friedberg R P P Fuchs et al ldquoThe Y-familyof DNA polymerasesrdquoMolecular Cell vol 8 no 1 pp 7ndash8 2001

[106] N Y Yao R E Georgescu J Finkelstein and M E OrsquoDonnellldquoSingle-molecule analysis reveals that the lagging strandincreases replisome processivity but slows replication forkprogressionrdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 106 no 32 pp 13236ndash132412009

[107] U Hubscher G Maga and S Spadari ldquoEukaryotic DNA poly-merasesrdquo Annual Review of Biochemistry vol 71 pp 133ndash1632002

[108] F Boudsocq S Iwai F Hanaoka and R Woodgate ldquoSulfolobussolfataricus P2 DNA polymerase IV (Dp04) an archaeal DinB-like DNA polymerase with lesion-bypass properties akin toeukaryotic pol120578rdquo Nucleic Acids Research vol 29 no 22 pp4607ndash4616 2001

[109] L-J Lin A Yoshinaga Y Lin et al ldquoMolecular analyses ofan unusual translesion DNA polymerase fromMethanosarcinaacetivorans C2Ardquo Journal of Molecular Biology vol 397 no 1pp 13ndash30 2010

[110] I K O Cann S Ishino NNomura Y Sako andY Ishino ldquoTwofamily B DNA polymerases from Aeropyrum pernix an aerobichyperthermophilic crenarchaeoterdquo Journal of Bacteriology vol181 no 19 pp 5984ndash5992 1999

[111] T Uemori Y Ishino H Doi and I Kato ldquoThe hyperther-mophilic archaeon Pyrodictium occultum has two 120572-like DNApolymerasesrdquo Journal of Bacteriology vol 177 no 8 pp 2164ndash2177 1995

[112] T Uemori Y Ishino H Toh K Asada and I Kato ldquoOrgani-zation and nucleotide sequence of the DNA polymerase genefrom the archaeon Pyrococcus furiosusrdquo Nucleic Acids Researchvol 21 no 2 pp 259ndash265 1993

[113] B A Connolly ldquoRecognition of deaminated bases by archaealfamily-B DNA polymerasesrdquo Biochemical Society Transactionsvol 37 no 1 pp 65ndash68 2009

[114] B A Connolly M J Fogg G Shuttleworth and B T WilsonldquoUracil recognition by archaeal family B DNA polymerasesrdquoBiochemical Society Transactions vol 31 no 3 pp 699ndash7022003

[115] T T Richardson X Wu B J Keith P Heslop A C Jones andB A Connolly ldquoUnwinding of primer-templates by archaealfamily-B DNA polymerases in response to template-stranduracilrdquo Nucleic Acids Research vol 41 no 4 pp 2466ndash24782013

[116] T Lindahl ldquoInstability and decay of the primary structure ofDNArdquo Nature vol 362 no 6422 pp 709ndash715 1993

[117] I B Rogozin K S Makarova Y I Pavlov and E V Koonin ldquoAhighly conserved family of inactivated archaeal B family DNApolymerasesrdquo Biology Direct vol 3 article 32 2008

[118] M Imamura T Uemori I Kato and Y Ishino ldquoA non-120572-like DNA polymerase from the hyperthermophilic archaeonPyrococcus furiosusrdquoBiological andPharmaceutical Bulletin vol18 no 12 pp 1647ndash1652 1995

[119] I K O Cann K Komori H Toh S Kanai and Y IshinoldquoA heterodimeric DNA polymerase evidence that members ofEuryarchaeota possess a distinct DNA polymeraserdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 95 no 24 pp 14250ndash14255 1998

[120] L Aravind D D Leipe and E V Koonin ldquoToprimmdasha con-served catalytic domain in type IA and II topoisomerases

14 Archaea

DnaG-type primases OLD family nucleases and RecR pro-teinsrdquo Nucleic Acids Research vol 26 no 18 pp 4205ndash42131998

[121] M Jokela A Eskelinen H Pospiech J Rouvinen and J ESyvaoja ldquoCharacterization of the 31015840 exonuclease subunit DP1of Methanococcus jannaschii replicative DNA polymerase DrdquoNucleic Acids Research vol 32 no 8 pp 2430ndash2440 2004

[122] T Uemori Y Sato I Kato H Doi and Y Ishino ldquoA novel DNApolymerase in the hyperthermophilic archaeon Pyrococcus fur-iosus gene cloning expression and characterizationrdquo Genes toCells vol 2 no 8 pp 499ndash512 1997

[123] Y Shen K Musti M Hiramoto H Kikuchi Y Kawarabayashiand I Matsui ldquoInvariant Asp-1122 and Asp-1124 are essentialresidues for polymerization catalysis of family D DNA poly-merase from Pyrococcus horikoshiirdquo The Journal of BiologicalChemistry vol 276 no 29 pp 27376ndash27383 2001

[124] G Henneke D Flament U Hubscher J Querellou and J-P Raffin ldquoThe hyperthermophilic euryarchaeota Pyrococcusabyssi likely requires the two DNA polymerases D and B forDNA replicationrdquo Journal of Molecular Biology vol 350 no 1pp 53ndash64 2005

[125] L Cubonova T Richardson B W Burkhart et al ldquoArchaealDNA polymerase D but not DNA polymerase B is required forgenome replication in Thermococcus kodakarensisrdquo Journal ofBacteriology vol 195 no 10 pp 2322ndash2328 2013

[126] C Rouillon G Henneke D Flament J Querellou and J-PRaffin ldquoDNA polymerase switching on homotrimeric PCNA atthe replication fork of the euryarchaea Pyrococcus abyssirdquo Jour-nal of Molecular Biology vol 369 no 2 pp 343ndash355 2007

[127] G Henneke ldquoIn vitro reconstitution of RNA primer removal inArchaea reveals the existence of two pathwaysrdquoTheBiochemicalJournal vol 447 no 2 pp 271ndash280 2012

[128] G-LMoldovan B Pfander and S Jentsch ldquoPCNA themaestroof the replication forkrdquo Cell vol 129 no 4 pp 665ndash679 2007

[129] X-P Kong R Onrust M OrsquoDonnell and J Kuriyan ldquoThree-dimensional structure of the 120573 subunit of E coli DNA poly-merase III holoenzyme a sliding DNA clamprdquo Cell vol 69 no3 pp 425ndash437 1992

[130] K Daimon Y Kawarabayasi H Kikuchi Y Sako and Y IshinoldquoThree proliferating cell nuclear antigen-like proteins foundin the hyperthermophilic archaeon Aeropyrum pemix interac-tions with the two DNA polymerasesrdquo Journal of Bacteriologyvol 184 no 3 pp 687ndash694 2002

[131] I Dionne R K Nookala S P Jackson A J Doherty andS D Bell ldquoA heterotrimeric PCNA in the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Cell vol 11 no 1pp 275ndash282 2003

[132] E Warbrick ldquoPCNA binding through a conserved motifrdquoBioEssays vol 20 no 3 pp 195ndash199 1998

[133] H Nishida K Mayanagi S Kiyonari et al ldquoStructural deter-minant for switching between the polymerase and exonucleasemodes in the PCNA-replicative DNA polymerase complexrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 106 no 49 pp 20693ndash20698 2009

[134] K Mayanagi S Kiyonari H Nishida et al ldquoArchitecture of theDNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complexrdquo Proceedings of the National Academy ofSciences of the United States of America vol 108 no 5 pp 1845ndash1849 2011

[135] B Castrec C Rouillon G Henneke D Flament J Querellouand J-P Raffin ldquoBinding to PCNA in Euryarchaeal DNA

replication requires two PIP motifs for DNA polymerase D andone PIP motif for DNA polymerase Brdquo Journal of MolecularBiology vol 394 no 2 pp 209ndash218 2009

[136] P F Pluchon T Fouqueau C Creze et al ldquoAn extendednetworkof genomic maintenance in the archaeon Pyrococcus abyssihighlights unexpected associations between eucaryotic homo-logsrdquo PLoS One vol 8 no 11 Article ID e79707 2013

[137] J E Ladner M Pan J Hurwitz and Z Kelman ldquoCrystalstructures of two active proliferating cell nuclear antigens(PCNAs) encoded byThermococcus kodakaraensisrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2711ndash2716 2011

[138] Y Kuba S Ishino T Yamagami et al ldquoComparative analyses ofthe two proliferating cell nuclear antigens from the hyperther-mophilic archaeonThermococcus kodakarensisrdquo Genes to Cellsvol 17 no 11 pp 923ndash937 2012

[139] T Fukui H Atomi T Kanai R Matsumi S Fujiwara andT Imanaka ldquoComplete genome sequence of the hyperther-mophilic archaeon Thermococcus kodakaraensis KOD1 andcomparison with Pyrococcus genomesrdquo Genome Research vol15 no 3 pp 352ndash363 2005

[140] D Jeruzalmi O Yurieva Y Zhao et al ldquoMechanism of proces-sivity clamp opening by the delta subunit wrench of the clamploader complex of E coliDNApolymerase IIIrdquoCell vol 106 no4 pp 417ndash428 2001

[141] Y Shiomi J Usukura Y Masamura et al ldquoATP-dependentstructural change of the eukaryotic clamp-loader protein repli-cation factor Crdquo Proceedings of the National Academy of Sciencesof the United States of America vol 97 no 26 pp 14127ndash141322000

[142] T Miyata T Oyama K Mayanagi S Ishino Y Ishino and KMorikawa ldquoThe clamp-loading complex for processive DNAreplicationrdquoNature Structural andMolecular Biology vol 11 no7 pp 632ndash636 2004

[143] T Oyama Y Ishino I K O Cann S Ishino and K MorikawaldquoAtomic structure of the clamp loader small subunit fromPyrococcus furiosusrdquo Molecular Cell vol 8 no 2 pp 455ndash4632001

[144] A Seybert D J Scott S Scaife M R Singleton and DB Wigley ldquoBiochemical characterisation of the clampclamploader proteins from the euryarchaeon Archaeoglobus fulgidusrdquoNucleic Acids Research vol 30 no 20 pp 4329ndash4338 2002

[145] Y-H Chen Y Lin A Yoshinaga et al ldquoMolecular analyses of athree-subunit euryarchaeal clamp loader complex from Meth-anosarcina acetivoransrdquo Journal of Bacteriology vol 191 no 21pp 6539ndash6549 2009

[146] Y-H Chen S A Kocherginskaya Y Lin et al ldquoBiochemicaland mutational analyses of a unique clamp loader complex inthe archaeon Methanosarcina acetivoransrdquo The Journal of Bio-logical Chemistry vol 280 no 51 pp 41852ndash41863 2005

[147] F Matsunaga C Norais P Forterre and H Myllykallio ldquoIden-tification of short ldquoeukaryoticrdquo Okazaki fragments synthesizedfrom a prokaryotic replication originrdquo EMBO Reports vol 4no 2 pp 154ndash158 2003

[148] H Kochiwa M Tomita and A Kanai ldquoEvolution of ribonucle-ase H genes in prokaryotes to avoid inheritance of redundantgenesrdquo BMC Evolutionary Biology vol 7 article 128 2007

[149] N OhtaniMHarukiMMorikawa and S Kanaya ldquoMoleculardiversities of RNases Hrdquo Journal of Bioscience and Bioengineer-ing vol 88 no 1 pp 12ndash19 1999

Archaea 15

[150] N Ohtani M Haruki M Morikawa R J Crouch M Itayaand S Kanaya ldquoIdentification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII fromBacillus subtilis classification of RNases H into three familiesrdquoBiochemistry vol 38 no 2 pp 605ndash618 1999

[151] N Ohtani H Yanagawa M Tomita and M Itaya ldquoIdentifi-cation of the first archaeal type 1 RNase H gene from Halobac-terium sp NRC-1 archaeal RNase HI can cleave an RNA-DNAjunctionrdquoThe Biochemical Journal vol 381 no 3 pp 795ndash8022004

[152] N Ohtani H Yanagawa M Tomita and M Itaya ldquoCleavage ofdouble-stranded RNA by RNase HI from a thermoacidophilicarchaeon Sulfolobus tokodaii 7rdquo Nucleic Acids Research vol 32no 19 pp 5809ndash5819 2004

[153] M A Nowak M C Boerlijst J Cooke and J M SmithldquoEvolution of genetic redundancyrdquo Nature vol 388 no 6638pp 167ndash170 1997

[154] A E Tomkinson S Vijayakumar J M Pascal and T Ellen-berger ldquoDNA ligases structure reactionmechanism and func-tionrdquo Chemical Reviews vol 106 no 2 pp 687ndash699 2006

[155] M Nakatani S Ezaki H Atomi and T Imanaka ldquoA DNAligase from a hyperthermophilic archaeon with unique cofactorspecificityrdquo Journal of Bacteriology vol 182 no 22 pp 6424ndash6433 2000

[156] Y Sun M S Seo J H Kim et al ldquoNovel DNA ligase with broadnucleotide cofactor specificity from the hyperthermophilic cre-narchaeon Sulfophobococcus zilligii influence of ancestral DNAligase on cofactor utilizationrdquo Environmental Microbiology vol10 no 12 pp 3212ndash3224 2008

[157] T R Beattie and S D Bell ldquoCoordination of multiple enzymeactivities by a single PCNA in archaeal Okazaki fragmentmaturationrdquo The EMBO Journal vol 31 no 6 pp 1556ndash15672012

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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International Journal of

Volume 2014

Zoology

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Molecular Biology International

GenomicsInternational Journal of

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The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Marine BiologyJournal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

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Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Archaea 7

together at the replication fork synthesizing the leading andlagging strand respectively [100 124] However in otherEuryarchaeota PolB does not appear to be essential Forinstance a recent report demonstrated that both subunits ofPolDwere essential but PolB was nonessential for the growthof M maripaludis S2 [62] Likewise in T kodakaraensisPolD can be coisolated with different proteins of the archaealreplication fork but PolB wasmainly coisolated with proteinsof unknown function [71] A deletion of the PolB in Tkodakaraensis also had no detectable effect on cell viability[125] Interestingly T kodakaraensis PolB mutants haveincreased sensitivity to UV radiation These results togethersuggest that PolD is the essential replicative DNA polymerasein these euryarchaeotes and not a PolB family polymeraseIn this scenario PolB may have some other crucial functionin Halobacterium and possibly other closely related specieswhich it is not conserved throughout the phylum Finallyit has been demonstrated that purified PolD from P abyssiis able to perform strand displacement and RNA primerextension in vitro Purified PolB on its own cannot performthese activities in vitro but in the presence of PCNA stranddisplacement activity is stimulated [124 126] A recent in vitrostudy in P abyssi demonstrated that RNase HII is required toinitiate strand displacement DNA synthesis by PolB [127]

34 Elongation (Other Accessory Proteins) Purified DNApolymerases possess low processivity however the addi-tion of an accessory factor the sliding clamp gives DNApolymerases the required processivity to replicate genomesThis factor whose structure resembles a doughnut functionsas a molecular platform which recruits several replication-associated enzymes and act together with DNA and thepolymerase to stabilize their interactions during replication[128] The structure of sliding clamps is conserved in thethree domains of life In Bacteria the sliding clamp or 120573-subunit is a homodimeric ring [129] In eukaryotes thesliding clamp or proliferating cell nuclear antigen (PCNA)is a homotrimeric ring [128] In Archaea the majority ofcrenarchaeotes have multiple PCNA homologs which formheterotrimeric rings [130 131] (Figure 1) In contrast mosteuryarchaeotes possess a single PCNA homolog (Figure 1)Interactions of DNA polymerase with the sliding clampare mediated through a common motif called the PCNAInteracting Protein (PIP) box [132] The three dimensionalstructures of PCNA-PolB and the PolB-PCNA-DNA complexfrom P furiosus have been solved shedding light on theinteractions between these molecules [133 134] In additiona study demonstrated that the PolDPCNA and PolBPCNAinteractions require two and one PIP boxes respectively[135] Recently through a protein-interaction network of Pabyssi a previously unknown protein with nuclease activity(Pab0431) and a PIP canonical motif was discovered tointeract with PCNA suggesting a possible involvement inDNA replication [136] T kodakaraensis is the only well-documented example of an euryarchaeotewith twohomologsfor PCNA TK0535 (PCNA1) and TK0582 (PCNA2) Recentwork demonstrated both proteins form stable homotrimericrings that interact with T kodakaraensis PolB in vitro [137]A more detailed study of the two homologs of PCNA in T

kodakaraensis demonstrated that both homologs stimulate invitro the primer extension activity of PolB but only PCNA1and not PCNA2 stimulates the same activity of PolD [138]Also the same report showed that the pcna2 gene can bedisrupted without causing growth deficiencies but it was notpossible to isolate mutants of pcna1 These results suggestthat PCNA1 but not PCNA2 is essential for DNA replication[138] It has been proposed that one of the PCNA geneswas acquired by lateral gene transfer [139] Members of theorderMethanococcales possess one PCNA homolog with twoexceptionsMmaripaludis S2 possesses twoPCNAhomologs(MMP1126 and 1711) [60] Both genes appeared to be essentialfor growth suggesting that they both play an importantrole in replication [62] The gene MMP1711 possesses highsimilarity to both T kodakaraensis genes and is likely thetrue methanococcal PCNA In contrast MMP1126 possessesonly low similarity to the T kodakaraensis genes and alsocontains an S-adenosylmethionine-dependent methyltrans-ferases domain Thus it is likely to possess some alternativefunction Methanotorris igneus Kol 5 also possesses twoPCNA homologs

For PCNA to assemble around DNA a specific loadingfactor is required In Bacteria the loading factor is knownas 120574-complex and comprises three different subunits ina 1205743-120575-1205751015840 stoichiometry [140] In eukaryotes the loading

factor is known as Replication Factor C (RFC) and is aheteropentameric complex comprising one large subunit andfour different small subunits [141] In contrast inArchaea theRFC consists of two different proteins a small subunit RFCSand a large subunit RFCLThey also form a heteropentamericcomplex in a 4 1 ratio (RFCS RFCL) Interestingly manycrenarchaeotes possess one homolog of RFCL and two orthree homologs of RFCS Alternatively most euryarchaeotespossess only one RFCL and RFCS homolog The exceptionsare somemembers of the ordersHalobacteriales Methanomi-crobiales and Methanosarcinales which possess two RFCShomologs (Figure 1) Structural and biochemical studies ofRFC have been conducted in several euryarchaeotes such asArchaeoglobus fulgidus and Pyrococcus species [142ndash144] Aninteresting case is observed in Methanosarcina acetivoransThis RFC possesses three subunits (RFC1 2 L) found ina ratio 3 1 1 [145] Homologs for these three subunits arealso present in most of the genomes of the haloarchaea[145] It is inferred that this type of RFC complex representsan intermediary form transitional between the canonicalarchaeal RFC complex of one small and one large subunit andthe eukaryotic RFC complex of four different small and onelarge subunit [146] The organization and spatial distributionexhibit a similarity to the E coliminimal 120574-complex but thefunction of the subunits is probably not conserved [145]

35 Maturation During DNA replication the lagging strandis discontinuously synthesized by extending the RNAprimersor Okazaki fragments This discontinuously synthesizedDNA strand requires maturation to form a single covalentlyclosed strand to end the replication process In ArchaeaOkazaki fragments were first demonstrated during replica-tion in P abyssi and Sulfolobus acidocaldarius [147] Duringreplication these RNA primers are replaced with DNA The

8 Archaea

removal of the primers is performed by the enzyme RNase Hwhich is ubiquitous in the three domains of life Accordingto their sequence similarity in prokaryotes the RNase Hproteins are classified into three groups RNase HI HII andHIII In eukaryotes they are classified as RNase H1 and H2[148] However phylogenetic analyses suggest that the RNaseH proteins can also be classified into two different groupsType 1 (prokaryotic RNaseHI eukaryotic RNaseH1 and viralRNase H) and Type 2 (prokaryotic RNase HII and HIII andeukaryotic RNase H2) [149] These two types of RNase Hpossess different specific activities metal ion preferences andcleavage sites [150] Originally it was thought that Archaeaonly possess type 2 RNase H [149] but several type 1 archaealRNase H enzymes have since then been discovered [151 152]Interestingly in eukaryotes RNaseH1 andH2 tend to coexistand different combinations of the three prokaryotic RNasesH(I II and III) are found except for the combination of RNasesHI and HIII This mutually exclusive evolution of some ofthe prokaryotic RNases seems to be related to functionalredundancy [148]

Another enzyme involved in primer replacement inDNA replication is the Flap endonuclease I (FEN-1) whichrecognizes double-strandedDNAwith an unannealed 51015840-flapand cleaves it A eukaryotic homolog of FEN-1 is found inevery archaeal member analyzed and one member of theThermoproteales Thermofilum pendens Hrk5 possesses twohomologs

M maripaludis S2 possesses genes for the prokaryoticRNase HI and HII and for FEN-1 but none are essentialsuggesting that they may be redundant in their functions[44 62] Possibly both RNase H proteins persist and areevolutionary stable in the genome The gene products mayperform the same function but one is less efficient than theother [153]

After the Okazaki fragments are replaced by DNA inthe lagging strand the nick between the newly synthesizedand the elongated DNA is repaired by a DNA ligase Thisenzyme uses a nucleotide cofactor to catalyze the formationof the phosphodiester bond in three well-characterized steps[154]The enzyme is common to all three domains but can begrouped into two families based on cofactor specificity (ATPor NAD+) The DNA ligases from several crenarchaeotes andeuryarchaeotes have been further characterized (reviewedin [43]) Many archaeal DNA ligases possess dual cofactorspecificity (ATPNAD+ or ATPADP) but every archaealDNA ligase characterized so far uses ATP A thermophilicDNA ligase from M thermautotrophicus which uses ATP assole cofactor was characterized in vitro [155] A characterizedDNA ligase from the crenarchaeote Sulfophobococcus zilligiidisplayed specificity for three cofactors (ATPNAD+GTP)[156]Major structuralwork in this enzymehas been achievedin P furiosus and S solfataricus and the findings have beenreviewed in detail [43] InM maripaludis S2 the DNA ligaseis likely to be essential for growth [44 62]

Understanding the maturation process in archaea hasbecome a focus of increasing research in recent years An invitro study reconstituted the Okazaki fragment maturationusing proteins derived from the crenarchaeote S solfataricusThey demonstrated that only six proteins are necessary for

coupled DNA synthesis RNA primer removal and DNAligation In this model a single PCNA (heterotrimeric ring)coordinates the activities of PolBI FEN-1 and DNA ligaseinto an efficient maturation complex [157] A different invitro study in P abyssi has demonstrated two different modelsfor Okazaki fragments maturation which differ in the RNAprimer removal process In the first model RNA primerelimination is executed by continuous PolD strand displace-ment DNA synthesis and 51015840RNA flap cleavage by FEN-1The resulting nicks are closed by DNA ligase Alternativelythe second model proposes that RNase HII cleaves theRNA primer followed by the action of FEN-1 and stranddisplacement DNA synthesis by polB or polD The nick isthen sealed by DNA ligase [127] Testing these models invivo is of great interest to complete the picture of how theseprocesses behave in the cell In addition other factors that canmodulate these processesmay be required for coordination ofthe in vivomaturation process

4 Conclusions

DNA replication in archaea possesses a dual nature wherethe machinery is structurally and functionally similar to theeukaryotic replication system but it is executed within abacterial context [11 25] Additionally unique archaeal fea-tures demonstrate the complexity of this process and it doesnot appear to be just a simplified version of the eukary-otic system For example the archaeal specific DNA poly-merase D is conserved across the Archaea domain with theexception of the Crenarchaeota phylumThe recent discoverythat it is the essential replicative polymerase in two differenteuryarchaeotic species demonstrates an unanticipated vari-ability in archaeal DNA replication and a fundamental differ-ence in the replication mechanism between crenarchaeotesand euryarchaeotes Interestingly the absence of PolD increnarchaeotes is not the only difference in DNA repli-cation These differences include the absence of histonesin crenarchaeotes [4] the presence of multiple origins ofreplication in crenarchaeotes and a single origin of repli-cation in most euryarchaeotes the absence of GINS23 inmost euryarchaeotes the absence of RPA protein in manycrenarchaeotes the presence of multiple MCM homologs inMethanococcales and the presence of one homolog of PCNAin euryarchaeotes compared to the multiple homologs increnarchaeotes These distinctive characteristics between thephyla highlight the complexity of archaeal DNA replicationand suggest a complex evolutionary history (Table 1)

Among the Euryarchaeota the ordersHalobacteriales andMethanococcales possess differences in the DNA replicationsystem that make them unique For instance Halobac-teriales possess many more origin recognition proteins(Orc1Cdc6) compared to the rest of the archaea On theother hand Methanococcales and Methanopyrales lack rec-ognizable homologs for the Orc1Cdc6 proteins suggestingthe presence of a very different mechanism for initiation ofreplication In addition the Methanococcales possess a largenumber of MCM protein homologs It has been proposedthat these distinctive features are connected and because ofthe absence of the Orc1Cdc6 proteins MCM proteins may

Archaea 9

Table1DNAreplicationproteins

andfeatures

inthed

omains

BacteriaEukaryotaand

thetwomajor

phylao

fthe

Archaeado

main

Mod

ified

from

[43]

DNAreplicationstage

Process

Bacteria

Eukaryota

Archaea

Crenarchaeota

Euryarchaeota

Preinitia

tion

Orig

inof

replication

Sing

leMultip

leMultip

leSing

lea

Orig

inrecogn

ition

DnaA

ORC

complex

(ORC

1-6)

Orc1C

dc6

Orc1C

dc6b

Initiation

DNAun

winding

(Helicase)

DnaB

MCM

complex

(MCM

2-7)

MCM

complex

MCM

complex

DNAun

winding

(Accessory

proteins)

DnaC

Cdc6

GIN

S23GIN

S15

GIN

S15c

Cdt1

GIN

Scomplex

(Sld5Psf1-3)

RecJho

molog

RecJho

molog

Cdc45

Prim

ersynthesis

DnaG

Pol120572

prim

asec

omplex

DNAprim

ase

(PriS

L)D

naG

dDNAprim

ase(PriSL)

Elon

gatio

n

DNAsynthesis

(polym

erase)

PolIII(Fam

ilyCDNApo

lymerase)

Pol120575and

Pol120576(Fam

ilyBDNA

polymerase)

Family

BDNApo

lymerase

Family

DDNA

polymerasee

DNAsynthesis

(Processivity

factors)

120574-com

plex

(clamploader)

RFC(clamploader)

RFC(clamploader)

RFC(clamploader)

120573-clamp(clamp)

PCNA(clamp)

PCNA(clamp)

PCNA(clamp)

Maturation

Maturation(O

kazaki

fragmentp

rocessing)

PolI

(family

ADNApo

lymerase)

Fen1D

na2

Fen1

Fen1

RNaseH

RNaseH

RNaseH

RNaseH

DNAligase

DNAligase

DNAligase

DNAligase

a Exceptio

ntheo

rder

Halobacteria

les

b Not

know

nform

embersof

theE

uryarchaeota

ordersMethanococcalesandMethanopyrales

c GIN

S23hasb

eenfoun

dedon

lyin

theo

rder

Thermococcales

oftheE

uryarchaeota

d Sulfolobu

ssolfataric

usdidshow

prim

asea

ctivity

invitro

e Fam

ilyBDNApo

lymeraseisa

lsoessentialinHalobacteriu

mB

ecause

itsfunctio

nhasn

otbeen

clearlyelu

cidateditmight

also

play

aroleinreplicationin

thisandclo

selyrelated

organism

s

10 Archaea

interact with other unknown initiation enzymes resultingin a complex phylogeny of the MCM homologs [49] Pre-sumably these differences also account for the inability torecognize the origin of replication in these microorganismsThis unique scenario for initiation of DNA replicationmay bea direct consequence of various processes such as duplicationmobile genetic elements and interactions with viruses [58]

The differences in DNA replication among archaealhigher taxa demonstrate an unexpected variability and sug-gest two alternative evolutionary models In the first modelDNA replication evolved late after the diversification ofthe archaeal lineages Because the replicative system wasnot fully formed it was possible to develop differentlybetween the lineages Once formed replication would thenbe highly conserved However this model is not consistentwith differences observed between lineages that must haveformed relatively late such as those between the orders oreven in some cases within certain orders The alternativemodel is that DNA replication has changed throughout theevolution of the archaea Thus differences in the replicativesystems may represent ancient as well as modern adaptationsto changing environments In this case differences in thereplicative systems may provide important insights into theevolutionary pressures in play during different episodes ofarchaeal evolution From this perspective the differencesbetween the eukaryotic and archaeal replicative systems maynot be evidence for an ancient origin of the eukaryotesInstead it is entirely plausible that the replicative system ineukaryotes could have evolved relatively late from a well-developed archaeal system

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] E F DeLong and N R Pace ldquoEnvironmental diversity ofbacteria and archaeardquo Systematic Biology vol 50 no 4 pp 470ndash478 2001

[2] B Chaban S Y M Ng and K F Jarrell ldquoArchaeal habitatsmdashfrom the extreme to the ordinaryrdquo Canadian Journal of Micro-biology vol 52 no 2 pp 73ndash116 2006

[3] M J Hanford and T L Peeples ldquoArchaeal tetraether lipidsunique structures and applicationsrdquo Applied Biochemistry andBiotechnology A vol 97 no 1 pp 45ndash62 2002

[4] K Sandman and J N Reeve ldquoArchaeal histones and the originof the histone foldrdquo Current Opinion in Microbiology vol 9 no5 pp 520ndash525 2006

[5] O Lecompte R Ripp J-C Thierry D Moras and O PochldquoComparative analysis of ribosomal proteins in complete gen-omes an example of reductive evolution at the domain scalerdquoNucleic Acids Research vol 30 no 24 pp 5382ndash5390 2002

[6] D R Edgell and W F Doolittle ldquoArchaea and the origin(s) ofDNA rplication poteinsrdquo Cell vol 89 no 7 pp 995ndash998 1997

[7] E R Barry and S D Bell ldquoDNA replication in the archaeardquoMicrobiology and Molecular Biology Reviews vol 70 no 4 pp876ndash887 2006

[8] S Gribaldo and C Brochier-Armanet ldquoThe origin and evolu-tion of archaea a state of the artrdquo Philosophical Transactions ofthe Royal Society B vol 361 no 1470 pp 1007ndash1022 2006

[9] P Londei ldquoEvolution of translational initiation new insightsfrom the archaeardquo FEMS Microbiology Reviews vol 29 no 2pp 185ndash200 2005

[10] B Grabowski and Z Kelman ldquoArchaeal DNA replicationeukaryal proteins in a bacterial contextrdquo Annual Review ofMicrobiology vol 57 pp 487ndash516 2003

[11] P Forterre J Filee and H Myllykallio ldquoOrigin and evolutionof DNA and DNA replication machineriesrdquo in The GeneticCode and the Origin of Life L Ribas Ed Landes BioscienceGeorgetown Tex USA 2007

[12] E V Koonin ldquoThe origin and early evolution of eukaryotesin the light of phylogenomicsrdquo Genome Biology vol 11 no 5article 209 2010

[13] M Konneke A E Bernhard J R de la Torre C B WalkerJ B Waterbury and D A Stahl ldquoIsolation of an autotrophicammonia-oxidizing marine archaeonrdquo Nature vol 437 no7058 pp 543ndash546 2005

[14] C Brochier-Armanet B Boussau S Gribaldo and P ForterreldquoMesophilic crenarchaeota proposal for a third archaeal phy-lum theThaumarchaeotardquoNature Reviews Microbiology vol 6no 3 pp 245ndash252 2008

[15] J G Elkins M Podar D E Graham et al ldquoA korarchaealgenome reveals insights into the evolution of the ArchaeardquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 105 no 23 pp 8102ndash8107 2008

[16] T Nunoura Y Takaki J Kakuta et al ldquoInsights into theevolution of Archaea and eukaryotic protein modifier systemsrevealed by the genome of a novel archaeal grouprdquoNucleic AcidsResearch vol 39 no 8 pp 3204ndash3223 2011

[17] HHuberM J Hohn R Rachel T Fuchs V CWimmer andKO Stetter ldquoAnewphylumofArchaea represented by a nanosizedhyperthermophilic symbiontrdquoNature vol 417 no 6884 pp 63ndash67 2002

[18] C Brochier S Gribaldo Y Zivanovic F Confalonieri and PForterre ldquoNanoarchaea representatives of a novel archaeal phy-lum or a fast-evolving euryarchaeal lineage related to Therm-ococcalesrdquo Genome Biology vol 6 no 5 article R42 2005

[19] S J Aves ldquoDNA replication initiationrdquo Methods in MolecularBiology vol 521 pp 3ndash17 2009

[20] N P Robinson I Dionne M Lundgren V L Marsh RBernander and S D Bell ldquoIdentification of two origins ofreplication in the single chromosome of the archaeon Sulfolobussolfataricusrdquo Cell vol 116 no 1 pp 25ndash38 2004

[21] M Lundgren A Andersson L Chen P Nilsson and RBernander ldquoThree replication origins in Sulfolobus speciessynchronous initiation of chromosome replication and asyn-chronous terminationrdquo Proceedings of the National Academy ofSciences of theUnited States of America vol 101 no 18 pp 7046ndash7051 2004

[22] N P Robinson and S D Bell ldquoExtrachromosomal element cap-ture and the evolution ofmultiple replication origins in archaealchromosomesrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 104 no 14 pp 5806ndash58112007

[23] E A Pelve A C Lindas A Knoppel A Mira and R Bernan-der ldquoFour chromosome replication origins in the archaeonPyrobaculum calidifontisrdquo Molecular Microbiology vol 85 no5 pp 986ndash995 2012

Archaea 11

[24] A F Andersson E A Pelve S LindebergM Lundgren P Nils-son and R Bernander ldquoReplication-biased genome organisa-tion in the crenarchaeon Sulfolobusrdquo BMCGenomics vol 11 no1 article 454 2010

[25] H Myllykallio P Lopez P Lopez-Garcıa et al ldquoBacterial modeof replication with eukaryotic-like machinery in a hyperther-mophilic archaeonrdquo Science vol 288 no 5474 pp 2212ndash22152000

[26] F Matsunaga P Forterre Y Ishino and H Myllykallio ldquoInvivo interactions of archaeal Cdc6Orc1 and minichromosomemaintenance proteins with the replication originrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 98 no 20 pp 11152ndash11157 2001

[27] S Maisnier-Patin L Malandrin N K Birkeland and RBernander ldquoChromosome replication patterns in the hyper-thermophilic euryarchaeaArchaeoglobus fulgidus andMethano-caldococcus (Methanococcus) jannaschiirdquo Molecular Microbiol-ogy vol 45 no 5 pp 1443ndash1450 2002

[28] R Zhang and C-T Zhang ldquoMultiple replication origins ofthe archaeon Halobacterium species NRC-1rdquo Biochemical andBiophysical Research Communications vol 302 no 4 pp 728ndash734 2003

[29] C Norais M Hawkins A L Hartman J A Eisen H Myl-lykallio and T Allers ldquoGenetic and physical mapping of DNAreplication origins in Haloferax volcaniirdquo PLoS Genetics vol 3no 5 article e77 2007

[30] J A Coker P DasSarma M Capes et al ldquoMultiple replicationorigins of Halobacterium sp strain NRC-1 properties of theconserved orc7-dependent oriC1rdquo Journal of Bacteriology vol191 no 16 pp 5253ndash5261 2009

[31] Z Wu J Liu H Yang H Liu and H Xiang ldquoMultiple repli-cation origins with diverse control mechanisms in Haloarculahispanicardquo Nucleic Acids Research 2013

[32] M Hawkins S Malla M J Blythe C A Nieduszynski and TAllers ldquoAccelerated growth in the absence of DNA replicationoriginsrdquo Nature vol 503 no 7477 pp 544ndash547 2013

[33] A I Majernık and J P J Chong ldquoA conserved mechanismfor replication origin recognition and binding in archaeardquo TheBiochemical Journal vol 409 no 2 pp 511ndash518 2008

[34] J E Galagan C Nusbaum A Roy et al ldquoThe genome of Macetivorans reveals extensive metabolic and physiological diver-sityrdquo Genome Research vol 12 no 4 pp 532ndash542 2002

[35] R Zhang and C-T Zhang ldquoIdentification of replication originsin archaeal genomes based on the Z-curve methodrdquo Archaeavol 1 no 5 pp 335ndash346 2005

[36] A Spang R Hatzenpichler C Brochier-Armanet et al ldquoDis-tinct gene set in two different lineages of ammonia-oxidizingarchaea supports the phylum Thaumarchaeotardquo Trends inMicrobiology vol 18 no 8 pp 331ndash340 2010

[37] K J Marians ldquoProkaryotic DNA replicationrdquo Annual Review ofBiochemistry vol 61 pp 673ndash719 1992

[38] S P Bell ldquoThe origin recognition complex from simple originsto complex functionsrdquo Genes and Development vol 16 no 6pp 659ndash672 2002

[39] V L Marsh and S D Bell ldquoDNA replication and the cell cyclerdquoin Archaea Evolution Physiology and Molecular Biology R AGarrett and H P Klenk Eds Blackwell Publishing HobokenNJ USA 2007

[40] F Matsunaga A Glatigny M-H Mucchielli-Giorgi et alldquoGenomewide and biochemical analyses of DNA-binding activ-ity of Cdc6Orc1 and Mcm proteins in Pyrococcus sprdquo NucleicAcids Research vol 35 no 10 pp 3214ndash3222 2007

[41] J Liu C L Smith D DeRyckere K DeAngelis G S Martinand J M Berger ldquoStructure and function of Cdc6Cdc18implications for origin recognition and checkpoint controlrdquoMolecular Cell vol 6 no 3 pp 637ndash648 2000

[42] M R Singleton R Morales I Grainge N Cook M NIsupov and D B Wigley ldquoConformational changes inducedby nucleotide binding in Cdc6ORC from Aeropyrum pernixrdquoJournal of Molecular Biology vol 343 no 3 pp 547ndash557 2004

[43] Y Ishino and S Ishino ldquoRapid progress of DNA replicationstudies in Archaea the third domain of liferdquo Science China LifeSciences vol 55 no 5 pp 386ndash403 2012

[44] E L Hendrickson R Kaul Y Zhou et al ldquoComplete genomesequence of the genetically tractable hydrogenotrophic meth-anogen Methanococcus maripaludisrdquo Journal of Bacteriologyvol 186 no 20 pp 6956ndash6969 2004

[45] B K Tye ldquoMCM proteins in DNA replicationrdquo Annual Reviewof Biochemistry vol 68 pp 649ndash686 1999

[46] K Labib and J F X Diffley ldquoIs the MCM2-7 complex theeukaryotic DNA replication fork helicaserdquo Current Opinion inGenetics amp Development vol 11 no 1 pp 64ndash70 2001

[47] I Ilves T Petojevic J J Pesavento and M R Botchan ldquoActi-vation of the MCM2-7 helicase by association with Cdc45 andGINS proteinsrdquoMolecular Cell vol 37 no 2 pp 247ndash258 2010

[48] M L Bochman andA Schwacha ldquoTheMcm complex unwind-ing the mechanism of a replicative helicaserdquo Microbiology andMolecular Biology Reviews vol 73 no 4 pp 652ndash683 2009

[49] Y Ishimi ldquoADNAhelicase activity is associated with anMCM4-6 and -7 protein complexrdquoThe Journal of Biological Chemistryvol 272 no 39 pp 24508ndash24513 1997

[50] Z Kelman and M F White ldquoArchaeal DNA replication andrepairrdquo Current Opinion in Microbiology vol 8 no 6 pp 669ndash676 2005

[51] J H LeBowitz and R McMacken ldquoThe Escherichia coli dnaBreplication protein is a DNA helicaserdquoThe Journal of BiologicalChemistry vol 261 no 10 pp 4738ndash4748 1986

[52] Z Kelman J-K Lee and J Hurwitz ldquoThe single minichro-mosome maintenance protein ofMethanobacterium thermoau-totrophicum ΔH contains DNA helicase activityrdquo Proceedings ofthe National Academy of Sciences of the United States of Americavol 96 no 26 pp 14783ndash14788 1999

[53] D F Shechter C Y Ying and J Gautier ldquoThe intrinsic DNAhelicase activity of Methanobacterium thermoautotrophicumΔH minichromosome maintenance proteinrdquo The Journal ofBiological Chemistry vol 275 no 20 pp 15049ndash15059 2000

[54] M de Felice L Esposito B Pucci M de Falco M Rossi andF M Pisani ldquoA CDC6-like factor from the archaea Sulfolobussolfataricus promotes binding of the mini-chromosome main-tenance complex to DNArdquoThe Journal of Biological Chemistryvol 279 no 41 pp 43008ndash43012 2004

[55] R Kasiviswanathan J-H Shin and Z Kelman ldquoInteractionsbetween the archaeal Cdc6 and MCM proteins modulate theirbiochemical propertiesrdquo Nucleic Acids Research vol 33 no 15pp 4940ndash4950 2005

[56] J-H Shin B Grabowski R Kasiviswanathan S D Bell andZ Kelman ldquoRegulation of minichromosomemaintenance heli-case activity by Cdc6rdquo The Journal of Biological Chemistry vol278 no 39 pp 38059ndash38067 2003

[57] M Akita A Adachi K Takemura T Yamagami F Matsunagaand Y Ishino ldquoCdc6Orc1 from Pyrococcus furiosus may actas the origin recognition protein and Mcm helicase recruiterrdquoGenes to Cells vol 15 no 5 pp 537ndash552 2010

12 Archaea

[58] M Krupovic S Gribaldo D H Bamford and P Forterre ldquoTheevolutionary history of archaeal MCM helicases a case study ofvertical evolution combined with hitchhiking of mobile geneticelementsrdquo Molecular Biology and Evolution vol 27 no 12 pp2716ndash2732 2010

[59] ADWalters and J P J Chong ldquoAn archaeal orderwithmultipleminichromosome maintenance genesrdquo Microbiology vol 156part 5 pp 1405ndash1414 2010

[60] A DWalters and J P J Chong ldquoMethanococcusmaripaludis anarchaeon with multiple functional MCM proteinsrdquo Biochemi-cal Society Transactions vol 37 no 1 pp 1ndash6 2009

[61] Q Xia E L Hendrickson Y Zhang et al ldquoQuantitative pro-teomics of the archaeon Methanococcus maripaludis validatedbymicroarray analysis and real time PCRrdquoMolecularampCellularProteomics vol 5 no 5 pp 868ndash881 2006

[62] F Sarmiento J Mrazek and W B Whitman ldquoGenome-scaleanalysis of gene function in the hydrogenotrophic methano-genic archaeon Methanococcus maripaludisrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 110 no 12 pp 4726ndash4731 2013

[63] M Pan T J Santangelo Z Li J N Reeve and Z KelmanldquoThermococcus kodakarensis encodes threeMCMhomologs butonly one is essentialrdquo Nucleic Acids Research vol 39 no 22 pp9671ndash9680 2011

[64] S Ishino S Fujino H Tomita et al ldquoBiochemical and geneticalanalyses of the three mcm genes from the hyperthermophilicarchaeon Thermococcus kodakarensisrdquo Genes to Cells vol 16no 12 pp 1176ndash1189 2011

[65] K S Makarova Y I Wolf S L Mekhedov B G Mirkin and EV Koonin ldquoAncestral paralogs and pseudoparalogs and theirrole in the emergence of the eukaryotic cellrdquo Nucleic AcidsResearch vol 33 no 14 pp 4626ndash4638 2005

[66] N Marinsek E R Barry K S Makarova I Dionne E VKoonin and S D Bell ldquoGINS a central nexus in the archaealDNA replication forkrdquo EMBOReports vol 7 no 5 pp 539ndash5452006

[67] T Yoshimochi R Fujikane M Kawanami F Matsunaga and YIshino ldquoTheGINS complex from Pyrococcus furiosus stimulatesthe MCM helicase activityrdquoThe Journal of Biological Chemistryvol 283 no 3 pp 1601ndash1609 2008

[68] T Oyama S Ishino S Fujino et al ldquoArchitectures of archaealGINS complexes essential DNA replication initiation factorsrdquoBMC Biology vol 9 article 28 2011

[69] H Ogino S Ishino K Mayanagi et al ldquoThe GINS com-plex from the thermophilic archaeon Thermoplasma aci-dophilummay function as a homotetramer inDNA replicationrdquoExtremophiles vol 15 no 4 pp 529ndash539 2011

[70] L Sanchez-Pulido and C P Ponting ldquoCdc45 the missing recjortholog in eukaryotesrdquoBioinformatics vol 27 no 14 pp 1885ndash1888 2011

[71] Z Li T J Santangelo L Cubonova J N Reeve and Z KelmanldquoAffinity purification of an archaeal DNA replication proteinnetworkrdquomBio vol 1 no 5 2010

[72] Z Li M Pan T J Santangelo et al ldquoA novel DNA nucleaseis stimulated by association with the GINS complexrdquo NucleicAcids Research vol 39 no 14 pp 6114ndash6123 2011

[73] L A Rajman and S T Lovett ldquoA thermostable single-strandDNase from Methanococcus jannaschii related to the RecJrecombination and repair exonuclease from Escherichia colirdquoJournal of Bacteriology vol 182 no 3 pp 607ndash612 2000

[74] K RWilliams J B Murphy and JW Chase ldquoCharacterizationof the structural and functional defect in the Escherichia colisingle-stranded DNA binding protein encoded by the ssb-1 mutant gene Expression of the ssb-1 gene under 120582p(L)regulationrdquoThe Journal of Biological Chemistry vol 259 no 19pp 11804ndash11811 1984

[75] S Dąbrowski M Olszewski R Pitek and J Kur ldquoNovel ther-mostable ssDNA-binding proteins fromThermus thermophilusand T aquaticus-expression and purificationrdquo Protein Expres-sion and Purification vol 26 no 1 pp 131ndash138 2002

[76] C Iftode Y Daniely and J A Borowiec ldquoReplication proteinA (RPA) the eukaryotic SSBrdquo Critical Reviews in Biochemistryand Molecular Biology vol 34 no 3 pp 141ndash180 1999

[77] A G Murzin ldquoOB(oligonucleotideoligosaccharide binding)-fold common structural and functional solution for non-hom-ologous sequencesrdquo The EMBO Journal vol 12 no 3 pp 861ndash867 1993

[78] C A Haseltine and S C Kowalczykowski ldquoA distinctive single-stranded DNA-binding protein from the Archaeon Sulfolobussolfataricusrdquo Molecular Microbiology vol 43 no 6 pp 1505ndash1515 2002

[79] R I M Wadsworth and M F White ldquoIdentification and pro-perties of the crenarchaeal single-stranded DNA binding pro-tein from Sulfolobus solfataricusrdquoNucleic Acids Research vol 29no 4 pp 914ndash920 2001

[80] I D Kerr R I M Wadsworth L Cubeddu W Blankenfeldt JHNaismith andM FWhite ldquoInsights into ssDNA recognitionby the OB fold from a structural and thermodynamic study ofSulfolobus SSB proteinrdquo The EMBO Journal vol 22 no 11 pp2561ndash2570 2003

[81] X Luo U Schwarz-Linek C H Botting R Hensel B Siebersand M F White ldquoCC1 a novel crenarchaeal DNA binding pro-teinrdquo Journal of Bacteriology vol 189 no 2 pp 403ndash409 2007

[82] T J Kelly P Simancek and G S Brush ldquoIdentification andcharacterization of a single-stranded DNA-binding proteinfrom the archaeonMethanococcus jannaschiirdquoProceedings of theNational Academy of Sciences of theUnited States of America vol95 no 25 pp 14634ndash14639 1998

[83] Z Kelman S Pietrokovski and J Hurwitz ldquoIsolation and cha-racterization of a split B-type DNA polymerase from the arch-aeonMethanobacterium thermoautotrophicumΔHrdquoTheJournalof Biological Chemistry vol 274 no 40 pp 28751ndash28761 1999

[84] K Komori and Y Ishino ldquoReplication protein A in Pyrococcusfuriosus is involved in homologous DNA recombinationrdquo TheJournal of Biological Chemistry vol 276 no 28 pp 25654ndash25660 2001

[85] J B Robbins M C Murphy B A White R I Mackie THa and I K O Cann ldquoFunctional analysis of multiple single-stranded DNA-binding proteins from Methanosarcina acetivo-rans and their effects on DNA synthesis by DNA polymeraseBIrdquoThe Journal of Biological Chemistry vol 279 no 8 pp 6315ndash6326 2004

[86] Y Lin L-J Lin P Sriratana et al ldquoEngineering of functionalreplication protein a homologs based on insights into the evolu-tion of oligonucleotideoligosaccharide-binding foldsrdquo Journalof Bacteriology vol 190 no 17 pp 5766ndash5780 2008

[87] D N Frick and C C Richardson ldquoDNA primasesrdquo AnnualReview of Biochemistry vol 70 pp 39ndash80 2001

[88] G Desogus S Onesti P Brick M Rossi and F M PisanildquoIdentification and characterization of a DNA primase fromthe hyperthermophilic archaeon Methanococcus jannaschiirdquoNucleic Acids Research vol 27 no 22 pp 4444ndash4450 1999

Archaea 13

[89] A A Bocquier L Liu I K O Cann K Komori D Kohda andY Ishino ldquoArchaeal primase bridging the gap between RNAand DNA polymerasesrdquo Current Biology vol 11 no 6 pp 452ndash456 2001

[90] L Liu K Komori S Ishino et al ldquoThe archaeal DNA primasebiochemical characterization of the p41-p46 complex fromPyrococcus furiosusrdquo The Journal of Biological Chemistry vol276 no 48 pp 45484ndash45490 2001

[91] E Matsui M Nishio H Yokoyama K Harata S Darnisand I Matsui ldquoDistinct domain functions regulating de novoDNA synthesis of thermostable DNA primase from hyperther-mophile Pyrococcus horikoshiirdquo Biochemistry vol 42 no 50 pp14968ndash14976 2003

[92] N Ito I Matsui and EMatsui ldquoMolecular basis for the subunitassembly of the primase from an archaeon Pyrococcus hori-koshiirdquoThe FEBS Journal vol 274 no 5 pp 1340ndash1351 2007

[93] M le Breton G Henneke C Norais et al ldquoThe heterodimericprimase from the euryarchaeon Pyrococcus abyssi a multifunc-tional enzyme for initiation and repairrdquo Journal of MolecularBiology vol 374 no 5 pp 1172ndash1185 2007

[94] S-H Lao-Sirieix and S D Bell ldquoThe heterodimeric primaseof the hyperthermophilic archaeon Sulfolobus solfataricus pos-sesses DNA and RNA primase polymerase and 31015840-terminalnucleotidyl transferase activitiesrdquo Journal of Molecular Biologyvol 344 no 5 pp 1251ndash1263 2004

[95] S-H Lao-Sirieix L Pellegrini and S D Bell ldquoThe promiscuousprimaserdquo Trends in Genetics vol 21 no 10 pp 568ndash572 2005

[96] J Hu L Guo K Wu B Liu S Lang and L Huang ldquoTemplate-dependent polymerization across discontinuous templatesby the heterodimeric primase from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquoNucleic Acids Research vol 40no 8 pp 3470ndash3483 2012

[97] E Evguenieva-Hackenberg P Walter E Hochleitner FLottspeich and G Klug ldquoAn exosome-like complex in Sulfolo-bus solfataricusrdquo EMBOReports vol 4 no 9 pp 889ndash893 2003

[98] P Walter F Klein E Lorentzen A Ilchmann G Klug andE Evguenieva-Hackenberg ldquoCharacterization of native andreconstituted exosome complexes from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Microbiology vol62 no 4 pp 1076ndash1089 2006

[99] Z Zuo C J Rodgers A L Mikheikin and M A Trak-selis ldquoCharacterization of a functional DnaG-type primase inarchaea implications for a dual-primase systemrdquo Journal ofMolecular Biology vol 397 no 3 pp 664ndash676 2010

[100] B R Berquist P DasSarma and S DasSarma ldquoEssential andnon-essential DNA replication genes in the model halophilicArchaeon Halobacterium sp NRC-1rdquo BMC Genetics vol 8article 31 2007

[101] D K Braithwaite and J Ito ldquoCompilation alignment andphylogenetic relationships of DNA polymerasesrdquo Nucleic AcidsResearch vol 21 no 4 pp 787ndash802 1993

[102] I K O Cann and Y Ishino ldquoArchaeal DNA replication iden-tifying the pieces to solve a puzzlerdquo Genetics vol 152 no 4 pp1249ndash1267 1999

[103] G Lipps S Rother C Hart and G Krauss ldquoA novel typeof replicative enzyme harbouring ATpase primase and DNApolymerase activityrdquo The EMBO Journal vol 22 no 10 pp2516ndash2525 2003

[104] J Yamtich and J B Sweasy ldquoDNA polymerase family X func-tion structure and cellular rolesrdquoBiochimica et BiophysicaActavol 1804 no 5 pp 1136ndash1150 2010

[105] H Ohmori E C Friedberg R P P Fuchs et al ldquoThe Y-familyof DNA polymerasesrdquoMolecular Cell vol 8 no 1 pp 7ndash8 2001

[106] N Y Yao R E Georgescu J Finkelstein and M E OrsquoDonnellldquoSingle-molecule analysis reveals that the lagging strandincreases replisome processivity but slows replication forkprogressionrdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 106 no 32 pp 13236ndash132412009

[107] U Hubscher G Maga and S Spadari ldquoEukaryotic DNA poly-merasesrdquo Annual Review of Biochemistry vol 71 pp 133ndash1632002

[108] F Boudsocq S Iwai F Hanaoka and R Woodgate ldquoSulfolobussolfataricus P2 DNA polymerase IV (Dp04) an archaeal DinB-like DNA polymerase with lesion-bypass properties akin toeukaryotic pol120578rdquo Nucleic Acids Research vol 29 no 22 pp4607ndash4616 2001

[109] L-J Lin A Yoshinaga Y Lin et al ldquoMolecular analyses ofan unusual translesion DNA polymerase fromMethanosarcinaacetivorans C2Ardquo Journal of Molecular Biology vol 397 no 1pp 13ndash30 2010

[110] I K O Cann S Ishino NNomura Y Sako andY Ishino ldquoTwofamily B DNA polymerases from Aeropyrum pernix an aerobichyperthermophilic crenarchaeoterdquo Journal of Bacteriology vol181 no 19 pp 5984ndash5992 1999

[111] T Uemori Y Ishino H Doi and I Kato ldquoThe hyperther-mophilic archaeon Pyrodictium occultum has two 120572-like DNApolymerasesrdquo Journal of Bacteriology vol 177 no 8 pp 2164ndash2177 1995

[112] T Uemori Y Ishino H Toh K Asada and I Kato ldquoOrgani-zation and nucleotide sequence of the DNA polymerase genefrom the archaeon Pyrococcus furiosusrdquo Nucleic Acids Researchvol 21 no 2 pp 259ndash265 1993

[113] B A Connolly ldquoRecognition of deaminated bases by archaealfamily-B DNA polymerasesrdquo Biochemical Society Transactionsvol 37 no 1 pp 65ndash68 2009

[114] B A Connolly M J Fogg G Shuttleworth and B T WilsonldquoUracil recognition by archaeal family B DNA polymerasesrdquoBiochemical Society Transactions vol 31 no 3 pp 699ndash7022003

[115] T T Richardson X Wu B J Keith P Heslop A C Jones andB A Connolly ldquoUnwinding of primer-templates by archaealfamily-B DNA polymerases in response to template-stranduracilrdquo Nucleic Acids Research vol 41 no 4 pp 2466ndash24782013

[116] T Lindahl ldquoInstability and decay of the primary structure ofDNArdquo Nature vol 362 no 6422 pp 709ndash715 1993

[117] I B Rogozin K S Makarova Y I Pavlov and E V Koonin ldquoAhighly conserved family of inactivated archaeal B family DNApolymerasesrdquo Biology Direct vol 3 article 32 2008

[118] M Imamura T Uemori I Kato and Y Ishino ldquoA non-120572-like DNA polymerase from the hyperthermophilic archaeonPyrococcus furiosusrdquoBiological andPharmaceutical Bulletin vol18 no 12 pp 1647ndash1652 1995

[119] I K O Cann K Komori H Toh S Kanai and Y IshinoldquoA heterodimeric DNA polymerase evidence that members ofEuryarchaeota possess a distinct DNA polymeraserdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 95 no 24 pp 14250ndash14255 1998

[120] L Aravind D D Leipe and E V Koonin ldquoToprimmdasha con-served catalytic domain in type IA and II topoisomerases

14 Archaea

DnaG-type primases OLD family nucleases and RecR pro-teinsrdquo Nucleic Acids Research vol 26 no 18 pp 4205ndash42131998

[121] M Jokela A Eskelinen H Pospiech J Rouvinen and J ESyvaoja ldquoCharacterization of the 31015840 exonuclease subunit DP1of Methanococcus jannaschii replicative DNA polymerase DrdquoNucleic Acids Research vol 32 no 8 pp 2430ndash2440 2004

[122] T Uemori Y Sato I Kato H Doi and Y Ishino ldquoA novel DNApolymerase in the hyperthermophilic archaeon Pyrococcus fur-iosus gene cloning expression and characterizationrdquo Genes toCells vol 2 no 8 pp 499ndash512 1997

[123] Y Shen K Musti M Hiramoto H Kikuchi Y Kawarabayashiand I Matsui ldquoInvariant Asp-1122 and Asp-1124 are essentialresidues for polymerization catalysis of family D DNA poly-merase from Pyrococcus horikoshiirdquo The Journal of BiologicalChemistry vol 276 no 29 pp 27376ndash27383 2001

[124] G Henneke D Flament U Hubscher J Querellou and J-P Raffin ldquoThe hyperthermophilic euryarchaeota Pyrococcusabyssi likely requires the two DNA polymerases D and B forDNA replicationrdquo Journal of Molecular Biology vol 350 no 1pp 53ndash64 2005

[125] L Cubonova T Richardson B W Burkhart et al ldquoArchaealDNA polymerase D but not DNA polymerase B is required forgenome replication in Thermococcus kodakarensisrdquo Journal ofBacteriology vol 195 no 10 pp 2322ndash2328 2013

[126] C Rouillon G Henneke D Flament J Querellou and J-PRaffin ldquoDNA polymerase switching on homotrimeric PCNA atthe replication fork of the euryarchaea Pyrococcus abyssirdquo Jour-nal of Molecular Biology vol 369 no 2 pp 343ndash355 2007

[127] G Henneke ldquoIn vitro reconstitution of RNA primer removal inArchaea reveals the existence of two pathwaysrdquoTheBiochemicalJournal vol 447 no 2 pp 271ndash280 2012

[128] G-LMoldovan B Pfander and S Jentsch ldquoPCNA themaestroof the replication forkrdquo Cell vol 129 no 4 pp 665ndash679 2007

[129] X-P Kong R Onrust M OrsquoDonnell and J Kuriyan ldquoThree-dimensional structure of the 120573 subunit of E coli DNA poly-merase III holoenzyme a sliding DNA clamprdquo Cell vol 69 no3 pp 425ndash437 1992

[130] K Daimon Y Kawarabayasi H Kikuchi Y Sako and Y IshinoldquoThree proliferating cell nuclear antigen-like proteins foundin the hyperthermophilic archaeon Aeropyrum pemix interac-tions with the two DNA polymerasesrdquo Journal of Bacteriologyvol 184 no 3 pp 687ndash694 2002

[131] I Dionne R K Nookala S P Jackson A J Doherty andS D Bell ldquoA heterotrimeric PCNA in the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Cell vol 11 no 1pp 275ndash282 2003

[132] E Warbrick ldquoPCNA binding through a conserved motifrdquoBioEssays vol 20 no 3 pp 195ndash199 1998

[133] H Nishida K Mayanagi S Kiyonari et al ldquoStructural deter-minant for switching between the polymerase and exonucleasemodes in the PCNA-replicative DNA polymerase complexrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 106 no 49 pp 20693ndash20698 2009

[134] K Mayanagi S Kiyonari H Nishida et al ldquoArchitecture of theDNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complexrdquo Proceedings of the National Academy ofSciences of the United States of America vol 108 no 5 pp 1845ndash1849 2011

[135] B Castrec C Rouillon G Henneke D Flament J Querellouand J-P Raffin ldquoBinding to PCNA in Euryarchaeal DNA

replication requires two PIP motifs for DNA polymerase D andone PIP motif for DNA polymerase Brdquo Journal of MolecularBiology vol 394 no 2 pp 209ndash218 2009

[136] P F Pluchon T Fouqueau C Creze et al ldquoAn extendednetworkof genomic maintenance in the archaeon Pyrococcus abyssihighlights unexpected associations between eucaryotic homo-logsrdquo PLoS One vol 8 no 11 Article ID e79707 2013

[137] J E Ladner M Pan J Hurwitz and Z Kelman ldquoCrystalstructures of two active proliferating cell nuclear antigens(PCNAs) encoded byThermococcus kodakaraensisrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2711ndash2716 2011

[138] Y Kuba S Ishino T Yamagami et al ldquoComparative analyses ofthe two proliferating cell nuclear antigens from the hyperther-mophilic archaeonThermococcus kodakarensisrdquo Genes to Cellsvol 17 no 11 pp 923ndash937 2012

[139] T Fukui H Atomi T Kanai R Matsumi S Fujiwara andT Imanaka ldquoComplete genome sequence of the hyperther-mophilic archaeon Thermococcus kodakaraensis KOD1 andcomparison with Pyrococcus genomesrdquo Genome Research vol15 no 3 pp 352ndash363 2005

[140] D Jeruzalmi O Yurieva Y Zhao et al ldquoMechanism of proces-sivity clamp opening by the delta subunit wrench of the clamploader complex of E coliDNApolymerase IIIrdquoCell vol 106 no4 pp 417ndash428 2001

[141] Y Shiomi J Usukura Y Masamura et al ldquoATP-dependentstructural change of the eukaryotic clamp-loader protein repli-cation factor Crdquo Proceedings of the National Academy of Sciencesof the United States of America vol 97 no 26 pp 14127ndash141322000

[142] T Miyata T Oyama K Mayanagi S Ishino Y Ishino and KMorikawa ldquoThe clamp-loading complex for processive DNAreplicationrdquoNature Structural andMolecular Biology vol 11 no7 pp 632ndash636 2004

[143] T Oyama Y Ishino I K O Cann S Ishino and K MorikawaldquoAtomic structure of the clamp loader small subunit fromPyrococcus furiosusrdquo Molecular Cell vol 8 no 2 pp 455ndash4632001

[144] A Seybert D J Scott S Scaife M R Singleton and DB Wigley ldquoBiochemical characterisation of the clampclamploader proteins from the euryarchaeon Archaeoglobus fulgidusrdquoNucleic Acids Research vol 30 no 20 pp 4329ndash4338 2002

[145] Y-H Chen Y Lin A Yoshinaga et al ldquoMolecular analyses of athree-subunit euryarchaeal clamp loader complex from Meth-anosarcina acetivoransrdquo Journal of Bacteriology vol 191 no 21pp 6539ndash6549 2009

[146] Y-H Chen S A Kocherginskaya Y Lin et al ldquoBiochemicaland mutational analyses of a unique clamp loader complex inthe archaeon Methanosarcina acetivoransrdquo The Journal of Bio-logical Chemistry vol 280 no 51 pp 41852ndash41863 2005

[147] F Matsunaga C Norais P Forterre and H Myllykallio ldquoIden-tification of short ldquoeukaryoticrdquo Okazaki fragments synthesizedfrom a prokaryotic replication originrdquo EMBO Reports vol 4no 2 pp 154ndash158 2003

[148] H Kochiwa M Tomita and A Kanai ldquoEvolution of ribonucle-ase H genes in prokaryotes to avoid inheritance of redundantgenesrdquo BMC Evolutionary Biology vol 7 article 128 2007

[149] N OhtaniMHarukiMMorikawa and S Kanaya ldquoMoleculardiversities of RNases Hrdquo Journal of Bioscience and Bioengineer-ing vol 88 no 1 pp 12ndash19 1999

Archaea 15

[150] N Ohtani M Haruki M Morikawa R J Crouch M Itayaand S Kanaya ldquoIdentification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII fromBacillus subtilis classification of RNases H into three familiesrdquoBiochemistry vol 38 no 2 pp 605ndash618 1999

[151] N Ohtani H Yanagawa M Tomita and M Itaya ldquoIdentifi-cation of the first archaeal type 1 RNase H gene from Halobac-terium sp NRC-1 archaeal RNase HI can cleave an RNA-DNAjunctionrdquoThe Biochemical Journal vol 381 no 3 pp 795ndash8022004

[152] N Ohtani H Yanagawa M Tomita and M Itaya ldquoCleavage ofdouble-stranded RNA by RNase HI from a thermoacidophilicarchaeon Sulfolobus tokodaii 7rdquo Nucleic Acids Research vol 32no 19 pp 5809ndash5819 2004

[153] M A Nowak M C Boerlijst J Cooke and J M SmithldquoEvolution of genetic redundancyrdquo Nature vol 388 no 6638pp 167ndash170 1997

[154] A E Tomkinson S Vijayakumar J M Pascal and T Ellen-berger ldquoDNA ligases structure reactionmechanism and func-tionrdquo Chemical Reviews vol 106 no 2 pp 687ndash699 2006

[155] M Nakatani S Ezaki H Atomi and T Imanaka ldquoA DNAligase from a hyperthermophilic archaeon with unique cofactorspecificityrdquo Journal of Bacteriology vol 182 no 22 pp 6424ndash6433 2000

[156] Y Sun M S Seo J H Kim et al ldquoNovel DNA ligase with broadnucleotide cofactor specificity from the hyperthermophilic cre-narchaeon Sulfophobococcus zilligii influence of ancestral DNAligase on cofactor utilizationrdquo Environmental Microbiology vol10 no 12 pp 3212ndash3224 2008

[157] T R Beattie and S D Bell ldquoCoordination of multiple enzymeactivities by a single PCNA in archaeal Okazaki fragmentmaturationrdquo The EMBO Journal vol 31 no 6 pp 1556ndash15672012

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

8 Archaea

removal of the primers is performed by the enzyme RNase Hwhich is ubiquitous in the three domains of life Accordingto their sequence similarity in prokaryotes the RNase Hproteins are classified into three groups RNase HI HII andHIII In eukaryotes they are classified as RNase H1 and H2[148] However phylogenetic analyses suggest that the RNaseH proteins can also be classified into two different groupsType 1 (prokaryotic RNaseHI eukaryotic RNaseH1 and viralRNase H) and Type 2 (prokaryotic RNase HII and HIII andeukaryotic RNase H2) [149] These two types of RNase Hpossess different specific activities metal ion preferences andcleavage sites [150] Originally it was thought that Archaeaonly possess type 2 RNase H [149] but several type 1 archaealRNase H enzymes have since then been discovered [151 152]Interestingly in eukaryotes RNaseH1 andH2 tend to coexistand different combinations of the three prokaryotic RNasesH(I II and III) are found except for the combination of RNasesHI and HIII This mutually exclusive evolution of some ofthe prokaryotic RNases seems to be related to functionalredundancy [148]

Another enzyme involved in primer replacement inDNA replication is the Flap endonuclease I (FEN-1) whichrecognizes double-strandedDNAwith an unannealed 51015840-flapand cleaves it A eukaryotic homolog of FEN-1 is found inevery archaeal member analyzed and one member of theThermoproteales Thermofilum pendens Hrk5 possesses twohomologs

M maripaludis S2 possesses genes for the prokaryoticRNase HI and HII and for FEN-1 but none are essentialsuggesting that they may be redundant in their functions[44 62] Possibly both RNase H proteins persist and areevolutionary stable in the genome The gene products mayperform the same function but one is less efficient than theother [153]

After the Okazaki fragments are replaced by DNA inthe lagging strand the nick between the newly synthesizedand the elongated DNA is repaired by a DNA ligase Thisenzyme uses a nucleotide cofactor to catalyze the formationof the phosphodiester bond in three well-characterized steps[154]The enzyme is common to all three domains but can begrouped into two families based on cofactor specificity (ATPor NAD+) The DNA ligases from several crenarchaeotes andeuryarchaeotes have been further characterized (reviewedin [43]) Many archaeal DNA ligases possess dual cofactorspecificity (ATPNAD+ or ATPADP) but every archaealDNA ligase characterized so far uses ATP A thermophilicDNA ligase from M thermautotrophicus which uses ATP assole cofactor was characterized in vitro [155] A characterizedDNA ligase from the crenarchaeote Sulfophobococcus zilligiidisplayed specificity for three cofactors (ATPNAD+GTP)[156]Major structuralwork in this enzymehas been achievedin P furiosus and S solfataricus and the findings have beenreviewed in detail [43] InM maripaludis S2 the DNA ligaseis likely to be essential for growth [44 62]

Understanding the maturation process in archaea hasbecome a focus of increasing research in recent years An invitro study reconstituted the Okazaki fragment maturationusing proteins derived from the crenarchaeote S solfataricusThey demonstrated that only six proteins are necessary for

coupled DNA synthesis RNA primer removal and DNAligation In this model a single PCNA (heterotrimeric ring)coordinates the activities of PolBI FEN-1 and DNA ligaseinto an efficient maturation complex [157] A different invitro study in P abyssi has demonstrated two different modelsfor Okazaki fragments maturation which differ in the RNAprimer removal process In the first model RNA primerelimination is executed by continuous PolD strand displace-ment DNA synthesis and 51015840RNA flap cleavage by FEN-1The resulting nicks are closed by DNA ligase Alternativelythe second model proposes that RNase HII cleaves theRNA primer followed by the action of FEN-1 and stranddisplacement DNA synthesis by polB or polD The nick isthen sealed by DNA ligase [127] Testing these models invivo is of great interest to complete the picture of how theseprocesses behave in the cell In addition other factors that canmodulate these processesmay be required for coordination ofthe in vivomaturation process

4 Conclusions

DNA replication in archaea possesses a dual nature wherethe machinery is structurally and functionally similar to theeukaryotic replication system but it is executed within abacterial context [11 25] Additionally unique archaeal fea-tures demonstrate the complexity of this process and it doesnot appear to be just a simplified version of the eukary-otic system For example the archaeal specific DNA poly-merase D is conserved across the Archaea domain with theexception of the Crenarchaeota phylumThe recent discoverythat it is the essential replicative polymerase in two differenteuryarchaeotic species demonstrates an unanticipated vari-ability in archaeal DNA replication and a fundamental differ-ence in the replication mechanism between crenarchaeotesand euryarchaeotes Interestingly the absence of PolD increnarchaeotes is not the only difference in DNA repli-cation These differences include the absence of histonesin crenarchaeotes [4] the presence of multiple origins ofreplication in crenarchaeotes and a single origin of repli-cation in most euryarchaeotes the absence of GINS23 inmost euryarchaeotes the absence of RPA protein in manycrenarchaeotes the presence of multiple MCM homologs inMethanococcales and the presence of one homolog of PCNAin euryarchaeotes compared to the multiple homologs increnarchaeotes These distinctive characteristics between thephyla highlight the complexity of archaeal DNA replicationand suggest a complex evolutionary history (Table 1)

Among the Euryarchaeota the ordersHalobacteriales andMethanococcales possess differences in the DNA replicationsystem that make them unique For instance Halobac-teriales possess many more origin recognition proteins(Orc1Cdc6) compared to the rest of the archaea On theother hand Methanococcales and Methanopyrales lack rec-ognizable homologs for the Orc1Cdc6 proteins suggestingthe presence of a very different mechanism for initiation ofreplication In addition the Methanococcales possess a largenumber of MCM protein homologs It has been proposedthat these distinctive features are connected and because ofthe absence of the Orc1Cdc6 proteins MCM proteins may

Archaea 9

Table1DNAreplicationproteins

andfeatures

inthed

omains

BacteriaEukaryotaand

thetwomajor

phylao

fthe

Archaeado

main

Mod

ified

from

[43]

DNAreplicationstage

Process

Bacteria

Eukaryota

Archaea

Crenarchaeota

Euryarchaeota

Preinitia

tion

Orig

inof

replication

Sing

leMultip

leMultip

leSing

lea

Orig

inrecogn

ition

DnaA

ORC

complex

(ORC

1-6)

Orc1C

dc6

Orc1C

dc6b

Initiation

DNAun

winding

(Helicase)

DnaB

MCM

complex

(MCM

2-7)

MCM

complex

MCM

complex

DNAun

winding

(Accessory

proteins)

DnaC

Cdc6

GIN

S23GIN

S15

GIN

S15c

Cdt1

GIN

Scomplex

(Sld5Psf1-3)

RecJho

molog

RecJho

molog

Cdc45

Prim

ersynthesis

DnaG

Pol120572

prim

asec

omplex

DNAprim

ase

(PriS

L)D

naG

dDNAprim

ase(PriSL)

Elon

gatio

n

DNAsynthesis

(polym

erase)

PolIII(Fam

ilyCDNApo

lymerase)

Pol120575and

Pol120576(Fam

ilyBDNA

polymerase)

Family

BDNApo

lymerase

Family

DDNA

polymerasee

DNAsynthesis

(Processivity

factors)

120574-com

plex

(clamploader)

RFC(clamploader)

RFC(clamploader)

RFC(clamploader)

120573-clamp(clamp)

PCNA(clamp)

PCNA(clamp)

PCNA(clamp)

Maturation

Maturation(O

kazaki

fragmentp

rocessing)

PolI

(family

ADNApo

lymerase)

Fen1D

na2

Fen1

Fen1

RNaseH

RNaseH

RNaseH

RNaseH

DNAligase

DNAligase

DNAligase

DNAligase

a Exceptio

ntheo

rder

Halobacteria

les

b Not

know

nform

embersof

theE

uryarchaeota

ordersMethanococcalesandMethanopyrales

c GIN

S23hasb

eenfoun

dedon

lyin

theo

rder

Thermococcales

oftheE

uryarchaeota

d Sulfolobu

ssolfataric

usdidshow

prim

asea

ctivity

invitro

e Fam

ilyBDNApo

lymeraseisa

lsoessentialinHalobacteriu

mB

ecause

itsfunctio

nhasn

otbeen

clearlyelu

cidateditmight

also

play

aroleinreplicationin

thisandclo

selyrelated

organism

s

10 Archaea

interact with other unknown initiation enzymes resultingin a complex phylogeny of the MCM homologs [49] Pre-sumably these differences also account for the inability torecognize the origin of replication in these microorganismsThis unique scenario for initiation of DNA replicationmay bea direct consequence of various processes such as duplicationmobile genetic elements and interactions with viruses [58]

The differences in DNA replication among archaealhigher taxa demonstrate an unexpected variability and sug-gest two alternative evolutionary models In the first modelDNA replication evolved late after the diversification ofthe archaeal lineages Because the replicative system wasnot fully formed it was possible to develop differentlybetween the lineages Once formed replication would thenbe highly conserved However this model is not consistentwith differences observed between lineages that must haveformed relatively late such as those between the orders oreven in some cases within certain orders The alternativemodel is that DNA replication has changed throughout theevolution of the archaea Thus differences in the replicativesystems may represent ancient as well as modern adaptationsto changing environments In this case differences in thereplicative systems may provide important insights into theevolutionary pressures in play during different episodes ofarchaeal evolution From this perspective the differencesbetween the eukaryotic and archaeal replicative systems maynot be evidence for an ancient origin of the eukaryotesInstead it is entirely plausible that the replicative system ineukaryotes could have evolved relatively late from a well-developed archaeal system

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] E F DeLong and N R Pace ldquoEnvironmental diversity ofbacteria and archaeardquo Systematic Biology vol 50 no 4 pp 470ndash478 2001

[2] B Chaban S Y M Ng and K F Jarrell ldquoArchaeal habitatsmdashfrom the extreme to the ordinaryrdquo Canadian Journal of Micro-biology vol 52 no 2 pp 73ndash116 2006

[3] M J Hanford and T L Peeples ldquoArchaeal tetraether lipidsunique structures and applicationsrdquo Applied Biochemistry andBiotechnology A vol 97 no 1 pp 45ndash62 2002

[4] K Sandman and J N Reeve ldquoArchaeal histones and the originof the histone foldrdquo Current Opinion in Microbiology vol 9 no5 pp 520ndash525 2006

[5] O Lecompte R Ripp J-C Thierry D Moras and O PochldquoComparative analysis of ribosomal proteins in complete gen-omes an example of reductive evolution at the domain scalerdquoNucleic Acids Research vol 30 no 24 pp 5382ndash5390 2002

[6] D R Edgell and W F Doolittle ldquoArchaea and the origin(s) ofDNA rplication poteinsrdquo Cell vol 89 no 7 pp 995ndash998 1997

[7] E R Barry and S D Bell ldquoDNA replication in the archaeardquoMicrobiology and Molecular Biology Reviews vol 70 no 4 pp876ndash887 2006

[8] S Gribaldo and C Brochier-Armanet ldquoThe origin and evolu-tion of archaea a state of the artrdquo Philosophical Transactions ofthe Royal Society B vol 361 no 1470 pp 1007ndash1022 2006

[9] P Londei ldquoEvolution of translational initiation new insightsfrom the archaeardquo FEMS Microbiology Reviews vol 29 no 2pp 185ndash200 2005

[10] B Grabowski and Z Kelman ldquoArchaeal DNA replicationeukaryal proteins in a bacterial contextrdquo Annual Review ofMicrobiology vol 57 pp 487ndash516 2003

[11] P Forterre J Filee and H Myllykallio ldquoOrigin and evolutionof DNA and DNA replication machineriesrdquo in The GeneticCode and the Origin of Life L Ribas Ed Landes BioscienceGeorgetown Tex USA 2007

[12] E V Koonin ldquoThe origin and early evolution of eukaryotesin the light of phylogenomicsrdquo Genome Biology vol 11 no 5article 209 2010

[13] M Konneke A E Bernhard J R de la Torre C B WalkerJ B Waterbury and D A Stahl ldquoIsolation of an autotrophicammonia-oxidizing marine archaeonrdquo Nature vol 437 no7058 pp 543ndash546 2005

[14] C Brochier-Armanet B Boussau S Gribaldo and P ForterreldquoMesophilic crenarchaeota proposal for a third archaeal phy-lum theThaumarchaeotardquoNature Reviews Microbiology vol 6no 3 pp 245ndash252 2008

[15] J G Elkins M Podar D E Graham et al ldquoA korarchaealgenome reveals insights into the evolution of the ArchaeardquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 105 no 23 pp 8102ndash8107 2008

[16] T Nunoura Y Takaki J Kakuta et al ldquoInsights into theevolution of Archaea and eukaryotic protein modifier systemsrevealed by the genome of a novel archaeal grouprdquoNucleic AcidsResearch vol 39 no 8 pp 3204ndash3223 2011

[17] HHuberM J Hohn R Rachel T Fuchs V CWimmer andKO Stetter ldquoAnewphylumofArchaea represented by a nanosizedhyperthermophilic symbiontrdquoNature vol 417 no 6884 pp 63ndash67 2002

[18] C Brochier S Gribaldo Y Zivanovic F Confalonieri and PForterre ldquoNanoarchaea representatives of a novel archaeal phy-lum or a fast-evolving euryarchaeal lineage related to Therm-ococcalesrdquo Genome Biology vol 6 no 5 article R42 2005

[19] S J Aves ldquoDNA replication initiationrdquo Methods in MolecularBiology vol 521 pp 3ndash17 2009

[20] N P Robinson I Dionne M Lundgren V L Marsh RBernander and S D Bell ldquoIdentification of two origins ofreplication in the single chromosome of the archaeon Sulfolobussolfataricusrdquo Cell vol 116 no 1 pp 25ndash38 2004

[21] M Lundgren A Andersson L Chen P Nilsson and RBernander ldquoThree replication origins in Sulfolobus speciessynchronous initiation of chromosome replication and asyn-chronous terminationrdquo Proceedings of the National Academy ofSciences of theUnited States of America vol 101 no 18 pp 7046ndash7051 2004

[22] N P Robinson and S D Bell ldquoExtrachromosomal element cap-ture and the evolution ofmultiple replication origins in archaealchromosomesrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 104 no 14 pp 5806ndash58112007

[23] E A Pelve A C Lindas A Knoppel A Mira and R Bernan-der ldquoFour chromosome replication origins in the archaeonPyrobaculum calidifontisrdquo Molecular Microbiology vol 85 no5 pp 986ndash995 2012

Archaea 11

[24] A F Andersson E A Pelve S LindebergM Lundgren P Nils-son and R Bernander ldquoReplication-biased genome organisa-tion in the crenarchaeon Sulfolobusrdquo BMCGenomics vol 11 no1 article 454 2010

[25] H Myllykallio P Lopez P Lopez-Garcıa et al ldquoBacterial modeof replication with eukaryotic-like machinery in a hyperther-mophilic archaeonrdquo Science vol 288 no 5474 pp 2212ndash22152000

[26] F Matsunaga P Forterre Y Ishino and H Myllykallio ldquoInvivo interactions of archaeal Cdc6Orc1 and minichromosomemaintenance proteins with the replication originrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 98 no 20 pp 11152ndash11157 2001

[27] S Maisnier-Patin L Malandrin N K Birkeland and RBernander ldquoChromosome replication patterns in the hyper-thermophilic euryarchaeaArchaeoglobus fulgidus andMethano-caldococcus (Methanococcus) jannaschiirdquo Molecular Microbiol-ogy vol 45 no 5 pp 1443ndash1450 2002

[28] R Zhang and C-T Zhang ldquoMultiple replication origins ofthe archaeon Halobacterium species NRC-1rdquo Biochemical andBiophysical Research Communications vol 302 no 4 pp 728ndash734 2003

[29] C Norais M Hawkins A L Hartman J A Eisen H Myl-lykallio and T Allers ldquoGenetic and physical mapping of DNAreplication origins in Haloferax volcaniirdquo PLoS Genetics vol 3no 5 article e77 2007

[30] J A Coker P DasSarma M Capes et al ldquoMultiple replicationorigins of Halobacterium sp strain NRC-1 properties of theconserved orc7-dependent oriC1rdquo Journal of Bacteriology vol191 no 16 pp 5253ndash5261 2009

[31] Z Wu J Liu H Yang H Liu and H Xiang ldquoMultiple repli-cation origins with diverse control mechanisms in Haloarculahispanicardquo Nucleic Acids Research 2013

[32] M Hawkins S Malla M J Blythe C A Nieduszynski and TAllers ldquoAccelerated growth in the absence of DNA replicationoriginsrdquo Nature vol 503 no 7477 pp 544ndash547 2013

[33] A I Majernık and J P J Chong ldquoA conserved mechanismfor replication origin recognition and binding in archaeardquo TheBiochemical Journal vol 409 no 2 pp 511ndash518 2008

[34] J E Galagan C Nusbaum A Roy et al ldquoThe genome of Macetivorans reveals extensive metabolic and physiological diver-sityrdquo Genome Research vol 12 no 4 pp 532ndash542 2002

[35] R Zhang and C-T Zhang ldquoIdentification of replication originsin archaeal genomes based on the Z-curve methodrdquo Archaeavol 1 no 5 pp 335ndash346 2005

[36] A Spang R Hatzenpichler C Brochier-Armanet et al ldquoDis-tinct gene set in two different lineages of ammonia-oxidizingarchaea supports the phylum Thaumarchaeotardquo Trends inMicrobiology vol 18 no 8 pp 331ndash340 2010

[37] K J Marians ldquoProkaryotic DNA replicationrdquo Annual Review ofBiochemistry vol 61 pp 673ndash719 1992

[38] S P Bell ldquoThe origin recognition complex from simple originsto complex functionsrdquo Genes and Development vol 16 no 6pp 659ndash672 2002

[39] V L Marsh and S D Bell ldquoDNA replication and the cell cyclerdquoin Archaea Evolution Physiology and Molecular Biology R AGarrett and H P Klenk Eds Blackwell Publishing HobokenNJ USA 2007

[40] F Matsunaga A Glatigny M-H Mucchielli-Giorgi et alldquoGenomewide and biochemical analyses of DNA-binding activ-ity of Cdc6Orc1 and Mcm proteins in Pyrococcus sprdquo NucleicAcids Research vol 35 no 10 pp 3214ndash3222 2007

[41] J Liu C L Smith D DeRyckere K DeAngelis G S Martinand J M Berger ldquoStructure and function of Cdc6Cdc18implications for origin recognition and checkpoint controlrdquoMolecular Cell vol 6 no 3 pp 637ndash648 2000

[42] M R Singleton R Morales I Grainge N Cook M NIsupov and D B Wigley ldquoConformational changes inducedby nucleotide binding in Cdc6ORC from Aeropyrum pernixrdquoJournal of Molecular Biology vol 343 no 3 pp 547ndash557 2004

[43] Y Ishino and S Ishino ldquoRapid progress of DNA replicationstudies in Archaea the third domain of liferdquo Science China LifeSciences vol 55 no 5 pp 386ndash403 2012

[44] E L Hendrickson R Kaul Y Zhou et al ldquoComplete genomesequence of the genetically tractable hydrogenotrophic meth-anogen Methanococcus maripaludisrdquo Journal of Bacteriologyvol 186 no 20 pp 6956ndash6969 2004

[45] B K Tye ldquoMCM proteins in DNA replicationrdquo Annual Reviewof Biochemistry vol 68 pp 649ndash686 1999

[46] K Labib and J F X Diffley ldquoIs the MCM2-7 complex theeukaryotic DNA replication fork helicaserdquo Current Opinion inGenetics amp Development vol 11 no 1 pp 64ndash70 2001

[47] I Ilves T Petojevic J J Pesavento and M R Botchan ldquoActi-vation of the MCM2-7 helicase by association with Cdc45 andGINS proteinsrdquoMolecular Cell vol 37 no 2 pp 247ndash258 2010

[48] M L Bochman andA Schwacha ldquoTheMcm complex unwind-ing the mechanism of a replicative helicaserdquo Microbiology andMolecular Biology Reviews vol 73 no 4 pp 652ndash683 2009

[49] Y Ishimi ldquoADNAhelicase activity is associated with anMCM4-6 and -7 protein complexrdquoThe Journal of Biological Chemistryvol 272 no 39 pp 24508ndash24513 1997

[50] Z Kelman and M F White ldquoArchaeal DNA replication andrepairrdquo Current Opinion in Microbiology vol 8 no 6 pp 669ndash676 2005

[51] J H LeBowitz and R McMacken ldquoThe Escherichia coli dnaBreplication protein is a DNA helicaserdquoThe Journal of BiologicalChemistry vol 261 no 10 pp 4738ndash4748 1986

[52] Z Kelman J-K Lee and J Hurwitz ldquoThe single minichro-mosome maintenance protein ofMethanobacterium thermoau-totrophicum ΔH contains DNA helicase activityrdquo Proceedings ofthe National Academy of Sciences of the United States of Americavol 96 no 26 pp 14783ndash14788 1999

[53] D F Shechter C Y Ying and J Gautier ldquoThe intrinsic DNAhelicase activity of Methanobacterium thermoautotrophicumΔH minichromosome maintenance proteinrdquo The Journal ofBiological Chemistry vol 275 no 20 pp 15049ndash15059 2000

[54] M de Felice L Esposito B Pucci M de Falco M Rossi andF M Pisani ldquoA CDC6-like factor from the archaea Sulfolobussolfataricus promotes binding of the mini-chromosome main-tenance complex to DNArdquoThe Journal of Biological Chemistryvol 279 no 41 pp 43008ndash43012 2004

[55] R Kasiviswanathan J-H Shin and Z Kelman ldquoInteractionsbetween the archaeal Cdc6 and MCM proteins modulate theirbiochemical propertiesrdquo Nucleic Acids Research vol 33 no 15pp 4940ndash4950 2005

[56] J-H Shin B Grabowski R Kasiviswanathan S D Bell andZ Kelman ldquoRegulation of minichromosomemaintenance heli-case activity by Cdc6rdquo The Journal of Biological Chemistry vol278 no 39 pp 38059ndash38067 2003

[57] M Akita A Adachi K Takemura T Yamagami F Matsunagaand Y Ishino ldquoCdc6Orc1 from Pyrococcus furiosus may actas the origin recognition protein and Mcm helicase recruiterrdquoGenes to Cells vol 15 no 5 pp 537ndash552 2010

12 Archaea

[58] M Krupovic S Gribaldo D H Bamford and P Forterre ldquoTheevolutionary history of archaeal MCM helicases a case study ofvertical evolution combined with hitchhiking of mobile geneticelementsrdquo Molecular Biology and Evolution vol 27 no 12 pp2716ndash2732 2010

[59] ADWalters and J P J Chong ldquoAn archaeal orderwithmultipleminichromosome maintenance genesrdquo Microbiology vol 156part 5 pp 1405ndash1414 2010

[60] A DWalters and J P J Chong ldquoMethanococcusmaripaludis anarchaeon with multiple functional MCM proteinsrdquo Biochemi-cal Society Transactions vol 37 no 1 pp 1ndash6 2009

[61] Q Xia E L Hendrickson Y Zhang et al ldquoQuantitative pro-teomics of the archaeon Methanococcus maripaludis validatedbymicroarray analysis and real time PCRrdquoMolecularampCellularProteomics vol 5 no 5 pp 868ndash881 2006

[62] F Sarmiento J Mrazek and W B Whitman ldquoGenome-scaleanalysis of gene function in the hydrogenotrophic methano-genic archaeon Methanococcus maripaludisrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 110 no 12 pp 4726ndash4731 2013

[63] M Pan T J Santangelo Z Li J N Reeve and Z KelmanldquoThermococcus kodakarensis encodes threeMCMhomologs butonly one is essentialrdquo Nucleic Acids Research vol 39 no 22 pp9671ndash9680 2011

[64] S Ishino S Fujino H Tomita et al ldquoBiochemical and geneticalanalyses of the three mcm genes from the hyperthermophilicarchaeon Thermococcus kodakarensisrdquo Genes to Cells vol 16no 12 pp 1176ndash1189 2011

[65] K S Makarova Y I Wolf S L Mekhedov B G Mirkin and EV Koonin ldquoAncestral paralogs and pseudoparalogs and theirrole in the emergence of the eukaryotic cellrdquo Nucleic AcidsResearch vol 33 no 14 pp 4626ndash4638 2005

[66] N Marinsek E R Barry K S Makarova I Dionne E VKoonin and S D Bell ldquoGINS a central nexus in the archaealDNA replication forkrdquo EMBOReports vol 7 no 5 pp 539ndash5452006

[67] T Yoshimochi R Fujikane M Kawanami F Matsunaga and YIshino ldquoTheGINS complex from Pyrococcus furiosus stimulatesthe MCM helicase activityrdquoThe Journal of Biological Chemistryvol 283 no 3 pp 1601ndash1609 2008

[68] T Oyama S Ishino S Fujino et al ldquoArchitectures of archaealGINS complexes essential DNA replication initiation factorsrdquoBMC Biology vol 9 article 28 2011

[69] H Ogino S Ishino K Mayanagi et al ldquoThe GINS com-plex from the thermophilic archaeon Thermoplasma aci-dophilummay function as a homotetramer inDNA replicationrdquoExtremophiles vol 15 no 4 pp 529ndash539 2011

[70] L Sanchez-Pulido and C P Ponting ldquoCdc45 the missing recjortholog in eukaryotesrdquoBioinformatics vol 27 no 14 pp 1885ndash1888 2011

[71] Z Li T J Santangelo L Cubonova J N Reeve and Z KelmanldquoAffinity purification of an archaeal DNA replication proteinnetworkrdquomBio vol 1 no 5 2010

[72] Z Li M Pan T J Santangelo et al ldquoA novel DNA nucleaseis stimulated by association with the GINS complexrdquo NucleicAcids Research vol 39 no 14 pp 6114ndash6123 2011

[73] L A Rajman and S T Lovett ldquoA thermostable single-strandDNase from Methanococcus jannaschii related to the RecJrecombination and repair exonuclease from Escherichia colirdquoJournal of Bacteriology vol 182 no 3 pp 607ndash612 2000

[74] K RWilliams J B Murphy and JW Chase ldquoCharacterizationof the structural and functional defect in the Escherichia colisingle-stranded DNA binding protein encoded by the ssb-1 mutant gene Expression of the ssb-1 gene under 120582p(L)regulationrdquoThe Journal of Biological Chemistry vol 259 no 19pp 11804ndash11811 1984

[75] S Dąbrowski M Olszewski R Pitek and J Kur ldquoNovel ther-mostable ssDNA-binding proteins fromThermus thermophilusand T aquaticus-expression and purificationrdquo Protein Expres-sion and Purification vol 26 no 1 pp 131ndash138 2002

[76] C Iftode Y Daniely and J A Borowiec ldquoReplication proteinA (RPA) the eukaryotic SSBrdquo Critical Reviews in Biochemistryand Molecular Biology vol 34 no 3 pp 141ndash180 1999

[77] A G Murzin ldquoOB(oligonucleotideoligosaccharide binding)-fold common structural and functional solution for non-hom-ologous sequencesrdquo The EMBO Journal vol 12 no 3 pp 861ndash867 1993

[78] C A Haseltine and S C Kowalczykowski ldquoA distinctive single-stranded DNA-binding protein from the Archaeon Sulfolobussolfataricusrdquo Molecular Microbiology vol 43 no 6 pp 1505ndash1515 2002

[79] R I M Wadsworth and M F White ldquoIdentification and pro-perties of the crenarchaeal single-stranded DNA binding pro-tein from Sulfolobus solfataricusrdquoNucleic Acids Research vol 29no 4 pp 914ndash920 2001

[80] I D Kerr R I M Wadsworth L Cubeddu W Blankenfeldt JHNaismith andM FWhite ldquoInsights into ssDNA recognitionby the OB fold from a structural and thermodynamic study ofSulfolobus SSB proteinrdquo The EMBO Journal vol 22 no 11 pp2561ndash2570 2003

[81] X Luo U Schwarz-Linek C H Botting R Hensel B Siebersand M F White ldquoCC1 a novel crenarchaeal DNA binding pro-teinrdquo Journal of Bacteriology vol 189 no 2 pp 403ndash409 2007

[82] T J Kelly P Simancek and G S Brush ldquoIdentification andcharacterization of a single-stranded DNA-binding proteinfrom the archaeonMethanococcus jannaschiirdquoProceedings of theNational Academy of Sciences of theUnited States of America vol95 no 25 pp 14634ndash14639 1998

[83] Z Kelman S Pietrokovski and J Hurwitz ldquoIsolation and cha-racterization of a split B-type DNA polymerase from the arch-aeonMethanobacterium thermoautotrophicumΔHrdquoTheJournalof Biological Chemistry vol 274 no 40 pp 28751ndash28761 1999

[84] K Komori and Y Ishino ldquoReplication protein A in Pyrococcusfuriosus is involved in homologous DNA recombinationrdquo TheJournal of Biological Chemistry vol 276 no 28 pp 25654ndash25660 2001

[85] J B Robbins M C Murphy B A White R I Mackie THa and I K O Cann ldquoFunctional analysis of multiple single-stranded DNA-binding proteins from Methanosarcina acetivo-rans and their effects on DNA synthesis by DNA polymeraseBIrdquoThe Journal of Biological Chemistry vol 279 no 8 pp 6315ndash6326 2004

[86] Y Lin L-J Lin P Sriratana et al ldquoEngineering of functionalreplication protein a homologs based on insights into the evolu-tion of oligonucleotideoligosaccharide-binding foldsrdquo Journalof Bacteriology vol 190 no 17 pp 5766ndash5780 2008

[87] D N Frick and C C Richardson ldquoDNA primasesrdquo AnnualReview of Biochemistry vol 70 pp 39ndash80 2001

[88] G Desogus S Onesti P Brick M Rossi and F M PisanildquoIdentification and characterization of a DNA primase fromthe hyperthermophilic archaeon Methanococcus jannaschiirdquoNucleic Acids Research vol 27 no 22 pp 4444ndash4450 1999

Archaea 13

[89] A A Bocquier L Liu I K O Cann K Komori D Kohda andY Ishino ldquoArchaeal primase bridging the gap between RNAand DNA polymerasesrdquo Current Biology vol 11 no 6 pp 452ndash456 2001

[90] L Liu K Komori S Ishino et al ldquoThe archaeal DNA primasebiochemical characterization of the p41-p46 complex fromPyrococcus furiosusrdquo The Journal of Biological Chemistry vol276 no 48 pp 45484ndash45490 2001

[91] E Matsui M Nishio H Yokoyama K Harata S Darnisand I Matsui ldquoDistinct domain functions regulating de novoDNA synthesis of thermostable DNA primase from hyperther-mophile Pyrococcus horikoshiirdquo Biochemistry vol 42 no 50 pp14968ndash14976 2003

[92] N Ito I Matsui and EMatsui ldquoMolecular basis for the subunitassembly of the primase from an archaeon Pyrococcus hori-koshiirdquoThe FEBS Journal vol 274 no 5 pp 1340ndash1351 2007

[93] M le Breton G Henneke C Norais et al ldquoThe heterodimericprimase from the euryarchaeon Pyrococcus abyssi a multifunc-tional enzyme for initiation and repairrdquo Journal of MolecularBiology vol 374 no 5 pp 1172ndash1185 2007

[94] S-H Lao-Sirieix and S D Bell ldquoThe heterodimeric primaseof the hyperthermophilic archaeon Sulfolobus solfataricus pos-sesses DNA and RNA primase polymerase and 31015840-terminalnucleotidyl transferase activitiesrdquo Journal of Molecular Biologyvol 344 no 5 pp 1251ndash1263 2004

[95] S-H Lao-Sirieix L Pellegrini and S D Bell ldquoThe promiscuousprimaserdquo Trends in Genetics vol 21 no 10 pp 568ndash572 2005

[96] J Hu L Guo K Wu B Liu S Lang and L Huang ldquoTemplate-dependent polymerization across discontinuous templatesby the heterodimeric primase from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquoNucleic Acids Research vol 40no 8 pp 3470ndash3483 2012

[97] E Evguenieva-Hackenberg P Walter E Hochleitner FLottspeich and G Klug ldquoAn exosome-like complex in Sulfolo-bus solfataricusrdquo EMBOReports vol 4 no 9 pp 889ndash893 2003

[98] P Walter F Klein E Lorentzen A Ilchmann G Klug andE Evguenieva-Hackenberg ldquoCharacterization of native andreconstituted exosome complexes from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Microbiology vol62 no 4 pp 1076ndash1089 2006

[99] Z Zuo C J Rodgers A L Mikheikin and M A Trak-selis ldquoCharacterization of a functional DnaG-type primase inarchaea implications for a dual-primase systemrdquo Journal ofMolecular Biology vol 397 no 3 pp 664ndash676 2010

[100] B R Berquist P DasSarma and S DasSarma ldquoEssential andnon-essential DNA replication genes in the model halophilicArchaeon Halobacterium sp NRC-1rdquo BMC Genetics vol 8article 31 2007

[101] D K Braithwaite and J Ito ldquoCompilation alignment andphylogenetic relationships of DNA polymerasesrdquo Nucleic AcidsResearch vol 21 no 4 pp 787ndash802 1993

[102] I K O Cann and Y Ishino ldquoArchaeal DNA replication iden-tifying the pieces to solve a puzzlerdquo Genetics vol 152 no 4 pp1249ndash1267 1999

[103] G Lipps S Rother C Hart and G Krauss ldquoA novel typeof replicative enzyme harbouring ATpase primase and DNApolymerase activityrdquo The EMBO Journal vol 22 no 10 pp2516ndash2525 2003

[104] J Yamtich and J B Sweasy ldquoDNA polymerase family X func-tion structure and cellular rolesrdquoBiochimica et BiophysicaActavol 1804 no 5 pp 1136ndash1150 2010

[105] H Ohmori E C Friedberg R P P Fuchs et al ldquoThe Y-familyof DNA polymerasesrdquoMolecular Cell vol 8 no 1 pp 7ndash8 2001

[106] N Y Yao R E Georgescu J Finkelstein and M E OrsquoDonnellldquoSingle-molecule analysis reveals that the lagging strandincreases replisome processivity but slows replication forkprogressionrdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 106 no 32 pp 13236ndash132412009

[107] U Hubscher G Maga and S Spadari ldquoEukaryotic DNA poly-merasesrdquo Annual Review of Biochemistry vol 71 pp 133ndash1632002

[108] F Boudsocq S Iwai F Hanaoka and R Woodgate ldquoSulfolobussolfataricus P2 DNA polymerase IV (Dp04) an archaeal DinB-like DNA polymerase with lesion-bypass properties akin toeukaryotic pol120578rdquo Nucleic Acids Research vol 29 no 22 pp4607ndash4616 2001

[109] L-J Lin A Yoshinaga Y Lin et al ldquoMolecular analyses ofan unusual translesion DNA polymerase fromMethanosarcinaacetivorans C2Ardquo Journal of Molecular Biology vol 397 no 1pp 13ndash30 2010

[110] I K O Cann S Ishino NNomura Y Sako andY Ishino ldquoTwofamily B DNA polymerases from Aeropyrum pernix an aerobichyperthermophilic crenarchaeoterdquo Journal of Bacteriology vol181 no 19 pp 5984ndash5992 1999

[111] T Uemori Y Ishino H Doi and I Kato ldquoThe hyperther-mophilic archaeon Pyrodictium occultum has two 120572-like DNApolymerasesrdquo Journal of Bacteriology vol 177 no 8 pp 2164ndash2177 1995

[112] T Uemori Y Ishino H Toh K Asada and I Kato ldquoOrgani-zation and nucleotide sequence of the DNA polymerase genefrom the archaeon Pyrococcus furiosusrdquo Nucleic Acids Researchvol 21 no 2 pp 259ndash265 1993

[113] B A Connolly ldquoRecognition of deaminated bases by archaealfamily-B DNA polymerasesrdquo Biochemical Society Transactionsvol 37 no 1 pp 65ndash68 2009

[114] B A Connolly M J Fogg G Shuttleworth and B T WilsonldquoUracil recognition by archaeal family B DNA polymerasesrdquoBiochemical Society Transactions vol 31 no 3 pp 699ndash7022003

[115] T T Richardson X Wu B J Keith P Heslop A C Jones andB A Connolly ldquoUnwinding of primer-templates by archaealfamily-B DNA polymerases in response to template-stranduracilrdquo Nucleic Acids Research vol 41 no 4 pp 2466ndash24782013

[116] T Lindahl ldquoInstability and decay of the primary structure ofDNArdquo Nature vol 362 no 6422 pp 709ndash715 1993

[117] I B Rogozin K S Makarova Y I Pavlov and E V Koonin ldquoAhighly conserved family of inactivated archaeal B family DNApolymerasesrdquo Biology Direct vol 3 article 32 2008

[118] M Imamura T Uemori I Kato and Y Ishino ldquoA non-120572-like DNA polymerase from the hyperthermophilic archaeonPyrococcus furiosusrdquoBiological andPharmaceutical Bulletin vol18 no 12 pp 1647ndash1652 1995

[119] I K O Cann K Komori H Toh S Kanai and Y IshinoldquoA heterodimeric DNA polymerase evidence that members ofEuryarchaeota possess a distinct DNA polymeraserdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 95 no 24 pp 14250ndash14255 1998

[120] L Aravind D D Leipe and E V Koonin ldquoToprimmdasha con-served catalytic domain in type IA and II topoisomerases

14 Archaea

DnaG-type primases OLD family nucleases and RecR pro-teinsrdquo Nucleic Acids Research vol 26 no 18 pp 4205ndash42131998

[121] M Jokela A Eskelinen H Pospiech J Rouvinen and J ESyvaoja ldquoCharacterization of the 31015840 exonuclease subunit DP1of Methanococcus jannaschii replicative DNA polymerase DrdquoNucleic Acids Research vol 32 no 8 pp 2430ndash2440 2004

[122] T Uemori Y Sato I Kato H Doi and Y Ishino ldquoA novel DNApolymerase in the hyperthermophilic archaeon Pyrococcus fur-iosus gene cloning expression and characterizationrdquo Genes toCells vol 2 no 8 pp 499ndash512 1997

[123] Y Shen K Musti M Hiramoto H Kikuchi Y Kawarabayashiand I Matsui ldquoInvariant Asp-1122 and Asp-1124 are essentialresidues for polymerization catalysis of family D DNA poly-merase from Pyrococcus horikoshiirdquo The Journal of BiologicalChemistry vol 276 no 29 pp 27376ndash27383 2001

[124] G Henneke D Flament U Hubscher J Querellou and J-P Raffin ldquoThe hyperthermophilic euryarchaeota Pyrococcusabyssi likely requires the two DNA polymerases D and B forDNA replicationrdquo Journal of Molecular Biology vol 350 no 1pp 53ndash64 2005

[125] L Cubonova T Richardson B W Burkhart et al ldquoArchaealDNA polymerase D but not DNA polymerase B is required forgenome replication in Thermococcus kodakarensisrdquo Journal ofBacteriology vol 195 no 10 pp 2322ndash2328 2013

[126] C Rouillon G Henneke D Flament J Querellou and J-PRaffin ldquoDNA polymerase switching on homotrimeric PCNA atthe replication fork of the euryarchaea Pyrococcus abyssirdquo Jour-nal of Molecular Biology vol 369 no 2 pp 343ndash355 2007

[127] G Henneke ldquoIn vitro reconstitution of RNA primer removal inArchaea reveals the existence of two pathwaysrdquoTheBiochemicalJournal vol 447 no 2 pp 271ndash280 2012

[128] G-LMoldovan B Pfander and S Jentsch ldquoPCNA themaestroof the replication forkrdquo Cell vol 129 no 4 pp 665ndash679 2007

[129] X-P Kong R Onrust M OrsquoDonnell and J Kuriyan ldquoThree-dimensional structure of the 120573 subunit of E coli DNA poly-merase III holoenzyme a sliding DNA clamprdquo Cell vol 69 no3 pp 425ndash437 1992

[130] K Daimon Y Kawarabayasi H Kikuchi Y Sako and Y IshinoldquoThree proliferating cell nuclear antigen-like proteins foundin the hyperthermophilic archaeon Aeropyrum pemix interac-tions with the two DNA polymerasesrdquo Journal of Bacteriologyvol 184 no 3 pp 687ndash694 2002

[131] I Dionne R K Nookala S P Jackson A J Doherty andS D Bell ldquoA heterotrimeric PCNA in the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Cell vol 11 no 1pp 275ndash282 2003

[132] E Warbrick ldquoPCNA binding through a conserved motifrdquoBioEssays vol 20 no 3 pp 195ndash199 1998

[133] H Nishida K Mayanagi S Kiyonari et al ldquoStructural deter-minant for switching between the polymerase and exonucleasemodes in the PCNA-replicative DNA polymerase complexrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 106 no 49 pp 20693ndash20698 2009

[134] K Mayanagi S Kiyonari H Nishida et al ldquoArchitecture of theDNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complexrdquo Proceedings of the National Academy ofSciences of the United States of America vol 108 no 5 pp 1845ndash1849 2011

[135] B Castrec C Rouillon G Henneke D Flament J Querellouand J-P Raffin ldquoBinding to PCNA in Euryarchaeal DNA

replication requires two PIP motifs for DNA polymerase D andone PIP motif for DNA polymerase Brdquo Journal of MolecularBiology vol 394 no 2 pp 209ndash218 2009

[136] P F Pluchon T Fouqueau C Creze et al ldquoAn extendednetworkof genomic maintenance in the archaeon Pyrococcus abyssihighlights unexpected associations between eucaryotic homo-logsrdquo PLoS One vol 8 no 11 Article ID e79707 2013

[137] J E Ladner M Pan J Hurwitz and Z Kelman ldquoCrystalstructures of two active proliferating cell nuclear antigens(PCNAs) encoded byThermococcus kodakaraensisrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2711ndash2716 2011

[138] Y Kuba S Ishino T Yamagami et al ldquoComparative analyses ofthe two proliferating cell nuclear antigens from the hyperther-mophilic archaeonThermococcus kodakarensisrdquo Genes to Cellsvol 17 no 11 pp 923ndash937 2012

[139] T Fukui H Atomi T Kanai R Matsumi S Fujiwara andT Imanaka ldquoComplete genome sequence of the hyperther-mophilic archaeon Thermococcus kodakaraensis KOD1 andcomparison with Pyrococcus genomesrdquo Genome Research vol15 no 3 pp 352ndash363 2005

[140] D Jeruzalmi O Yurieva Y Zhao et al ldquoMechanism of proces-sivity clamp opening by the delta subunit wrench of the clamploader complex of E coliDNApolymerase IIIrdquoCell vol 106 no4 pp 417ndash428 2001

[141] Y Shiomi J Usukura Y Masamura et al ldquoATP-dependentstructural change of the eukaryotic clamp-loader protein repli-cation factor Crdquo Proceedings of the National Academy of Sciencesof the United States of America vol 97 no 26 pp 14127ndash141322000

[142] T Miyata T Oyama K Mayanagi S Ishino Y Ishino and KMorikawa ldquoThe clamp-loading complex for processive DNAreplicationrdquoNature Structural andMolecular Biology vol 11 no7 pp 632ndash636 2004

[143] T Oyama Y Ishino I K O Cann S Ishino and K MorikawaldquoAtomic structure of the clamp loader small subunit fromPyrococcus furiosusrdquo Molecular Cell vol 8 no 2 pp 455ndash4632001

[144] A Seybert D J Scott S Scaife M R Singleton and DB Wigley ldquoBiochemical characterisation of the clampclamploader proteins from the euryarchaeon Archaeoglobus fulgidusrdquoNucleic Acids Research vol 30 no 20 pp 4329ndash4338 2002

[145] Y-H Chen Y Lin A Yoshinaga et al ldquoMolecular analyses of athree-subunit euryarchaeal clamp loader complex from Meth-anosarcina acetivoransrdquo Journal of Bacteriology vol 191 no 21pp 6539ndash6549 2009

[146] Y-H Chen S A Kocherginskaya Y Lin et al ldquoBiochemicaland mutational analyses of a unique clamp loader complex inthe archaeon Methanosarcina acetivoransrdquo The Journal of Bio-logical Chemistry vol 280 no 51 pp 41852ndash41863 2005

[147] F Matsunaga C Norais P Forterre and H Myllykallio ldquoIden-tification of short ldquoeukaryoticrdquo Okazaki fragments synthesizedfrom a prokaryotic replication originrdquo EMBO Reports vol 4no 2 pp 154ndash158 2003

[148] H Kochiwa M Tomita and A Kanai ldquoEvolution of ribonucle-ase H genes in prokaryotes to avoid inheritance of redundantgenesrdquo BMC Evolutionary Biology vol 7 article 128 2007

[149] N OhtaniMHarukiMMorikawa and S Kanaya ldquoMoleculardiversities of RNases Hrdquo Journal of Bioscience and Bioengineer-ing vol 88 no 1 pp 12ndash19 1999

Archaea 15

[150] N Ohtani M Haruki M Morikawa R J Crouch M Itayaand S Kanaya ldquoIdentification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII fromBacillus subtilis classification of RNases H into three familiesrdquoBiochemistry vol 38 no 2 pp 605ndash618 1999

[151] N Ohtani H Yanagawa M Tomita and M Itaya ldquoIdentifi-cation of the first archaeal type 1 RNase H gene from Halobac-terium sp NRC-1 archaeal RNase HI can cleave an RNA-DNAjunctionrdquoThe Biochemical Journal vol 381 no 3 pp 795ndash8022004

[152] N Ohtani H Yanagawa M Tomita and M Itaya ldquoCleavage ofdouble-stranded RNA by RNase HI from a thermoacidophilicarchaeon Sulfolobus tokodaii 7rdquo Nucleic Acids Research vol 32no 19 pp 5809ndash5819 2004

[153] M A Nowak M C Boerlijst J Cooke and J M SmithldquoEvolution of genetic redundancyrdquo Nature vol 388 no 6638pp 167ndash170 1997

[154] A E Tomkinson S Vijayakumar J M Pascal and T Ellen-berger ldquoDNA ligases structure reactionmechanism and func-tionrdquo Chemical Reviews vol 106 no 2 pp 687ndash699 2006

[155] M Nakatani S Ezaki H Atomi and T Imanaka ldquoA DNAligase from a hyperthermophilic archaeon with unique cofactorspecificityrdquo Journal of Bacteriology vol 182 no 22 pp 6424ndash6433 2000

[156] Y Sun M S Seo J H Kim et al ldquoNovel DNA ligase with broadnucleotide cofactor specificity from the hyperthermophilic cre-narchaeon Sulfophobococcus zilligii influence of ancestral DNAligase on cofactor utilizationrdquo Environmental Microbiology vol10 no 12 pp 3212ndash3224 2008

[157] T R Beattie and S D Bell ldquoCoordination of multiple enzymeactivities by a single PCNA in archaeal Okazaki fragmentmaturationrdquo The EMBO Journal vol 31 no 6 pp 1556ndash15672012

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Archaea 9

Table1DNAreplicationproteins

andfeatures

inthed

omains

BacteriaEukaryotaand

thetwomajor

phylao

fthe

Archaeado

main

Mod

ified

from

[43]

DNAreplicationstage

Process

Bacteria

Eukaryota

Archaea

Crenarchaeota

Euryarchaeota

Preinitia

tion

Orig

inof

replication

Sing

leMultip

leMultip

leSing

lea

Orig

inrecogn

ition

DnaA

ORC

complex

(ORC

1-6)

Orc1C

dc6

Orc1C

dc6b

Initiation

DNAun

winding

(Helicase)

DnaB

MCM

complex

(MCM

2-7)

MCM

complex

MCM

complex

DNAun

winding

(Accessory

proteins)

DnaC

Cdc6

GIN

S23GIN

S15

GIN

S15c

Cdt1

GIN

Scomplex

(Sld5Psf1-3)

RecJho

molog

RecJho

molog

Cdc45

Prim

ersynthesis

DnaG

Pol120572

prim

asec

omplex

DNAprim

ase

(PriS

L)D

naG

dDNAprim

ase(PriSL)

Elon

gatio

n

DNAsynthesis

(polym

erase)

PolIII(Fam

ilyCDNApo

lymerase)

Pol120575and

Pol120576(Fam

ilyBDNA

polymerase)

Family

BDNApo

lymerase

Family

DDNA

polymerasee

DNAsynthesis

(Processivity

factors)

120574-com

plex

(clamploader)

RFC(clamploader)

RFC(clamploader)

RFC(clamploader)

120573-clamp(clamp)

PCNA(clamp)

PCNA(clamp)

PCNA(clamp)

Maturation

Maturation(O

kazaki

fragmentp

rocessing)

PolI

(family

ADNApo

lymerase)

Fen1D

na2

Fen1

Fen1

RNaseH

RNaseH

RNaseH

RNaseH

DNAligase

DNAligase

DNAligase

DNAligase

a Exceptio

ntheo

rder

Halobacteria

les

b Not

know

nform

embersof

theE

uryarchaeota

ordersMethanococcalesandMethanopyrales

c GIN

S23hasb

eenfoun

dedon

lyin

theo

rder

Thermococcales

oftheE

uryarchaeota

d Sulfolobu

ssolfataric

usdidshow

prim

asea

ctivity

invitro

e Fam

ilyBDNApo

lymeraseisa

lsoessentialinHalobacteriu

mB

ecause

itsfunctio

nhasn

otbeen

clearlyelu

cidateditmight

also

play

aroleinreplicationin

thisandclo

selyrelated

organism

s

10 Archaea

interact with other unknown initiation enzymes resultingin a complex phylogeny of the MCM homologs [49] Pre-sumably these differences also account for the inability torecognize the origin of replication in these microorganismsThis unique scenario for initiation of DNA replicationmay bea direct consequence of various processes such as duplicationmobile genetic elements and interactions with viruses [58]

The differences in DNA replication among archaealhigher taxa demonstrate an unexpected variability and sug-gest two alternative evolutionary models In the first modelDNA replication evolved late after the diversification ofthe archaeal lineages Because the replicative system wasnot fully formed it was possible to develop differentlybetween the lineages Once formed replication would thenbe highly conserved However this model is not consistentwith differences observed between lineages that must haveformed relatively late such as those between the orders oreven in some cases within certain orders The alternativemodel is that DNA replication has changed throughout theevolution of the archaea Thus differences in the replicativesystems may represent ancient as well as modern adaptationsto changing environments In this case differences in thereplicative systems may provide important insights into theevolutionary pressures in play during different episodes ofarchaeal evolution From this perspective the differencesbetween the eukaryotic and archaeal replicative systems maynot be evidence for an ancient origin of the eukaryotesInstead it is entirely plausible that the replicative system ineukaryotes could have evolved relatively late from a well-developed archaeal system

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] E F DeLong and N R Pace ldquoEnvironmental diversity ofbacteria and archaeardquo Systematic Biology vol 50 no 4 pp 470ndash478 2001

[2] B Chaban S Y M Ng and K F Jarrell ldquoArchaeal habitatsmdashfrom the extreme to the ordinaryrdquo Canadian Journal of Micro-biology vol 52 no 2 pp 73ndash116 2006

[3] M J Hanford and T L Peeples ldquoArchaeal tetraether lipidsunique structures and applicationsrdquo Applied Biochemistry andBiotechnology A vol 97 no 1 pp 45ndash62 2002

[4] K Sandman and J N Reeve ldquoArchaeal histones and the originof the histone foldrdquo Current Opinion in Microbiology vol 9 no5 pp 520ndash525 2006

[5] O Lecompte R Ripp J-C Thierry D Moras and O PochldquoComparative analysis of ribosomal proteins in complete gen-omes an example of reductive evolution at the domain scalerdquoNucleic Acids Research vol 30 no 24 pp 5382ndash5390 2002

[6] D R Edgell and W F Doolittle ldquoArchaea and the origin(s) ofDNA rplication poteinsrdquo Cell vol 89 no 7 pp 995ndash998 1997

[7] E R Barry and S D Bell ldquoDNA replication in the archaeardquoMicrobiology and Molecular Biology Reviews vol 70 no 4 pp876ndash887 2006

[8] S Gribaldo and C Brochier-Armanet ldquoThe origin and evolu-tion of archaea a state of the artrdquo Philosophical Transactions ofthe Royal Society B vol 361 no 1470 pp 1007ndash1022 2006

[9] P Londei ldquoEvolution of translational initiation new insightsfrom the archaeardquo FEMS Microbiology Reviews vol 29 no 2pp 185ndash200 2005

[10] B Grabowski and Z Kelman ldquoArchaeal DNA replicationeukaryal proteins in a bacterial contextrdquo Annual Review ofMicrobiology vol 57 pp 487ndash516 2003

[11] P Forterre J Filee and H Myllykallio ldquoOrigin and evolutionof DNA and DNA replication machineriesrdquo in The GeneticCode and the Origin of Life L Ribas Ed Landes BioscienceGeorgetown Tex USA 2007

[12] E V Koonin ldquoThe origin and early evolution of eukaryotesin the light of phylogenomicsrdquo Genome Biology vol 11 no 5article 209 2010

[13] M Konneke A E Bernhard J R de la Torre C B WalkerJ B Waterbury and D A Stahl ldquoIsolation of an autotrophicammonia-oxidizing marine archaeonrdquo Nature vol 437 no7058 pp 543ndash546 2005

[14] C Brochier-Armanet B Boussau S Gribaldo and P ForterreldquoMesophilic crenarchaeota proposal for a third archaeal phy-lum theThaumarchaeotardquoNature Reviews Microbiology vol 6no 3 pp 245ndash252 2008

[15] J G Elkins M Podar D E Graham et al ldquoA korarchaealgenome reveals insights into the evolution of the ArchaeardquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 105 no 23 pp 8102ndash8107 2008

[16] T Nunoura Y Takaki J Kakuta et al ldquoInsights into theevolution of Archaea and eukaryotic protein modifier systemsrevealed by the genome of a novel archaeal grouprdquoNucleic AcidsResearch vol 39 no 8 pp 3204ndash3223 2011

[17] HHuberM J Hohn R Rachel T Fuchs V CWimmer andKO Stetter ldquoAnewphylumofArchaea represented by a nanosizedhyperthermophilic symbiontrdquoNature vol 417 no 6884 pp 63ndash67 2002

[18] C Brochier S Gribaldo Y Zivanovic F Confalonieri and PForterre ldquoNanoarchaea representatives of a novel archaeal phy-lum or a fast-evolving euryarchaeal lineage related to Therm-ococcalesrdquo Genome Biology vol 6 no 5 article R42 2005

[19] S J Aves ldquoDNA replication initiationrdquo Methods in MolecularBiology vol 521 pp 3ndash17 2009

[20] N P Robinson I Dionne M Lundgren V L Marsh RBernander and S D Bell ldquoIdentification of two origins ofreplication in the single chromosome of the archaeon Sulfolobussolfataricusrdquo Cell vol 116 no 1 pp 25ndash38 2004

[21] M Lundgren A Andersson L Chen P Nilsson and RBernander ldquoThree replication origins in Sulfolobus speciessynchronous initiation of chromosome replication and asyn-chronous terminationrdquo Proceedings of the National Academy ofSciences of theUnited States of America vol 101 no 18 pp 7046ndash7051 2004

[22] N P Robinson and S D Bell ldquoExtrachromosomal element cap-ture and the evolution ofmultiple replication origins in archaealchromosomesrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 104 no 14 pp 5806ndash58112007

[23] E A Pelve A C Lindas A Knoppel A Mira and R Bernan-der ldquoFour chromosome replication origins in the archaeonPyrobaculum calidifontisrdquo Molecular Microbiology vol 85 no5 pp 986ndash995 2012

Archaea 11

[24] A F Andersson E A Pelve S LindebergM Lundgren P Nils-son and R Bernander ldquoReplication-biased genome organisa-tion in the crenarchaeon Sulfolobusrdquo BMCGenomics vol 11 no1 article 454 2010

[25] H Myllykallio P Lopez P Lopez-Garcıa et al ldquoBacterial modeof replication with eukaryotic-like machinery in a hyperther-mophilic archaeonrdquo Science vol 288 no 5474 pp 2212ndash22152000

[26] F Matsunaga P Forterre Y Ishino and H Myllykallio ldquoInvivo interactions of archaeal Cdc6Orc1 and minichromosomemaintenance proteins with the replication originrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 98 no 20 pp 11152ndash11157 2001

[27] S Maisnier-Patin L Malandrin N K Birkeland and RBernander ldquoChromosome replication patterns in the hyper-thermophilic euryarchaeaArchaeoglobus fulgidus andMethano-caldococcus (Methanococcus) jannaschiirdquo Molecular Microbiol-ogy vol 45 no 5 pp 1443ndash1450 2002

[28] R Zhang and C-T Zhang ldquoMultiple replication origins ofthe archaeon Halobacterium species NRC-1rdquo Biochemical andBiophysical Research Communications vol 302 no 4 pp 728ndash734 2003

[29] C Norais M Hawkins A L Hartman J A Eisen H Myl-lykallio and T Allers ldquoGenetic and physical mapping of DNAreplication origins in Haloferax volcaniirdquo PLoS Genetics vol 3no 5 article e77 2007

[30] J A Coker P DasSarma M Capes et al ldquoMultiple replicationorigins of Halobacterium sp strain NRC-1 properties of theconserved orc7-dependent oriC1rdquo Journal of Bacteriology vol191 no 16 pp 5253ndash5261 2009

[31] Z Wu J Liu H Yang H Liu and H Xiang ldquoMultiple repli-cation origins with diverse control mechanisms in Haloarculahispanicardquo Nucleic Acids Research 2013

[32] M Hawkins S Malla M J Blythe C A Nieduszynski and TAllers ldquoAccelerated growth in the absence of DNA replicationoriginsrdquo Nature vol 503 no 7477 pp 544ndash547 2013

[33] A I Majernık and J P J Chong ldquoA conserved mechanismfor replication origin recognition and binding in archaeardquo TheBiochemical Journal vol 409 no 2 pp 511ndash518 2008

[34] J E Galagan C Nusbaum A Roy et al ldquoThe genome of Macetivorans reveals extensive metabolic and physiological diver-sityrdquo Genome Research vol 12 no 4 pp 532ndash542 2002

[35] R Zhang and C-T Zhang ldquoIdentification of replication originsin archaeal genomes based on the Z-curve methodrdquo Archaeavol 1 no 5 pp 335ndash346 2005

[36] A Spang R Hatzenpichler C Brochier-Armanet et al ldquoDis-tinct gene set in two different lineages of ammonia-oxidizingarchaea supports the phylum Thaumarchaeotardquo Trends inMicrobiology vol 18 no 8 pp 331ndash340 2010

[37] K J Marians ldquoProkaryotic DNA replicationrdquo Annual Review ofBiochemistry vol 61 pp 673ndash719 1992

[38] S P Bell ldquoThe origin recognition complex from simple originsto complex functionsrdquo Genes and Development vol 16 no 6pp 659ndash672 2002

[39] V L Marsh and S D Bell ldquoDNA replication and the cell cyclerdquoin Archaea Evolution Physiology and Molecular Biology R AGarrett and H P Klenk Eds Blackwell Publishing HobokenNJ USA 2007

[40] F Matsunaga A Glatigny M-H Mucchielli-Giorgi et alldquoGenomewide and biochemical analyses of DNA-binding activ-ity of Cdc6Orc1 and Mcm proteins in Pyrococcus sprdquo NucleicAcids Research vol 35 no 10 pp 3214ndash3222 2007

[41] J Liu C L Smith D DeRyckere K DeAngelis G S Martinand J M Berger ldquoStructure and function of Cdc6Cdc18implications for origin recognition and checkpoint controlrdquoMolecular Cell vol 6 no 3 pp 637ndash648 2000

[42] M R Singleton R Morales I Grainge N Cook M NIsupov and D B Wigley ldquoConformational changes inducedby nucleotide binding in Cdc6ORC from Aeropyrum pernixrdquoJournal of Molecular Biology vol 343 no 3 pp 547ndash557 2004

[43] Y Ishino and S Ishino ldquoRapid progress of DNA replicationstudies in Archaea the third domain of liferdquo Science China LifeSciences vol 55 no 5 pp 386ndash403 2012

[44] E L Hendrickson R Kaul Y Zhou et al ldquoComplete genomesequence of the genetically tractable hydrogenotrophic meth-anogen Methanococcus maripaludisrdquo Journal of Bacteriologyvol 186 no 20 pp 6956ndash6969 2004

[45] B K Tye ldquoMCM proteins in DNA replicationrdquo Annual Reviewof Biochemistry vol 68 pp 649ndash686 1999

[46] K Labib and J F X Diffley ldquoIs the MCM2-7 complex theeukaryotic DNA replication fork helicaserdquo Current Opinion inGenetics amp Development vol 11 no 1 pp 64ndash70 2001

[47] I Ilves T Petojevic J J Pesavento and M R Botchan ldquoActi-vation of the MCM2-7 helicase by association with Cdc45 andGINS proteinsrdquoMolecular Cell vol 37 no 2 pp 247ndash258 2010

[48] M L Bochman andA Schwacha ldquoTheMcm complex unwind-ing the mechanism of a replicative helicaserdquo Microbiology andMolecular Biology Reviews vol 73 no 4 pp 652ndash683 2009

[49] Y Ishimi ldquoADNAhelicase activity is associated with anMCM4-6 and -7 protein complexrdquoThe Journal of Biological Chemistryvol 272 no 39 pp 24508ndash24513 1997

[50] Z Kelman and M F White ldquoArchaeal DNA replication andrepairrdquo Current Opinion in Microbiology vol 8 no 6 pp 669ndash676 2005

[51] J H LeBowitz and R McMacken ldquoThe Escherichia coli dnaBreplication protein is a DNA helicaserdquoThe Journal of BiologicalChemistry vol 261 no 10 pp 4738ndash4748 1986

[52] Z Kelman J-K Lee and J Hurwitz ldquoThe single minichro-mosome maintenance protein ofMethanobacterium thermoau-totrophicum ΔH contains DNA helicase activityrdquo Proceedings ofthe National Academy of Sciences of the United States of Americavol 96 no 26 pp 14783ndash14788 1999

[53] D F Shechter C Y Ying and J Gautier ldquoThe intrinsic DNAhelicase activity of Methanobacterium thermoautotrophicumΔH minichromosome maintenance proteinrdquo The Journal ofBiological Chemistry vol 275 no 20 pp 15049ndash15059 2000

[54] M de Felice L Esposito B Pucci M de Falco M Rossi andF M Pisani ldquoA CDC6-like factor from the archaea Sulfolobussolfataricus promotes binding of the mini-chromosome main-tenance complex to DNArdquoThe Journal of Biological Chemistryvol 279 no 41 pp 43008ndash43012 2004

[55] R Kasiviswanathan J-H Shin and Z Kelman ldquoInteractionsbetween the archaeal Cdc6 and MCM proteins modulate theirbiochemical propertiesrdquo Nucleic Acids Research vol 33 no 15pp 4940ndash4950 2005

[56] J-H Shin B Grabowski R Kasiviswanathan S D Bell andZ Kelman ldquoRegulation of minichromosomemaintenance heli-case activity by Cdc6rdquo The Journal of Biological Chemistry vol278 no 39 pp 38059ndash38067 2003

[57] M Akita A Adachi K Takemura T Yamagami F Matsunagaand Y Ishino ldquoCdc6Orc1 from Pyrococcus furiosus may actas the origin recognition protein and Mcm helicase recruiterrdquoGenes to Cells vol 15 no 5 pp 537ndash552 2010

12 Archaea

[58] M Krupovic S Gribaldo D H Bamford and P Forterre ldquoTheevolutionary history of archaeal MCM helicases a case study ofvertical evolution combined with hitchhiking of mobile geneticelementsrdquo Molecular Biology and Evolution vol 27 no 12 pp2716ndash2732 2010

[59] ADWalters and J P J Chong ldquoAn archaeal orderwithmultipleminichromosome maintenance genesrdquo Microbiology vol 156part 5 pp 1405ndash1414 2010

[60] A DWalters and J P J Chong ldquoMethanococcusmaripaludis anarchaeon with multiple functional MCM proteinsrdquo Biochemi-cal Society Transactions vol 37 no 1 pp 1ndash6 2009

[61] Q Xia E L Hendrickson Y Zhang et al ldquoQuantitative pro-teomics of the archaeon Methanococcus maripaludis validatedbymicroarray analysis and real time PCRrdquoMolecularampCellularProteomics vol 5 no 5 pp 868ndash881 2006

[62] F Sarmiento J Mrazek and W B Whitman ldquoGenome-scaleanalysis of gene function in the hydrogenotrophic methano-genic archaeon Methanococcus maripaludisrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 110 no 12 pp 4726ndash4731 2013

[63] M Pan T J Santangelo Z Li J N Reeve and Z KelmanldquoThermococcus kodakarensis encodes threeMCMhomologs butonly one is essentialrdquo Nucleic Acids Research vol 39 no 22 pp9671ndash9680 2011

[64] S Ishino S Fujino H Tomita et al ldquoBiochemical and geneticalanalyses of the three mcm genes from the hyperthermophilicarchaeon Thermococcus kodakarensisrdquo Genes to Cells vol 16no 12 pp 1176ndash1189 2011

[65] K S Makarova Y I Wolf S L Mekhedov B G Mirkin and EV Koonin ldquoAncestral paralogs and pseudoparalogs and theirrole in the emergence of the eukaryotic cellrdquo Nucleic AcidsResearch vol 33 no 14 pp 4626ndash4638 2005

[66] N Marinsek E R Barry K S Makarova I Dionne E VKoonin and S D Bell ldquoGINS a central nexus in the archaealDNA replication forkrdquo EMBOReports vol 7 no 5 pp 539ndash5452006

[67] T Yoshimochi R Fujikane M Kawanami F Matsunaga and YIshino ldquoTheGINS complex from Pyrococcus furiosus stimulatesthe MCM helicase activityrdquoThe Journal of Biological Chemistryvol 283 no 3 pp 1601ndash1609 2008

[68] T Oyama S Ishino S Fujino et al ldquoArchitectures of archaealGINS complexes essential DNA replication initiation factorsrdquoBMC Biology vol 9 article 28 2011

[69] H Ogino S Ishino K Mayanagi et al ldquoThe GINS com-plex from the thermophilic archaeon Thermoplasma aci-dophilummay function as a homotetramer inDNA replicationrdquoExtremophiles vol 15 no 4 pp 529ndash539 2011

[70] L Sanchez-Pulido and C P Ponting ldquoCdc45 the missing recjortholog in eukaryotesrdquoBioinformatics vol 27 no 14 pp 1885ndash1888 2011

[71] Z Li T J Santangelo L Cubonova J N Reeve and Z KelmanldquoAffinity purification of an archaeal DNA replication proteinnetworkrdquomBio vol 1 no 5 2010

[72] Z Li M Pan T J Santangelo et al ldquoA novel DNA nucleaseis stimulated by association with the GINS complexrdquo NucleicAcids Research vol 39 no 14 pp 6114ndash6123 2011

[73] L A Rajman and S T Lovett ldquoA thermostable single-strandDNase from Methanococcus jannaschii related to the RecJrecombination and repair exonuclease from Escherichia colirdquoJournal of Bacteriology vol 182 no 3 pp 607ndash612 2000

[74] K RWilliams J B Murphy and JW Chase ldquoCharacterizationof the structural and functional defect in the Escherichia colisingle-stranded DNA binding protein encoded by the ssb-1 mutant gene Expression of the ssb-1 gene under 120582p(L)regulationrdquoThe Journal of Biological Chemistry vol 259 no 19pp 11804ndash11811 1984

[75] S Dąbrowski M Olszewski R Pitek and J Kur ldquoNovel ther-mostable ssDNA-binding proteins fromThermus thermophilusand T aquaticus-expression and purificationrdquo Protein Expres-sion and Purification vol 26 no 1 pp 131ndash138 2002

[76] C Iftode Y Daniely and J A Borowiec ldquoReplication proteinA (RPA) the eukaryotic SSBrdquo Critical Reviews in Biochemistryand Molecular Biology vol 34 no 3 pp 141ndash180 1999

[77] A G Murzin ldquoOB(oligonucleotideoligosaccharide binding)-fold common structural and functional solution for non-hom-ologous sequencesrdquo The EMBO Journal vol 12 no 3 pp 861ndash867 1993

[78] C A Haseltine and S C Kowalczykowski ldquoA distinctive single-stranded DNA-binding protein from the Archaeon Sulfolobussolfataricusrdquo Molecular Microbiology vol 43 no 6 pp 1505ndash1515 2002

[79] R I M Wadsworth and M F White ldquoIdentification and pro-perties of the crenarchaeal single-stranded DNA binding pro-tein from Sulfolobus solfataricusrdquoNucleic Acids Research vol 29no 4 pp 914ndash920 2001

[80] I D Kerr R I M Wadsworth L Cubeddu W Blankenfeldt JHNaismith andM FWhite ldquoInsights into ssDNA recognitionby the OB fold from a structural and thermodynamic study ofSulfolobus SSB proteinrdquo The EMBO Journal vol 22 no 11 pp2561ndash2570 2003

[81] X Luo U Schwarz-Linek C H Botting R Hensel B Siebersand M F White ldquoCC1 a novel crenarchaeal DNA binding pro-teinrdquo Journal of Bacteriology vol 189 no 2 pp 403ndash409 2007

[82] T J Kelly P Simancek and G S Brush ldquoIdentification andcharacterization of a single-stranded DNA-binding proteinfrom the archaeonMethanococcus jannaschiirdquoProceedings of theNational Academy of Sciences of theUnited States of America vol95 no 25 pp 14634ndash14639 1998

[83] Z Kelman S Pietrokovski and J Hurwitz ldquoIsolation and cha-racterization of a split B-type DNA polymerase from the arch-aeonMethanobacterium thermoautotrophicumΔHrdquoTheJournalof Biological Chemistry vol 274 no 40 pp 28751ndash28761 1999

[84] K Komori and Y Ishino ldquoReplication protein A in Pyrococcusfuriosus is involved in homologous DNA recombinationrdquo TheJournal of Biological Chemistry vol 276 no 28 pp 25654ndash25660 2001

[85] J B Robbins M C Murphy B A White R I Mackie THa and I K O Cann ldquoFunctional analysis of multiple single-stranded DNA-binding proteins from Methanosarcina acetivo-rans and their effects on DNA synthesis by DNA polymeraseBIrdquoThe Journal of Biological Chemistry vol 279 no 8 pp 6315ndash6326 2004

[86] Y Lin L-J Lin P Sriratana et al ldquoEngineering of functionalreplication protein a homologs based on insights into the evolu-tion of oligonucleotideoligosaccharide-binding foldsrdquo Journalof Bacteriology vol 190 no 17 pp 5766ndash5780 2008

[87] D N Frick and C C Richardson ldquoDNA primasesrdquo AnnualReview of Biochemistry vol 70 pp 39ndash80 2001

[88] G Desogus S Onesti P Brick M Rossi and F M PisanildquoIdentification and characterization of a DNA primase fromthe hyperthermophilic archaeon Methanococcus jannaschiirdquoNucleic Acids Research vol 27 no 22 pp 4444ndash4450 1999

Archaea 13

[89] A A Bocquier L Liu I K O Cann K Komori D Kohda andY Ishino ldquoArchaeal primase bridging the gap between RNAand DNA polymerasesrdquo Current Biology vol 11 no 6 pp 452ndash456 2001

[90] L Liu K Komori S Ishino et al ldquoThe archaeal DNA primasebiochemical characterization of the p41-p46 complex fromPyrococcus furiosusrdquo The Journal of Biological Chemistry vol276 no 48 pp 45484ndash45490 2001

[91] E Matsui M Nishio H Yokoyama K Harata S Darnisand I Matsui ldquoDistinct domain functions regulating de novoDNA synthesis of thermostable DNA primase from hyperther-mophile Pyrococcus horikoshiirdquo Biochemistry vol 42 no 50 pp14968ndash14976 2003

[92] N Ito I Matsui and EMatsui ldquoMolecular basis for the subunitassembly of the primase from an archaeon Pyrococcus hori-koshiirdquoThe FEBS Journal vol 274 no 5 pp 1340ndash1351 2007

[93] M le Breton G Henneke C Norais et al ldquoThe heterodimericprimase from the euryarchaeon Pyrococcus abyssi a multifunc-tional enzyme for initiation and repairrdquo Journal of MolecularBiology vol 374 no 5 pp 1172ndash1185 2007

[94] S-H Lao-Sirieix and S D Bell ldquoThe heterodimeric primaseof the hyperthermophilic archaeon Sulfolobus solfataricus pos-sesses DNA and RNA primase polymerase and 31015840-terminalnucleotidyl transferase activitiesrdquo Journal of Molecular Biologyvol 344 no 5 pp 1251ndash1263 2004

[95] S-H Lao-Sirieix L Pellegrini and S D Bell ldquoThe promiscuousprimaserdquo Trends in Genetics vol 21 no 10 pp 568ndash572 2005

[96] J Hu L Guo K Wu B Liu S Lang and L Huang ldquoTemplate-dependent polymerization across discontinuous templatesby the heterodimeric primase from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquoNucleic Acids Research vol 40no 8 pp 3470ndash3483 2012

[97] E Evguenieva-Hackenberg P Walter E Hochleitner FLottspeich and G Klug ldquoAn exosome-like complex in Sulfolo-bus solfataricusrdquo EMBOReports vol 4 no 9 pp 889ndash893 2003

[98] P Walter F Klein E Lorentzen A Ilchmann G Klug andE Evguenieva-Hackenberg ldquoCharacterization of native andreconstituted exosome complexes from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Microbiology vol62 no 4 pp 1076ndash1089 2006

[99] Z Zuo C J Rodgers A L Mikheikin and M A Trak-selis ldquoCharacterization of a functional DnaG-type primase inarchaea implications for a dual-primase systemrdquo Journal ofMolecular Biology vol 397 no 3 pp 664ndash676 2010

[100] B R Berquist P DasSarma and S DasSarma ldquoEssential andnon-essential DNA replication genes in the model halophilicArchaeon Halobacterium sp NRC-1rdquo BMC Genetics vol 8article 31 2007

[101] D K Braithwaite and J Ito ldquoCompilation alignment andphylogenetic relationships of DNA polymerasesrdquo Nucleic AcidsResearch vol 21 no 4 pp 787ndash802 1993

[102] I K O Cann and Y Ishino ldquoArchaeal DNA replication iden-tifying the pieces to solve a puzzlerdquo Genetics vol 152 no 4 pp1249ndash1267 1999

[103] G Lipps S Rother C Hart and G Krauss ldquoA novel typeof replicative enzyme harbouring ATpase primase and DNApolymerase activityrdquo The EMBO Journal vol 22 no 10 pp2516ndash2525 2003

[104] J Yamtich and J B Sweasy ldquoDNA polymerase family X func-tion structure and cellular rolesrdquoBiochimica et BiophysicaActavol 1804 no 5 pp 1136ndash1150 2010

[105] H Ohmori E C Friedberg R P P Fuchs et al ldquoThe Y-familyof DNA polymerasesrdquoMolecular Cell vol 8 no 1 pp 7ndash8 2001

[106] N Y Yao R E Georgescu J Finkelstein and M E OrsquoDonnellldquoSingle-molecule analysis reveals that the lagging strandincreases replisome processivity but slows replication forkprogressionrdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 106 no 32 pp 13236ndash132412009

[107] U Hubscher G Maga and S Spadari ldquoEukaryotic DNA poly-merasesrdquo Annual Review of Biochemistry vol 71 pp 133ndash1632002

[108] F Boudsocq S Iwai F Hanaoka and R Woodgate ldquoSulfolobussolfataricus P2 DNA polymerase IV (Dp04) an archaeal DinB-like DNA polymerase with lesion-bypass properties akin toeukaryotic pol120578rdquo Nucleic Acids Research vol 29 no 22 pp4607ndash4616 2001

[109] L-J Lin A Yoshinaga Y Lin et al ldquoMolecular analyses ofan unusual translesion DNA polymerase fromMethanosarcinaacetivorans C2Ardquo Journal of Molecular Biology vol 397 no 1pp 13ndash30 2010

[110] I K O Cann S Ishino NNomura Y Sako andY Ishino ldquoTwofamily B DNA polymerases from Aeropyrum pernix an aerobichyperthermophilic crenarchaeoterdquo Journal of Bacteriology vol181 no 19 pp 5984ndash5992 1999

[111] T Uemori Y Ishino H Doi and I Kato ldquoThe hyperther-mophilic archaeon Pyrodictium occultum has two 120572-like DNApolymerasesrdquo Journal of Bacteriology vol 177 no 8 pp 2164ndash2177 1995

[112] T Uemori Y Ishino H Toh K Asada and I Kato ldquoOrgani-zation and nucleotide sequence of the DNA polymerase genefrom the archaeon Pyrococcus furiosusrdquo Nucleic Acids Researchvol 21 no 2 pp 259ndash265 1993

[113] B A Connolly ldquoRecognition of deaminated bases by archaealfamily-B DNA polymerasesrdquo Biochemical Society Transactionsvol 37 no 1 pp 65ndash68 2009

[114] B A Connolly M J Fogg G Shuttleworth and B T WilsonldquoUracil recognition by archaeal family B DNA polymerasesrdquoBiochemical Society Transactions vol 31 no 3 pp 699ndash7022003

[115] T T Richardson X Wu B J Keith P Heslop A C Jones andB A Connolly ldquoUnwinding of primer-templates by archaealfamily-B DNA polymerases in response to template-stranduracilrdquo Nucleic Acids Research vol 41 no 4 pp 2466ndash24782013

[116] T Lindahl ldquoInstability and decay of the primary structure ofDNArdquo Nature vol 362 no 6422 pp 709ndash715 1993

[117] I B Rogozin K S Makarova Y I Pavlov and E V Koonin ldquoAhighly conserved family of inactivated archaeal B family DNApolymerasesrdquo Biology Direct vol 3 article 32 2008

[118] M Imamura T Uemori I Kato and Y Ishino ldquoA non-120572-like DNA polymerase from the hyperthermophilic archaeonPyrococcus furiosusrdquoBiological andPharmaceutical Bulletin vol18 no 12 pp 1647ndash1652 1995

[119] I K O Cann K Komori H Toh S Kanai and Y IshinoldquoA heterodimeric DNA polymerase evidence that members ofEuryarchaeota possess a distinct DNA polymeraserdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 95 no 24 pp 14250ndash14255 1998

[120] L Aravind D D Leipe and E V Koonin ldquoToprimmdasha con-served catalytic domain in type IA and II topoisomerases

14 Archaea

DnaG-type primases OLD family nucleases and RecR pro-teinsrdquo Nucleic Acids Research vol 26 no 18 pp 4205ndash42131998

[121] M Jokela A Eskelinen H Pospiech J Rouvinen and J ESyvaoja ldquoCharacterization of the 31015840 exonuclease subunit DP1of Methanococcus jannaschii replicative DNA polymerase DrdquoNucleic Acids Research vol 32 no 8 pp 2430ndash2440 2004

[122] T Uemori Y Sato I Kato H Doi and Y Ishino ldquoA novel DNApolymerase in the hyperthermophilic archaeon Pyrococcus fur-iosus gene cloning expression and characterizationrdquo Genes toCells vol 2 no 8 pp 499ndash512 1997

[123] Y Shen K Musti M Hiramoto H Kikuchi Y Kawarabayashiand I Matsui ldquoInvariant Asp-1122 and Asp-1124 are essentialresidues for polymerization catalysis of family D DNA poly-merase from Pyrococcus horikoshiirdquo The Journal of BiologicalChemistry vol 276 no 29 pp 27376ndash27383 2001

[124] G Henneke D Flament U Hubscher J Querellou and J-P Raffin ldquoThe hyperthermophilic euryarchaeota Pyrococcusabyssi likely requires the two DNA polymerases D and B forDNA replicationrdquo Journal of Molecular Biology vol 350 no 1pp 53ndash64 2005

[125] L Cubonova T Richardson B W Burkhart et al ldquoArchaealDNA polymerase D but not DNA polymerase B is required forgenome replication in Thermococcus kodakarensisrdquo Journal ofBacteriology vol 195 no 10 pp 2322ndash2328 2013

[126] C Rouillon G Henneke D Flament J Querellou and J-PRaffin ldquoDNA polymerase switching on homotrimeric PCNA atthe replication fork of the euryarchaea Pyrococcus abyssirdquo Jour-nal of Molecular Biology vol 369 no 2 pp 343ndash355 2007

[127] G Henneke ldquoIn vitro reconstitution of RNA primer removal inArchaea reveals the existence of two pathwaysrdquoTheBiochemicalJournal vol 447 no 2 pp 271ndash280 2012

[128] G-LMoldovan B Pfander and S Jentsch ldquoPCNA themaestroof the replication forkrdquo Cell vol 129 no 4 pp 665ndash679 2007

[129] X-P Kong R Onrust M OrsquoDonnell and J Kuriyan ldquoThree-dimensional structure of the 120573 subunit of E coli DNA poly-merase III holoenzyme a sliding DNA clamprdquo Cell vol 69 no3 pp 425ndash437 1992

[130] K Daimon Y Kawarabayasi H Kikuchi Y Sako and Y IshinoldquoThree proliferating cell nuclear antigen-like proteins foundin the hyperthermophilic archaeon Aeropyrum pemix interac-tions with the two DNA polymerasesrdquo Journal of Bacteriologyvol 184 no 3 pp 687ndash694 2002

[131] I Dionne R K Nookala S P Jackson A J Doherty andS D Bell ldquoA heterotrimeric PCNA in the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Cell vol 11 no 1pp 275ndash282 2003

[132] E Warbrick ldquoPCNA binding through a conserved motifrdquoBioEssays vol 20 no 3 pp 195ndash199 1998

[133] H Nishida K Mayanagi S Kiyonari et al ldquoStructural deter-minant for switching between the polymerase and exonucleasemodes in the PCNA-replicative DNA polymerase complexrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 106 no 49 pp 20693ndash20698 2009

[134] K Mayanagi S Kiyonari H Nishida et al ldquoArchitecture of theDNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complexrdquo Proceedings of the National Academy ofSciences of the United States of America vol 108 no 5 pp 1845ndash1849 2011

[135] B Castrec C Rouillon G Henneke D Flament J Querellouand J-P Raffin ldquoBinding to PCNA in Euryarchaeal DNA

replication requires two PIP motifs for DNA polymerase D andone PIP motif for DNA polymerase Brdquo Journal of MolecularBiology vol 394 no 2 pp 209ndash218 2009

[136] P F Pluchon T Fouqueau C Creze et al ldquoAn extendednetworkof genomic maintenance in the archaeon Pyrococcus abyssihighlights unexpected associations between eucaryotic homo-logsrdquo PLoS One vol 8 no 11 Article ID e79707 2013

[137] J E Ladner M Pan J Hurwitz and Z Kelman ldquoCrystalstructures of two active proliferating cell nuclear antigens(PCNAs) encoded byThermococcus kodakaraensisrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2711ndash2716 2011

[138] Y Kuba S Ishino T Yamagami et al ldquoComparative analyses ofthe two proliferating cell nuclear antigens from the hyperther-mophilic archaeonThermococcus kodakarensisrdquo Genes to Cellsvol 17 no 11 pp 923ndash937 2012

[139] T Fukui H Atomi T Kanai R Matsumi S Fujiwara andT Imanaka ldquoComplete genome sequence of the hyperther-mophilic archaeon Thermococcus kodakaraensis KOD1 andcomparison with Pyrococcus genomesrdquo Genome Research vol15 no 3 pp 352ndash363 2005

[140] D Jeruzalmi O Yurieva Y Zhao et al ldquoMechanism of proces-sivity clamp opening by the delta subunit wrench of the clamploader complex of E coliDNApolymerase IIIrdquoCell vol 106 no4 pp 417ndash428 2001

[141] Y Shiomi J Usukura Y Masamura et al ldquoATP-dependentstructural change of the eukaryotic clamp-loader protein repli-cation factor Crdquo Proceedings of the National Academy of Sciencesof the United States of America vol 97 no 26 pp 14127ndash141322000

[142] T Miyata T Oyama K Mayanagi S Ishino Y Ishino and KMorikawa ldquoThe clamp-loading complex for processive DNAreplicationrdquoNature Structural andMolecular Biology vol 11 no7 pp 632ndash636 2004

[143] T Oyama Y Ishino I K O Cann S Ishino and K MorikawaldquoAtomic structure of the clamp loader small subunit fromPyrococcus furiosusrdquo Molecular Cell vol 8 no 2 pp 455ndash4632001

[144] A Seybert D J Scott S Scaife M R Singleton and DB Wigley ldquoBiochemical characterisation of the clampclamploader proteins from the euryarchaeon Archaeoglobus fulgidusrdquoNucleic Acids Research vol 30 no 20 pp 4329ndash4338 2002

[145] Y-H Chen Y Lin A Yoshinaga et al ldquoMolecular analyses of athree-subunit euryarchaeal clamp loader complex from Meth-anosarcina acetivoransrdquo Journal of Bacteriology vol 191 no 21pp 6539ndash6549 2009

[146] Y-H Chen S A Kocherginskaya Y Lin et al ldquoBiochemicaland mutational analyses of a unique clamp loader complex inthe archaeon Methanosarcina acetivoransrdquo The Journal of Bio-logical Chemistry vol 280 no 51 pp 41852ndash41863 2005

[147] F Matsunaga C Norais P Forterre and H Myllykallio ldquoIden-tification of short ldquoeukaryoticrdquo Okazaki fragments synthesizedfrom a prokaryotic replication originrdquo EMBO Reports vol 4no 2 pp 154ndash158 2003

[148] H Kochiwa M Tomita and A Kanai ldquoEvolution of ribonucle-ase H genes in prokaryotes to avoid inheritance of redundantgenesrdquo BMC Evolutionary Biology vol 7 article 128 2007

[149] N OhtaniMHarukiMMorikawa and S Kanaya ldquoMoleculardiversities of RNases Hrdquo Journal of Bioscience and Bioengineer-ing vol 88 no 1 pp 12ndash19 1999

Archaea 15

[150] N Ohtani M Haruki M Morikawa R J Crouch M Itayaand S Kanaya ldquoIdentification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII fromBacillus subtilis classification of RNases H into three familiesrdquoBiochemistry vol 38 no 2 pp 605ndash618 1999

[151] N Ohtani H Yanagawa M Tomita and M Itaya ldquoIdentifi-cation of the first archaeal type 1 RNase H gene from Halobac-terium sp NRC-1 archaeal RNase HI can cleave an RNA-DNAjunctionrdquoThe Biochemical Journal vol 381 no 3 pp 795ndash8022004

[152] N Ohtani H Yanagawa M Tomita and M Itaya ldquoCleavage ofdouble-stranded RNA by RNase HI from a thermoacidophilicarchaeon Sulfolobus tokodaii 7rdquo Nucleic Acids Research vol 32no 19 pp 5809ndash5819 2004

[153] M A Nowak M C Boerlijst J Cooke and J M SmithldquoEvolution of genetic redundancyrdquo Nature vol 388 no 6638pp 167ndash170 1997

[154] A E Tomkinson S Vijayakumar J M Pascal and T Ellen-berger ldquoDNA ligases structure reactionmechanism and func-tionrdquo Chemical Reviews vol 106 no 2 pp 687ndash699 2006

[155] M Nakatani S Ezaki H Atomi and T Imanaka ldquoA DNAligase from a hyperthermophilic archaeon with unique cofactorspecificityrdquo Journal of Bacteriology vol 182 no 22 pp 6424ndash6433 2000

[156] Y Sun M S Seo J H Kim et al ldquoNovel DNA ligase with broadnucleotide cofactor specificity from the hyperthermophilic cre-narchaeon Sulfophobococcus zilligii influence of ancestral DNAligase on cofactor utilizationrdquo Environmental Microbiology vol10 no 12 pp 3212ndash3224 2008

[157] T R Beattie and S D Bell ldquoCoordination of multiple enzymeactivities by a single PCNA in archaeal Okazaki fragmentmaturationrdquo The EMBO Journal vol 31 no 6 pp 1556ndash15672012

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

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BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

10 Archaea

interact with other unknown initiation enzymes resultingin a complex phylogeny of the MCM homologs [49] Pre-sumably these differences also account for the inability torecognize the origin of replication in these microorganismsThis unique scenario for initiation of DNA replicationmay bea direct consequence of various processes such as duplicationmobile genetic elements and interactions with viruses [58]

The differences in DNA replication among archaealhigher taxa demonstrate an unexpected variability and sug-gest two alternative evolutionary models In the first modelDNA replication evolved late after the diversification ofthe archaeal lineages Because the replicative system wasnot fully formed it was possible to develop differentlybetween the lineages Once formed replication would thenbe highly conserved However this model is not consistentwith differences observed between lineages that must haveformed relatively late such as those between the orders oreven in some cases within certain orders The alternativemodel is that DNA replication has changed throughout theevolution of the archaea Thus differences in the replicativesystems may represent ancient as well as modern adaptationsto changing environments In this case differences in thereplicative systems may provide important insights into theevolutionary pressures in play during different episodes ofarchaeal evolution From this perspective the differencesbetween the eukaryotic and archaeal replicative systems maynot be evidence for an ancient origin of the eukaryotesInstead it is entirely plausible that the replicative system ineukaryotes could have evolved relatively late from a well-developed archaeal system

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] E F DeLong and N R Pace ldquoEnvironmental diversity ofbacteria and archaeardquo Systematic Biology vol 50 no 4 pp 470ndash478 2001

[2] B Chaban S Y M Ng and K F Jarrell ldquoArchaeal habitatsmdashfrom the extreme to the ordinaryrdquo Canadian Journal of Micro-biology vol 52 no 2 pp 73ndash116 2006

[3] M J Hanford and T L Peeples ldquoArchaeal tetraether lipidsunique structures and applicationsrdquo Applied Biochemistry andBiotechnology A vol 97 no 1 pp 45ndash62 2002

[4] K Sandman and J N Reeve ldquoArchaeal histones and the originof the histone foldrdquo Current Opinion in Microbiology vol 9 no5 pp 520ndash525 2006

[5] O Lecompte R Ripp J-C Thierry D Moras and O PochldquoComparative analysis of ribosomal proteins in complete gen-omes an example of reductive evolution at the domain scalerdquoNucleic Acids Research vol 30 no 24 pp 5382ndash5390 2002

[6] D R Edgell and W F Doolittle ldquoArchaea and the origin(s) ofDNA rplication poteinsrdquo Cell vol 89 no 7 pp 995ndash998 1997

[7] E R Barry and S D Bell ldquoDNA replication in the archaeardquoMicrobiology and Molecular Biology Reviews vol 70 no 4 pp876ndash887 2006

[8] S Gribaldo and C Brochier-Armanet ldquoThe origin and evolu-tion of archaea a state of the artrdquo Philosophical Transactions ofthe Royal Society B vol 361 no 1470 pp 1007ndash1022 2006

[9] P Londei ldquoEvolution of translational initiation new insightsfrom the archaeardquo FEMS Microbiology Reviews vol 29 no 2pp 185ndash200 2005

[10] B Grabowski and Z Kelman ldquoArchaeal DNA replicationeukaryal proteins in a bacterial contextrdquo Annual Review ofMicrobiology vol 57 pp 487ndash516 2003

[11] P Forterre J Filee and H Myllykallio ldquoOrigin and evolutionof DNA and DNA replication machineriesrdquo in The GeneticCode and the Origin of Life L Ribas Ed Landes BioscienceGeorgetown Tex USA 2007

[12] E V Koonin ldquoThe origin and early evolution of eukaryotesin the light of phylogenomicsrdquo Genome Biology vol 11 no 5article 209 2010

[13] M Konneke A E Bernhard J R de la Torre C B WalkerJ B Waterbury and D A Stahl ldquoIsolation of an autotrophicammonia-oxidizing marine archaeonrdquo Nature vol 437 no7058 pp 543ndash546 2005

[14] C Brochier-Armanet B Boussau S Gribaldo and P ForterreldquoMesophilic crenarchaeota proposal for a third archaeal phy-lum theThaumarchaeotardquoNature Reviews Microbiology vol 6no 3 pp 245ndash252 2008

[15] J G Elkins M Podar D E Graham et al ldquoA korarchaealgenome reveals insights into the evolution of the ArchaeardquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 105 no 23 pp 8102ndash8107 2008

[16] T Nunoura Y Takaki J Kakuta et al ldquoInsights into theevolution of Archaea and eukaryotic protein modifier systemsrevealed by the genome of a novel archaeal grouprdquoNucleic AcidsResearch vol 39 no 8 pp 3204ndash3223 2011

[17] HHuberM J Hohn R Rachel T Fuchs V CWimmer andKO Stetter ldquoAnewphylumofArchaea represented by a nanosizedhyperthermophilic symbiontrdquoNature vol 417 no 6884 pp 63ndash67 2002

[18] C Brochier S Gribaldo Y Zivanovic F Confalonieri and PForterre ldquoNanoarchaea representatives of a novel archaeal phy-lum or a fast-evolving euryarchaeal lineage related to Therm-ococcalesrdquo Genome Biology vol 6 no 5 article R42 2005

[19] S J Aves ldquoDNA replication initiationrdquo Methods in MolecularBiology vol 521 pp 3ndash17 2009

[20] N P Robinson I Dionne M Lundgren V L Marsh RBernander and S D Bell ldquoIdentification of two origins ofreplication in the single chromosome of the archaeon Sulfolobussolfataricusrdquo Cell vol 116 no 1 pp 25ndash38 2004

[21] M Lundgren A Andersson L Chen P Nilsson and RBernander ldquoThree replication origins in Sulfolobus speciessynchronous initiation of chromosome replication and asyn-chronous terminationrdquo Proceedings of the National Academy ofSciences of theUnited States of America vol 101 no 18 pp 7046ndash7051 2004

[22] N P Robinson and S D Bell ldquoExtrachromosomal element cap-ture and the evolution ofmultiple replication origins in archaealchromosomesrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 104 no 14 pp 5806ndash58112007

[23] E A Pelve A C Lindas A Knoppel A Mira and R Bernan-der ldquoFour chromosome replication origins in the archaeonPyrobaculum calidifontisrdquo Molecular Microbiology vol 85 no5 pp 986ndash995 2012

Archaea 11

[24] A F Andersson E A Pelve S LindebergM Lundgren P Nils-son and R Bernander ldquoReplication-biased genome organisa-tion in the crenarchaeon Sulfolobusrdquo BMCGenomics vol 11 no1 article 454 2010

[25] H Myllykallio P Lopez P Lopez-Garcıa et al ldquoBacterial modeof replication with eukaryotic-like machinery in a hyperther-mophilic archaeonrdquo Science vol 288 no 5474 pp 2212ndash22152000

[26] F Matsunaga P Forterre Y Ishino and H Myllykallio ldquoInvivo interactions of archaeal Cdc6Orc1 and minichromosomemaintenance proteins with the replication originrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 98 no 20 pp 11152ndash11157 2001

[27] S Maisnier-Patin L Malandrin N K Birkeland and RBernander ldquoChromosome replication patterns in the hyper-thermophilic euryarchaeaArchaeoglobus fulgidus andMethano-caldococcus (Methanococcus) jannaschiirdquo Molecular Microbiol-ogy vol 45 no 5 pp 1443ndash1450 2002

[28] R Zhang and C-T Zhang ldquoMultiple replication origins ofthe archaeon Halobacterium species NRC-1rdquo Biochemical andBiophysical Research Communications vol 302 no 4 pp 728ndash734 2003

[29] C Norais M Hawkins A L Hartman J A Eisen H Myl-lykallio and T Allers ldquoGenetic and physical mapping of DNAreplication origins in Haloferax volcaniirdquo PLoS Genetics vol 3no 5 article e77 2007

[30] J A Coker P DasSarma M Capes et al ldquoMultiple replicationorigins of Halobacterium sp strain NRC-1 properties of theconserved orc7-dependent oriC1rdquo Journal of Bacteriology vol191 no 16 pp 5253ndash5261 2009

[31] Z Wu J Liu H Yang H Liu and H Xiang ldquoMultiple repli-cation origins with diverse control mechanisms in Haloarculahispanicardquo Nucleic Acids Research 2013

[32] M Hawkins S Malla M J Blythe C A Nieduszynski and TAllers ldquoAccelerated growth in the absence of DNA replicationoriginsrdquo Nature vol 503 no 7477 pp 544ndash547 2013

[33] A I Majernık and J P J Chong ldquoA conserved mechanismfor replication origin recognition and binding in archaeardquo TheBiochemical Journal vol 409 no 2 pp 511ndash518 2008

[34] J E Galagan C Nusbaum A Roy et al ldquoThe genome of Macetivorans reveals extensive metabolic and physiological diver-sityrdquo Genome Research vol 12 no 4 pp 532ndash542 2002

[35] R Zhang and C-T Zhang ldquoIdentification of replication originsin archaeal genomes based on the Z-curve methodrdquo Archaeavol 1 no 5 pp 335ndash346 2005

[36] A Spang R Hatzenpichler C Brochier-Armanet et al ldquoDis-tinct gene set in two different lineages of ammonia-oxidizingarchaea supports the phylum Thaumarchaeotardquo Trends inMicrobiology vol 18 no 8 pp 331ndash340 2010

[37] K J Marians ldquoProkaryotic DNA replicationrdquo Annual Review ofBiochemistry vol 61 pp 673ndash719 1992

[38] S P Bell ldquoThe origin recognition complex from simple originsto complex functionsrdquo Genes and Development vol 16 no 6pp 659ndash672 2002

[39] V L Marsh and S D Bell ldquoDNA replication and the cell cyclerdquoin Archaea Evolution Physiology and Molecular Biology R AGarrett and H P Klenk Eds Blackwell Publishing HobokenNJ USA 2007

[40] F Matsunaga A Glatigny M-H Mucchielli-Giorgi et alldquoGenomewide and biochemical analyses of DNA-binding activ-ity of Cdc6Orc1 and Mcm proteins in Pyrococcus sprdquo NucleicAcids Research vol 35 no 10 pp 3214ndash3222 2007

[41] J Liu C L Smith D DeRyckere K DeAngelis G S Martinand J M Berger ldquoStructure and function of Cdc6Cdc18implications for origin recognition and checkpoint controlrdquoMolecular Cell vol 6 no 3 pp 637ndash648 2000

[42] M R Singleton R Morales I Grainge N Cook M NIsupov and D B Wigley ldquoConformational changes inducedby nucleotide binding in Cdc6ORC from Aeropyrum pernixrdquoJournal of Molecular Biology vol 343 no 3 pp 547ndash557 2004

[43] Y Ishino and S Ishino ldquoRapid progress of DNA replicationstudies in Archaea the third domain of liferdquo Science China LifeSciences vol 55 no 5 pp 386ndash403 2012

[44] E L Hendrickson R Kaul Y Zhou et al ldquoComplete genomesequence of the genetically tractable hydrogenotrophic meth-anogen Methanococcus maripaludisrdquo Journal of Bacteriologyvol 186 no 20 pp 6956ndash6969 2004

[45] B K Tye ldquoMCM proteins in DNA replicationrdquo Annual Reviewof Biochemistry vol 68 pp 649ndash686 1999

[46] K Labib and J F X Diffley ldquoIs the MCM2-7 complex theeukaryotic DNA replication fork helicaserdquo Current Opinion inGenetics amp Development vol 11 no 1 pp 64ndash70 2001

[47] I Ilves T Petojevic J J Pesavento and M R Botchan ldquoActi-vation of the MCM2-7 helicase by association with Cdc45 andGINS proteinsrdquoMolecular Cell vol 37 no 2 pp 247ndash258 2010

[48] M L Bochman andA Schwacha ldquoTheMcm complex unwind-ing the mechanism of a replicative helicaserdquo Microbiology andMolecular Biology Reviews vol 73 no 4 pp 652ndash683 2009

[49] Y Ishimi ldquoADNAhelicase activity is associated with anMCM4-6 and -7 protein complexrdquoThe Journal of Biological Chemistryvol 272 no 39 pp 24508ndash24513 1997

[50] Z Kelman and M F White ldquoArchaeal DNA replication andrepairrdquo Current Opinion in Microbiology vol 8 no 6 pp 669ndash676 2005

[51] J H LeBowitz and R McMacken ldquoThe Escherichia coli dnaBreplication protein is a DNA helicaserdquoThe Journal of BiologicalChemistry vol 261 no 10 pp 4738ndash4748 1986

[52] Z Kelman J-K Lee and J Hurwitz ldquoThe single minichro-mosome maintenance protein ofMethanobacterium thermoau-totrophicum ΔH contains DNA helicase activityrdquo Proceedings ofthe National Academy of Sciences of the United States of Americavol 96 no 26 pp 14783ndash14788 1999

[53] D F Shechter C Y Ying and J Gautier ldquoThe intrinsic DNAhelicase activity of Methanobacterium thermoautotrophicumΔH minichromosome maintenance proteinrdquo The Journal ofBiological Chemistry vol 275 no 20 pp 15049ndash15059 2000

[54] M de Felice L Esposito B Pucci M de Falco M Rossi andF M Pisani ldquoA CDC6-like factor from the archaea Sulfolobussolfataricus promotes binding of the mini-chromosome main-tenance complex to DNArdquoThe Journal of Biological Chemistryvol 279 no 41 pp 43008ndash43012 2004

[55] R Kasiviswanathan J-H Shin and Z Kelman ldquoInteractionsbetween the archaeal Cdc6 and MCM proteins modulate theirbiochemical propertiesrdquo Nucleic Acids Research vol 33 no 15pp 4940ndash4950 2005

[56] J-H Shin B Grabowski R Kasiviswanathan S D Bell andZ Kelman ldquoRegulation of minichromosomemaintenance heli-case activity by Cdc6rdquo The Journal of Biological Chemistry vol278 no 39 pp 38059ndash38067 2003

[57] M Akita A Adachi K Takemura T Yamagami F Matsunagaand Y Ishino ldquoCdc6Orc1 from Pyrococcus furiosus may actas the origin recognition protein and Mcm helicase recruiterrdquoGenes to Cells vol 15 no 5 pp 537ndash552 2010

12 Archaea

[58] M Krupovic S Gribaldo D H Bamford and P Forterre ldquoTheevolutionary history of archaeal MCM helicases a case study ofvertical evolution combined with hitchhiking of mobile geneticelementsrdquo Molecular Biology and Evolution vol 27 no 12 pp2716ndash2732 2010

[59] ADWalters and J P J Chong ldquoAn archaeal orderwithmultipleminichromosome maintenance genesrdquo Microbiology vol 156part 5 pp 1405ndash1414 2010

[60] A DWalters and J P J Chong ldquoMethanococcusmaripaludis anarchaeon with multiple functional MCM proteinsrdquo Biochemi-cal Society Transactions vol 37 no 1 pp 1ndash6 2009

[61] Q Xia E L Hendrickson Y Zhang et al ldquoQuantitative pro-teomics of the archaeon Methanococcus maripaludis validatedbymicroarray analysis and real time PCRrdquoMolecularampCellularProteomics vol 5 no 5 pp 868ndash881 2006

[62] F Sarmiento J Mrazek and W B Whitman ldquoGenome-scaleanalysis of gene function in the hydrogenotrophic methano-genic archaeon Methanococcus maripaludisrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 110 no 12 pp 4726ndash4731 2013

[63] M Pan T J Santangelo Z Li J N Reeve and Z KelmanldquoThermococcus kodakarensis encodes threeMCMhomologs butonly one is essentialrdquo Nucleic Acids Research vol 39 no 22 pp9671ndash9680 2011

[64] S Ishino S Fujino H Tomita et al ldquoBiochemical and geneticalanalyses of the three mcm genes from the hyperthermophilicarchaeon Thermococcus kodakarensisrdquo Genes to Cells vol 16no 12 pp 1176ndash1189 2011

[65] K S Makarova Y I Wolf S L Mekhedov B G Mirkin and EV Koonin ldquoAncestral paralogs and pseudoparalogs and theirrole in the emergence of the eukaryotic cellrdquo Nucleic AcidsResearch vol 33 no 14 pp 4626ndash4638 2005

[66] N Marinsek E R Barry K S Makarova I Dionne E VKoonin and S D Bell ldquoGINS a central nexus in the archaealDNA replication forkrdquo EMBOReports vol 7 no 5 pp 539ndash5452006

[67] T Yoshimochi R Fujikane M Kawanami F Matsunaga and YIshino ldquoTheGINS complex from Pyrococcus furiosus stimulatesthe MCM helicase activityrdquoThe Journal of Biological Chemistryvol 283 no 3 pp 1601ndash1609 2008

[68] T Oyama S Ishino S Fujino et al ldquoArchitectures of archaealGINS complexes essential DNA replication initiation factorsrdquoBMC Biology vol 9 article 28 2011

[69] H Ogino S Ishino K Mayanagi et al ldquoThe GINS com-plex from the thermophilic archaeon Thermoplasma aci-dophilummay function as a homotetramer inDNA replicationrdquoExtremophiles vol 15 no 4 pp 529ndash539 2011

[70] L Sanchez-Pulido and C P Ponting ldquoCdc45 the missing recjortholog in eukaryotesrdquoBioinformatics vol 27 no 14 pp 1885ndash1888 2011

[71] Z Li T J Santangelo L Cubonova J N Reeve and Z KelmanldquoAffinity purification of an archaeal DNA replication proteinnetworkrdquomBio vol 1 no 5 2010

[72] Z Li M Pan T J Santangelo et al ldquoA novel DNA nucleaseis stimulated by association with the GINS complexrdquo NucleicAcids Research vol 39 no 14 pp 6114ndash6123 2011

[73] L A Rajman and S T Lovett ldquoA thermostable single-strandDNase from Methanococcus jannaschii related to the RecJrecombination and repair exonuclease from Escherichia colirdquoJournal of Bacteriology vol 182 no 3 pp 607ndash612 2000

[74] K RWilliams J B Murphy and JW Chase ldquoCharacterizationof the structural and functional defect in the Escherichia colisingle-stranded DNA binding protein encoded by the ssb-1 mutant gene Expression of the ssb-1 gene under 120582p(L)regulationrdquoThe Journal of Biological Chemistry vol 259 no 19pp 11804ndash11811 1984

[75] S Dąbrowski M Olszewski R Pitek and J Kur ldquoNovel ther-mostable ssDNA-binding proteins fromThermus thermophilusand T aquaticus-expression and purificationrdquo Protein Expres-sion and Purification vol 26 no 1 pp 131ndash138 2002

[76] C Iftode Y Daniely and J A Borowiec ldquoReplication proteinA (RPA) the eukaryotic SSBrdquo Critical Reviews in Biochemistryand Molecular Biology vol 34 no 3 pp 141ndash180 1999

[77] A G Murzin ldquoOB(oligonucleotideoligosaccharide binding)-fold common structural and functional solution for non-hom-ologous sequencesrdquo The EMBO Journal vol 12 no 3 pp 861ndash867 1993

[78] C A Haseltine and S C Kowalczykowski ldquoA distinctive single-stranded DNA-binding protein from the Archaeon Sulfolobussolfataricusrdquo Molecular Microbiology vol 43 no 6 pp 1505ndash1515 2002

[79] R I M Wadsworth and M F White ldquoIdentification and pro-perties of the crenarchaeal single-stranded DNA binding pro-tein from Sulfolobus solfataricusrdquoNucleic Acids Research vol 29no 4 pp 914ndash920 2001

[80] I D Kerr R I M Wadsworth L Cubeddu W Blankenfeldt JHNaismith andM FWhite ldquoInsights into ssDNA recognitionby the OB fold from a structural and thermodynamic study ofSulfolobus SSB proteinrdquo The EMBO Journal vol 22 no 11 pp2561ndash2570 2003

[81] X Luo U Schwarz-Linek C H Botting R Hensel B Siebersand M F White ldquoCC1 a novel crenarchaeal DNA binding pro-teinrdquo Journal of Bacteriology vol 189 no 2 pp 403ndash409 2007

[82] T J Kelly P Simancek and G S Brush ldquoIdentification andcharacterization of a single-stranded DNA-binding proteinfrom the archaeonMethanococcus jannaschiirdquoProceedings of theNational Academy of Sciences of theUnited States of America vol95 no 25 pp 14634ndash14639 1998

[83] Z Kelman S Pietrokovski and J Hurwitz ldquoIsolation and cha-racterization of a split B-type DNA polymerase from the arch-aeonMethanobacterium thermoautotrophicumΔHrdquoTheJournalof Biological Chemistry vol 274 no 40 pp 28751ndash28761 1999

[84] K Komori and Y Ishino ldquoReplication protein A in Pyrococcusfuriosus is involved in homologous DNA recombinationrdquo TheJournal of Biological Chemistry vol 276 no 28 pp 25654ndash25660 2001

[85] J B Robbins M C Murphy B A White R I Mackie THa and I K O Cann ldquoFunctional analysis of multiple single-stranded DNA-binding proteins from Methanosarcina acetivo-rans and their effects on DNA synthesis by DNA polymeraseBIrdquoThe Journal of Biological Chemistry vol 279 no 8 pp 6315ndash6326 2004

[86] Y Lin L-J Lin P Sriratana et al ldquoEngineering of functionalreplication protein a homologs based on insights into the evolu-tion of oligonucleotideoligosaccharide-binding foldsrdquo Journalof Bacteriology vol 190 no 17 pp 5766ndash5780 2008

[87] D N Frick and C C Richardson ldquoDNA primasesrdquo AnnualReview of Biochemistry vol 70 pp 39ndash80 2001

[88] G Desogus S Onesti P Brick M Rossi and F M PisanildquoIdentification and characterization of a DNA primase fromthe hyperthermophilic archaeon Methanococcus jannaschiirdquoNucleic Acids Research vol 27 no 22 pp 4444ndash4450 1999

Archaea 13

[89] A A Bocquier L Liu I K O Cann K Komori D Kohda andY Ishino ldquoArchaeal primase bridging the gap between RNAand DNA polymerasesrdquo Current Biology vol 11 no 6 pp 452ndash456 2001

[90] L Liu K Komori S Ishino et al ldquoThe archaeal DNA primasebiochemical characterization of the p41-p46 complex fromPyrococcus furiosusrdquo The Journal of Biological Chemistry vol276 no 48 pp 45484ndash45490 2001

[91] E Matsui M Nishio H Yokoyama K Harata S Darnisand I Matsui ldquoDistinct domain functions regulating de novoDNA synthesis of thermostable DNA primase from hyperther-mophile Pyrococcus horikoshiirdquo Biochemistry vol 42 no 50 pp14968ndash14976 2003

[92] N Ito I Matsui and EMatsui ldquoMolecular basis for the subunitassembly of the primase from an archaeon Pyrococcus hori-koshiirdquoThe FEBS Journal vol 274 no 5 pp 1340ndash1351 2007

[93] M le Breton G Henneke C Norais et al ldquoThe heterodimericprimase from the euryarchaeon Pyrococcus abyssi a multifunc-tional enzyme for initiation and repairrdquo Journal of MolecularBiology vol 374 no 5 pp 1172ndash1185 2007

[94] S-H Lao-Sirieix and S D Bell ldquoThe heterodimeric primaseof the hyperthermophilic archaeon Sulfolobus solfataricus pos-sesses DNA and RNA primase polymerase and 31015840-terminalnucleotidyl transferase activitiesrdquo Journal of Molecular Biologyvol 344 no 5 pp 1251ndash1263 2004

[95] S-H Lao-Sirieix L Pellegrini and S D Bell ldquoThe promiscuousprimaserdquo Trends in Genetics vol 21 no 10 pp 568ndash572 2005

[96] J Hu L Guo K Wu B Liu S Lang and L Huang ldquoTemplate-dependent polymerization across discontinuous templatesby the heterodimeric primase from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquoNucleic Acids Research vol 40no 8 pp 3470ndash3483 2012

[97] E Evguenieva-Hackenberg P Walter E Hochleitner FLottspeich and G Klug ldquoAn exosome-like complex in Sulfolo-bus solfataricusrdquo EMBOReports vol 4 no 9 pp 889ndash893 2003

[98] P Walter F Klein E Lorentzen A Ilchmann G Klug andE Evguenieva-Hackenberg ldquoCharacterization of native andreconstituted exosome complexes from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Microbiology vol62 no 4 pp 1076ndash1089 2006

[99] Z Zuo C J Rodgers A L Mikheikin and M A Trak-selis ldquoCharacterization of a functional DnaG-type primase inarchaea implications for a dual-primase systemrdquo Journal ofMolecular Biology vol 397 no 3 pp 664ndash676 2010

[100] B R Berquist P DasSarma and S DasSarma ldquoEssential andnon-essential DNA replication genes in the model halophilicArchaeon Halobacterium sp NRC-1rdquo BMC Genetics vol 8article 31 2007

[101] D K Braithwaite and J Ito ldquoCompilation alignment andphylogenetic relationships of DNA polymerasesrdquo Nucleic AcidsResearch vol 21 no 4 pp 787ndash802 1993

[102] I K O Cann and Y Ishino ldquoArchaeal DNA replication iden-tifying the pieces to solve a puzzlerdquo Genetics vol 152 no 4 pp1249ndash1267 1999

[103] G Lipps S Rother C Hart and G Krauss ldquoA novel typeof replicative enzyme harbouring ATpase primase and DNApolymerase activityrdquo The EMBO Journal vol 22 no 10 pp2516ndash2525 2003

[104] J Yamtich and J B Sweasy ldquoDNA polymerase family X func-tion structure and cellular rolesrdquoBiochimica et BiophysicaActavol 1804 no 5 pp 1136ndash1150 2010

[105] H Ohmori E C Friedberg R P P Fuchs et al ldquoThe Y-familyof DNA polymerasesrdquoMolecular Cell vol 8 no 1 pp 7ndash8 2001

[106] N Y Yao R E Georgescu J Finkelstein and M E OrsquoDonnellldquoSingle-molecule analysis reveals that the lagging strandincreases replisome processivity but slows replication forkprogressionrdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 106 no 32 pp 13236ndash132412009

[107] U Hubscher G Maga and S Spadari ldquoEukaryotic DNA poly-merasesrdquo Annual Review of Biochemistry vol 71 pp 133ndash1632002

[108] F Boudsocq S Iwai F Hanaoka and R Woodgate ldquoSulfolobussolfataricus P2 DNA polymerase IV (Dp04) an archaeal DinB-like DNA polymerase with lesion-bypass properties akin toeukaryotic pol120578rdquo Nucleic Acids Research vol 29 no 22 pp4607ndash4616 2001

[109] L-J Lin A Yoshinaga Y Lin et al ldquoMolecular analyses ofan unusual translesion DNA polymerase fromMethanosarcinaacetivorans C2Ardquo Journal of Molecular Biology vol 397 no 1pp 13ndash30 2010

[110] I K O Cann S Ishino NNomura Y Sako andY Ishino ldquoTwofamily B DNA polymerases from Aeropyrum pernix an aerobichyperthermophilic crenarchaeoterdquo Journal of Bacteriology vol181 no 19 pp 5984ndash5992 1999

[111] T Uemori Y Ishino H Doi and I Kato ldquoThe hyperther-mophilic archaeon Pyrodictium occultum has two 120572-like DNApolymerasesrdquo Journal of Bacteriology vol 177 no 8 pp 2164ndash2177 1995

[112] T Uemori Y Ishino H Toh K Asada and I Kato ldquoOrgani-zation and nucleotide sequence of the DNA polymerase genefrom the archaeon Pyrococcus furiosusrdquo Nucleic Acids Researchvol 21 no 2 pp 259ndash265 1993

[113] B A Connolly ldquoRecognition of deaminated bases by archaealfamily-B DNA polymerasesrdquo Biochemical Society Transactionsvol 37 no 1 pp 65ndash68 2009

[114] B A Connolly M J Fogg G Shuttleworth and B T WilsonldquoUracil recognition by archaeal family B DNA polymerasesrdquoBiochemical Society Transactions vol 31 no 3 pp 699ndash7022003

[115] T T Richardson X Wu B J Keith P Heslop A C Jones andB A Connolly ldquoUnwinding of primer-templates by archaealfamily-B DNA polymerases in response to template-stranduracilrdquo Nucleic Acids Research vol 41 no 4 pp 2466ndash24782013

[116] T Lindahl ldquoInstability and decay of the primary structure ofDNArdquo Nature vol 362 no 6422 pp 709ndash715 1993

[117] I B Rogozin K S Makarova Y I Pavlov and E V Koonin ldquoAhighly conserved family of inactivated archaeal B family DNApolymerasesrdquo Biology Direct vol 3 article 32 2008

[118] M Imamura T Uemori I Kato and Y Ishino ldquoA non-120572-like DNA polymerase from the hyperthermophilic archaeonPyrococcus furiosusrdquoBiological andPharmaceutical Bulletin vol18 no 12 pp 1647ndash1652 1995

[119] I K O Cann K Komori H Toh S Kanai and Y IshinoldquoA heterodimeric DNA polymerase evidence that members ofEuryarchaeota possess a distinct DNA polymeraserdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 95 no 24 pp 14250ndash14255 1998

[120] L Aravind D D Leipe and E V Koonin ldquoToprimmdasha con-served catalytic domain in type IA and II topoisomerases

14 Archaea

DnaG-type primases OLD family nucleases and RecR pro-teinsrdquo Nucleic Acids Research vol 26 no 18 pp 4205ndash42131998

[121] M Jokela A Eskelinen H Pospiech J Rouvinen and J ESyvaoja ldquoCharacterization of the 31015840 exonuclease subunit DP1of Methanococcus jannaschii replicative DNA polymerase DrdquoNucleic Acids Research vol 32 no 8 pp 2430ndash2440 2004

[122] T Uemori Y Sato I Kato H Doi and Y Ishino ldquoA novel DNApolymerase in the hyperthermophilic archaeon Pyrococcus fur-iosus gene cloning expression and characterizationrdquo Genes toCells vol 2 no 8 pp 499ndash512 1997

[123] Y Shen K Musti M Hiramoto H Kikuchi Y Kawarabayashiand I Matsui ldquoInvariant Asp-1122 and Asp-1124 are essentialresidues for polymerization catalysis of family D DNA poly-merase from Pyrococcus horikoshiirdquo The Journal of BiologicalChemistry vol 276 no 29 pp 27376ndash27383 2001

[124] G Henneke D Flament U Hubscher J Querellou and J-P Raffin ldquoThe hyperthermophilic euryarchaeota Pyrococcusabyssi likely requires the two DNA polymerases D and B forDNA replicationrdquo Journal of Molecular Biology vol 350 no 1pp 53ndash64 2005

[125] L Cubonova T Richardson B W Burkhart et al ldquoArchaealDNA polymerase D but not DNA polymerase B is required forgenome replication in Thermococcus kodakarensisrdquo Journal ofBacteriology vol 195 no 10 pp 2322ndash2328 2013

[126] C Rouillon G Henneke D Flament J Querellou and J-PRaffin ldquoDNA polymerase switching on homotrimeric PCNA atthe replication fork of the euryarchaea Pyrococcus abyssirdquo Jour-nal of Molecular Biology vol 369 no 2 pp 343ndash355 2007

[127] G Henneke ldquoIn vitro reconstitution of RNA primer removal inArchaea reveals the existence of two pathwaysrdquoTheBiochemicalJournal vol 447 no 2 pp 271ndash280 2012

[128] G-LMoldovan B Pfander and S Jentsch ldquoPCNA themaestroof the replication forkrdquo Cell vol 129 no 4 pp 665ndash679 2007

[129] X-P Kong R Onrust M OrsquoDonnell and J Kuriyan ldquoThree-dimensional structure of the 120573 subunit of E coli DNA poly-merase III holoenzyme a sliding DNA clamprdquo Cell vol 69 no3 pp 425ndash437 1992

[130] K Daimon Y Kawarabayasi H Kikuchi Y Sako and Y IshinoldquoThree proliferating cell nuclear antigen-like proteins foundin the hyperthermophilic archaeon Aeropyrum pemix interac-tions with the two DNA polymerasesrdquo Journal of Bacteriologyvol 184 no 3 pp 687ndash694 2002

[131] I Dionne R K Nookala S P Jackson A J Doherty andS D Bell ldquoA heterotrimeric PCNA in the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Cell vol 11 no 1pp 275ndash282 2003

[132] E Warbrick ldquoPCNA binding through a conserved motifrdquoBioEssays vol 20 no 3 pp 195ndash199 1998

[133] H Nishida K Mayanagi S Kiyonari et al ldquoStructural deter-minant for switching between the polymerase and exonucleasemodes in the PCNA-replicative DNA polymerase complexrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 106 no 49 pp 20693ndash20698 2009

[134] K Mayanagi S Kiyonari H Nishida et al ldquoArchitecture of theDNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complexrdquo Proceedings of the National Academy ofSciences of the United States of America vol 108 no 5 pp 1845ndash1849 2011

[135] B Castrec C Rouillon G Henneke D Flament J Querellouand J-P Raffin ldquoBinding to PCNA in Euryarchaeal DNA

replication requires two PIP motifs for DNA polymerase D andone PIP motif for DNA polymerase Brdquo Journal of MolecularBiology vol 394 no 2 pp 209ndash218 2009

[136] P F Pluchon T Fouqueau C Creze et al ldquoAn extendednetworkof genomic maintenance in the archaeon Pyrococcus abyssihighlights unexpected associations between eucaryotic homo-logsrdquo PLoS One vol 8 no 11 Article ID e79707 2013

[137] J E Ladner M Pan J Hurwitz and Z Kelman ldquoCrystalstructures of two active proliferating cell nuclear antigens(PCNAs) encoded byThermococcus kodakaraensisrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2711ndash2716 2011

[138] Y Kuba S Ishino T Yamagami et al ldquoComparative analyses ofthe two proliferating cell nuclear antigens from the hyperther-mophilic archaeonThermococcus kodakarensisrdquo Genes to Cellsvol 17 no 11 pp 923ndash937 2012

[139] T Fukui H Atomi T Kanai R Matsumi S Fujiwara andT Imanaka ldquoComplete genome sequence of the hyperther-mophilic archaeon Thermococcus kodakaraensis KOD1 andcomparison with Pyrococcus genomesrdquo Genome Research vol15 no 3 pp 352ndash363 2005

[140] D Jeruzalmi O Yurieva Y Zhao et al ldquoMechanism of proces-sivity clamp opening by the delta subunit wrench of the clamploader complex of E coliDNApolymerase IIIrdquoCell vol 106 no4 pp 417ndash428 2001

[141] Y Shiomi J Usukura Y Masamura et al ldquoATP-dependentstructural change of the eukaryotic clamp-loader protein repli-cation factor Crdquo Proceedings of the National Academy of Sciencesof the United States of America vol 97 no 26 pp 14127ndash141322000

[142] T Miyata T Oyama K Mayanagi S Ishino Y Ishino and KMorikawa ldquoThe clamp-loading complex for processive DNAreplicationrdquoNature Structural andMolecular Biology vol 11 no7 pp 632ndash636 2004

[143] T Oyama Y Ishino I K O Cann S Ishino and K MorikawaldquoAtomic structure of the clamp loader small subunit fromPyrococcus furiosusrdquo Molecular Cell vol 8 no 2 pp 455ndash4632001

[144] A Seybert D J Scott S Scaife M R Singleton and DB Wigley ldquoBiochemical characterisation of the clampclamploader proteins from the euryarchaeon Archaeoglobus fulgidusrdquoNucleic Acids Research vol 30 no 20 pp 4329ndash4338 2002

[145] Y-H Chen Y Lin A Yoshinaga et al ldquoMolecular analyses of athree-subunit euryarchaeal clamp loader complex from Meth-anosarcina acetivoransrdquo Journal of Bacteriology vol 191 no 21pp 6539ndash6549 2009

[146] Y-H Chen S A Kocherginskaya Y Lin et al ldquoBiochemicaland mutational analyses of a unique clamp loader complex inthe archaeon Methanosarcina acetivoransrdquo The Journal of Bio-logical Chemistry vol 280 no 51 pp 41852ndash41863 2005

[147] F Matsunaga C Norais P Forterre and H Myllykallio ldquoIden-tification of short ldquoeukaryoticrdquo Okazaki fragments synthesizedfrom a prokaryotic replication originrdquo EMBO Reports vol 4no 2 pp 154ndash158 2003

[148] H Kochiwa M Tomita and A Kanai ldquoEvolution of ribonucle-ase H genes in prokaryotes to avoid inheritance of redundantgenesrdquo BMC Evolutionary Biology vol 7 article 128 2007

[149] N OhtaniMHarukiMMorikawa and S Kanaya ldquoMoleculardiversities of RNases Hrdquo Journal of Bioscience and Bioengineer-ing vol 88 no 1 pp 12ndash19 1999

Archaea 15

[150] N Ohtani M Haruki M Morikawa R J Crouch M Itayaand S Kanaya ldquoIdentification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII fromBacillus subtilis classification of RNases H into three familiesrdquoBiochemistry vol 38 no 2 pp 605ndash618 1999

[151] N Ohtani H Yanagawa M Tomita and M Itaya ldquoIdentifi-cation of the first archaeal type 1 RNase H gene from Halobac-terium sp NRC-1 archaeal RNase HI can cleave an RNA-DNAjunctionrdquoThe Biochemical Journal vol 381 no 3 pp 795ndash8022004

[152] N Ohtani H Yanagawa M Tomita and M Itaya ldquoCleavage ofdouble-stranded RNA by RNase HI from a thermoacidophilicarchaeon Sulfolobus tokodaii 7rdquo Nucleic Acids Research vol 32no 19 pp 5809ndash5819 2004

[153] M A Nowak M C Boerlijst J Cooke and J M SmithldquoEvolution of genetic redundancyrdquo Nature vol 388 no 6638pp 167ndash170 1997

[154] A E Tomkinson S Vijayakumar J M Pascal and T Ellen-berger ldquoDNA ligases structure reactionmechanism and func-tionrdquo Chemical Reviews vol 106 no 2 pp 687ndash699 2006

[155] M Nakatani S Ezaki H Atomi and T Imanaka ldquoA DNAligase from a hyperthermophilic archaeon with unique cofactorspecificityrdquo Journal of Bacteriology vol 182 no 22 pp 6424ndash6433 2000

[156] Y Sun M S Seo J H Kim et al ldquoNovel DNA ligase with broadnucleotide cofactor specificity from the hyperthermophilic cre-narchaeon Sulfophobococcus zilligii influence of ancestral DNAligase on cofactor utilizationrdquo Environmental Microbiology vol10 no 12 pp 3212ndash3224 2008

[157] T R Beattie and S D Bell ldquoCoordination of multiple enzymeactivities by a single PCNA in archaeal Okazaki fragmentmaturationrdquo The EMBO Journal vol 31 no 6 pp 1556ndash15672012

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

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BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

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Nucleic AcidsJournal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Archaea 11

[24] A F Andersson E A Pelve S LindebergM Lundgren P Nils-son and R Bernander ldquoReplication-biased genome organisa-tion in the crenarchaeon Sulfolobusrdquo BMCGenomics vol 11 no1 article 454 2010

[25] H Myllykallio P Lopez P Lopez-Garcıa et al ldquoBacterial modeof replication with eukaryotic-like machinery in a hyperther-mophilic archaeonrdquo Science vol 288 no 5474 pp 2212ndash22152000

[26] F Matsunaga P Forterre Y Ishino and H Myllykallio ldquoInvivo interactions of archaeal Cdc6Orc1 and minichromosomemaintenance proteins with the replication originrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 98 no 20 pp 11152ndash11157 2001

[27] S Maisnier-Patin L Malandrin N K Birkeland and RBernander ldquoChromosome replication patterns in the hyper-thermophilic euryarchaeaArchaeoglobus fulgidus andMethano-caldococcus (Methanococcus) jannaschiirdquo Molecular Microbiol-ogy vol 45 no 5 pp 1443ndash1450 2002

[28] R Zhang and C-T Zhang ldquoMultiple replication origins ofthe archaeon Halobacterium species NRC-1rdquo Biochemical andBiophysical Research Communications vol 302 no 4 pp 728ndash734 2003

[29] C Norais M Hawkins A L Hartman J A Eisen H Myl-lykallio and T Allers ldquoGenetic and physical mapping of DNAreplication origins in Haloferax volcaniirdquo PLoS Genetics vol 3no 5 article e77 2007

[30] J A Coker P DasSarma M Capes et al ldquoMultiple replicationorigins of Halobacterium sp strain NRC-1 properties of theconserved orc7-dependent oriC1rdquo Journal of Bacteriology vol191 no 16 pp 5253ndash5261 2009

[31] Z Wu J Liu H Yang H Liu and H Xiang ldquoMultiple repli-cation origins with diverse control mechanisms in Haloarculahispanicardquo Nucleic Acids Research 2013

[32] M Hawkins S Malla M J Blythe C A Nieduszynski and TAllers ldquoAccelerated growth in the absence of DNA replicationoriginsrdquo Nature vol 503 no 7477 pp 544ndash547 2013

[33] A I Majernık and J P J Chong ldquoA conserved mechanismfor replication origin recognition and binding in archaeardquo TheBiochemical Journal vol 409 no 2 pp 511ndash518 2008

[34] J E Galagan C Nusbaum A Roy et al ldquoThe genome of Macetivorans reveals extensive metabolic and physiological diver-sityrdquo Genome Research vol 12 no 4 pp 532ndash542 2002

[35] R Zhang and C-T Zhang ldquoIdentification of replication originsin archaeal genomes based on the Z-curve methodrdquo Archaeavol 1 no 5 pp 335ndash346 2005

[36] A Spang R Hatzenpichler C Brochier-Armanet et al ldquoDis-tinct gene set in two different lineages of ammonia-oxidizingarchaea supports the phylum Thaumarchaeotardquo Trends inMicrobiology vol 18 no 8 pp 331ndash340 2010

[37] K J Marians ldquoProkaryotic DNA replicationrdquo Annual Review ofBiochemistry vol 61 pp 673ndash719 1992

[38] S P Bell ldquoThe origin recognition complex from simple originsto complex functionsrdquo Genes and Development vol 16 no 6pp 659ndash672 2002

[39] V L Marsh and S D Bell ldquoDNA replication and the cell cyclerdquoin Archaea Evolution Physiology and Molecular Biology R AGarrett and H P Klenk Eds Blackwell Publishing HobokenNJ USA 2007

[40] F Matsunaga A Glatigny M-H Mucchielli-Giorgi et alldquoGenomewide and biochemical analyses of DNA-binding activ-ity of Cdc6Orc1 and Mcm proteins in Pyrococcus sprdquo NucleicAcids Research vol 35 no 10 pp 3214ndash3222 2007

[41] J Liu C L Smith D DeRyckere K DeAngelis G S Martinand J M Berger ldquoStructure and function of Cdc6Cdc18implications for origin recognition and checkpoint controlrdquoMolecular Cell vol 6 no 3 pp 637ndash648 2000

[42] M R Singleton R Morales I Grainge N Cook M NIsupov and D B Wigley ldquoConformational changes inducedby nucleotide binding in Cdc6ORC from Aeropyrum pernixrdquoJournal of Molecular Biology vol 343 no 3 pp 547ndash557 2004

[43] Y Ishino and S Ishino ldquoRapid progress of DNA replicationstudies in Archaea the third domain of liferdquo Science China LifeSciences vol 55 no 5 pp 386ndash403 2012

[44] E L Hendrickson R Kaul Y Zhou et al ldquoComplete genomesequence of the genetically tractable hydrogenotrophic meth-anogen Methanococcus maripaludisrdquo Journal of Bacteriologyvol 186 no 20 pp 6956ndash6969 2004

[45] B K Tye ldquoMCM proteins in DNA replicationrdquo Annual Reviewof Biochemistry vol 68 pp 649ndash686 1999

[46] K Labib and J F X Diffley ldquoIs the MCM2-7 complex theeukaryotic DNA replication fork helicaserdquo Current Opinion inGenetics amp Development vol 11 no 1 pp 64ndash70 2001

[47] I Ilves T Petojevic J J Pesavento and M R Botchan ldquoActi-vation of the MCM2-7 helicase by association with Cdc45 andGINS proteinsrdquoMolecular Cell vol 37 no 2 pp 247ndash258 2010

[48] M L Bochman andA Schwacha ldquoTheMcm complex unwind-ing the mechanism of a replicative helicaserdquo Microbiology andMolecular Biology Reviews vol 73 no 4 pp 652ndash683 2009

[49] Y Ishimi ldquoADNAhelicase activity is associated with anMCM4-6 and -7 protein complexrdquoThe Journal of Biological Chemistryvol 272 no 39 pp 24508ndash24513 1997

[50] Z Kelman and M F White ldquoArchaeal DNA replication andrepairrdquo Current Opinion in Microbiology vol 8 no 6 pp 669ndash676 2005

[51] J H LeBowitz and R McMacken ldquoThe Escherichia coli dnaBreplication protein is a DNA helicaserdquoThe Journal of BiologicalChemistry vol 261 no 10 pp 4738ndash4748 1986

[52] Z Kelman J-K Lee and J Hurwitz ldquoThe single minichro-mosome maintenance protein ofMethanobacterium thermoau-totrophicum ΔH contains DNA helicase activityrdquo Proceedings ofthe National Academy of Sciences of the United States of Americavol 96 no 26 pp 14783ndash14788 1999

[53] D F Shechter C Y Ying and J Gautier ldquoThe intrinsic DNAhelicase activity of Methanobacterium thermoautotrophicumΔH minichromosome maintenance proteinrdquo The Journal ofBiological Chemistry vol 275 no 20 pp 15049ndash15059 2000

[54] M de Felice L Esposito B Pucci M de Falco M Rossi andF M Pisani ldquoA CDC6-like factor from the archaea Sulfolobussolfataricus promotes binding of the mini-chromosome main-tenance complex to DNArdquoThe Journal of Biological Chemistryvol 279 no 41 pp 43008ndash43012 2004

[55] R Kasiviswanathan J-H Shin and Z Kelman ldquoInteractionsbetween the archaeal Cdc6 and MCM proteins modulate theirbiochemical propertiesrdquo Nucleic Acids Research vol 33 no 15pp 4940ndash4950 2005

[56] J-H Shin B Grabowski R Kasiviswanathan S D Bell andZ Kelman ldquoRegulation of minichromosomemaintenance heli-case activity by Cdc6rdquo The Journal of Biological Chemistry vol278 no 39 pp 38059ndash38067 2003

[57] M Akita A Adachi K Takemura T Yamagami F Matsunagaand Y Ishino ldquoCdc6Orc1 from Pyrococcus furiosus may actas the origin recognition protein and Mcm helicase recruiterrdquoGenes to Cells vol 15 no 5 pp 537ndash552 2010

12 Archaea

[58] M Krupovic S Gribaldo D H Bamford and P Forterre ldquoTheevolutionary history of archaeal MCM helicases a case study ofvertical evolution combined with hitchhiking of mobile geneticelementsrdquo Molecular Biology and Evolution vol 27 no 12 pp2716ndash2732 2010

[59] ADWalters and J P J Chong ldquoAn archaeal orderwithmultipleminichromosome maintenance genesrdquo Microbiology vol 156part 5 pp 1405ndash1414 2010

[60] A DWalters and J P J Chong ldquoMethanococcusmaripaludis anarchaeon with multiple functional MCM proteinsrdquo Biochemi-cal Society Transactions vol 37 no 1 pp 1ndash6 2009

[61] Q Xia E L Hendrickson Y Zhang et al ldquoQuantitative pro-teomics of the archaeon Methanococcus maripaludis validatedbymicroarray analysis and real time PCRrdquoMolecularampCellularProteomics vol 5 no 5 pp 868ndash881 2006

[62] F Sarmiento J Mrazek and W B Whitman ldquoGenome-scaleanalysis of gene function in the hydrogenotrophic methano-genic archaeon Methanococcus maripaludisrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 110 no 12 pp 4726ndash4731 2013

[63] M Pan T J Santangelo Z Li J N Reeve and Z KelmanldquoThermococcus kodakarensis encodes threeMCMhomologs butonly one is essentialrdquo Nucleic Acids Research vol 39 no 22 pp9671ndash9680 2011

[64] S Ishino S Fujino H Tomita et al ldquoBiochemical and geneticalanalyses of the three mcm genes from the hyperthermophilicarchaeon Thermococcus kodakarensisrdquo Genes to Cells vol 16no 12 pp 1176ndash1189 2011

[65] K S Makarova Y I Wolf S L Mekhedov B G Mirkin and EV Koonin ldquoAncestral paralogs and pseudoparalogs and theirrole in the emergence of the eukaryotic cellrdquo Nucleic AcidsResearch vol 33 no 14 pp 4626ndash4638 2005

[66] N Marinsek E R Barry K S Makarova I Dionne E VKoonin and S D Bell ldquoGINS a central nexus in the archaealDNA replication forkrdquo EMBOReports vol 7 no 5 pp 539ndash5452006

[67] T Yoshimochi R Fujikane M Kawanami F Matsunaga and YIshino ldquoTheGINS complex from Pyrococcus furiosus stimulatesthe MCM helicase activityrdquoThe Journal of Biological Chemistryvol 283 no 3 pp 1601ndash1609 2008

[68] T Oyama S Ishino S Fujino et al ldquoArchitectures of archaealGINS complexes essential DNA replication initiation factorsrdquoBMC Biology vol 9 article 28 2011

[69] H Ogino S Ishino K Mayanagi et al ldquoThe GINS com-plex from the thermophilic archaeon Thermoplasma aci-dophilummay function as a homotetramer inDNA replicationrdquoExtremophiles vol 15 no 4 pp 529ndash539 2011

[70] L Sanchez-Pulido and C P Ponting ldquoCdc45 the missing recjortholog in eukaryotesrdquoBioinformatics vol 27 no 14 pp 1885ndash1888 2011

[71] Z Li T J Santangelo L Cubonova J N Reeve and Z KelmanldquoAffinity purification of an archaeal DNA replication proteinnetworkrdquomBio vol 1 no 5 2010

[72] Z Li M Pan T J Santangelo et al ldquoA novel DNA nucleaseis stimulated by association with the GINS complexrdquo NucleicAcids Research vol 39 no 14 pp 6114ndash6123 2011

[73] L A Rajman and S T Lovett ldquoA thermostable single-strandDNase from Methanococcus jannaschii related to the RecJrecombination and repair exonuclease from Escherichia colirdquoJournal of Bacteriology vol 182 no 3 pp 607ndash612 2000

[74] K RWilliams J B Murphy and JW Chase ldquoCharacterizationof the structural and functional defect in the Escherichia colisingle-stranded DNA binding protein encoded by the ssb-1 mutant gene Expression of the ssb-1 gene under 120582p(L)regulationrdquoThe Journal of Biological Chemistry vol 259 no 19pp 11804ndash11811 1984

[75] S Dąbrowski M Olszewski R Pitek and J Kur ldquoNovel ther-mostable ssDNA-binding proteins fromThermus thermophilusand T aquaticus-expression and purificationrdquo Protein Expres-sion and Purification vol 26 no 1 pp 131ndash138 2002

[76] C Iftode Y Daniely and J A Borowiec ldquoReplication proteinA (RPA) the eukaryotic SSBrdquo Critical Reviews in Biochemistryand Molecular Biology vol 34 no 3 pp 141ndash180 1999

[77] A G Murzin ldquoOB(oligonucleotideoligosaccharide binding)-fold common structural and functional solution for non-hom-ologous sequencesrdquo The EMBO Journal vol 12 no 3 pp 861ndash867 1993

[78] C A Haseltine and S C Kowalczykowski ldquoA distinctive single-stranded DNA-binding protein from the Archaeon Sulfolobussolfataricusrdquo Molecular Microbiology vol 43 no 6 pp 1505ndash1515 2002

[79] R I M Wadsworth and M F White ldquoIdentification and pro-perties of the crenarchaeal single-stranded DNA binding pro-tein from Sulfolobus solfataricusrdquoNucleic Acids Research vol 29no 4 pp 914ndash920 2001

[80] I D Kerr R I M Wadsworth L Cubeddu W Blankenfeldt JHNaismith andM FWhite ldquoInsights into ssDNA recognitionby the OB fold from a structural and thermodynamic study ofSulfolobus SSB proteinrdquo The EMBO Journal vol 22 no 11 pp2561ndash2570 2003

[81] X Luo U Schwarz-Linek C H Botting R Hensel B Siebersand M F White ldquoCC1 a novel crenarchaeal DNA binding pro-teinrdquo Journal of Bacteriology vol 189 no 2 pp 403ndash409 2007

[82] T J Kelly P Simancek and G S Brush ldquoIdentification andcharacterization of a single-stranded DNA-binding proteinfrom the archaeonMethanococcus jannaschiirdquoProceedings of theNational Academy of Sciences of theUnited States of America vol95 no 25 pp 14634ndash14639 1998

[83] Z Kelman S Pietrokovski and J Hurwitz ldquoIsolation and cha-racterization of a split B-type DNA polymerase from the arch-aeonMethanobacterium thermoautotrophicumΔHrdquoTheJournalof Biological Chemistry vol 274 no 40 pp 28751ndash28761 1999

[84] K Komori and Y Ishino ldquoReplication protein A in Pyrococcusfuriosus is involved in homologous DNA recombinationrdquo TheJournal of Biological Chemistry vol 276 no 28 pp 25654ndash25660 2001

[85] J B Robbins M C Murphy B A White R I Mackie THa and I K O Cann ldquoFunctional analysis of multiple single-stranded DNA-binding proteins from Methanosarcina acetivo-rans and their effects on DNA synthesis by DNA polymeraseBIrdquoThe Journal of Biological Chemistry vol 279 no 8 pp 6315ndash6326 2004

[86] Y Lin L-J Lin P Sriratana et al ldquoEngineering of functionalreplication protein a homologs based on insights into the evolu-tion of oligonucleotideoligosaccharide-binding foldsrdquo Journalof Bacteriology vol 190 no 17 pp 5766ndash5780 2008

[87] D N Frick and C C Richardson ldquoDNA primasesrdquo AnnualReview of Biochemistry vol 70 pp 39ndash80 2001

[88] G Desogus S Onesti P Brick M Rossi and F M PisanildquoIdentification and characterization of a DNA primase fromthe hyperthermophilic archaeon Methanococcus jannaschiirdquoNucleic Acids Research vol 27 no 22 pp 4444ndash4450 1999

Archaea 13

[89] A A Bocquier L Liu I K O Cann K Komori D Kohda andY Ishino ldquoArchaeal primase bridging the gap between RNAand DNA polymerasesrdquo Current Biology vol 11 no 6 pp 452ndash456 2001

[90] L Liu K Komori S Ishino et al ldquoThe archaeal DNA primasebiochemical characterization of the p41-p46 complex fromPyrococcus furiosusrdquo The Journal of Biological Chemistry vol276 no 48 pp 45484ndash45490 2001

[91] E Matsui M Nishio H Yokoyama K Harata S Darnisand I Matsui ldquoDistinct domain functions regulating de novoDNA synthesis of thermostable DNA primase from hyperther-mophile Pyrococcus horikoshiirdquo Biochemistry vol 42 no 50 pp14968ndash14976 2003

[92] N Ito I Matsui and EMatsui ldquoMolecular basis for the subunitassembly of the primase from an archaeon Pyrococcus hori-koshiirdquoThe FEBS Journal vol 274 no 5 pp 1340ndash1351 2007

[93] M le Breton G Henneke C Norais et al ldquoThe heterodimericprimase from the euryarchaeon Pyrococcus abyssi a multifunc-tional enzyme for initiation and repairrdquo Journal of MolecularBiology vol 374 no 5 pp 1172ndash1185 2007

[94] S-H Lao-Sirieix and S D Bell ldquoThe heterodimeric primaseof the hyperthermophilic archaeon Sulfolobus solfataricus pos-sesses DNA and RNA primase polymerase and 31015840-terminalnucleotidyl transferase activitiesrdquo Journal of Molecular Biologyvol 344 no 5 pp 1251ndash1263 2004

[95] S-H Lao-Sirieix L Pellegrini and S D Bell ldquoThe promiscuousprimaserdquo Trends in Genetics vol 21 no 10 pp 568ndash572 2005

[96] J Hu L Guo K Wu B Liu S Lang and L Huang ldquoTemplate-dependent polymerization across discontinuous templatesby the heterodimeric primase from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquoNucleic Acids Research vol 40no 8 pp 3470ndash3483 2012

[97] E Evguenieva-Hackenberg P Walter E Hochleitner FLottspeich and G Klug ldquoAn exosome-like complex in Sulfolo-bus solfataricusrdquo EMBOReports vol 4 no 9 pp 889ndash893 2003

[98] P Walter F Klein E Lorentzen A Ilchmann G Klug andE Evguenieva-Hackenberg ldquoCharacterization of native andreconstituted exosome complexes from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Microbiology vol62 no 4 pp 1076ndash1089 2006

[99] Z Zuo C J Rodgers A L Mikheikin and M A Trak-selis ldquoCharacterization of a functional DnaG-type primase inarchaea implications for a dual-primase systemrdquo Journal ofMolecular Biology vol 397 no 3 pp 664ndash676 2010

[100] B R Berquist P DasSarma and S DasSarma ldquoEssential andnon-essential DNA replication genes in the model halophilicArchaeon Halobacterium sp NRC-1rdquo BMC Genetics vol 8article 31 2007

[101] D K Braithwaite and J Ito ldquoCompilation alignment andphylogenetic relationships of DNA polymerasesrdquo Nucleic AcidsResearch vol 21 no 4 pp 787ndash802 1993

[102] I K O Cann and Y Ishino ldquoArchaeal DNA replication iden-tifying the pieces to solve a puzzlerdquo Genetics vol 152 no 4 pp1249ndash1267 1999

[103] G Lipps S Rother C Hart and G Krauss ldquoA novel typeof replicative enzyme harbouring ATpase primase and DNApolymerase activityrdquo The EMBO Journal vol 22 no 10 pp2516ndash2525 2003

[104] J Yamtich and J B Sweasy ldquoDNA polymerase family X func-tion structure and cellular rolesrdquoBiochimica et BiophysicaActavol 1804 no 5 pp 1136ndash1150 2010

[105] H Ohmori E C Friedberg R P P Fuchs et al ldquoThe Y-familyof DNA polymerasesrdquoMolecular Cell vol 8 no 1 pp 7ndash8 2001

[106] N Y Yao R E Georgescu J Finkelstein and M E OrsquoDonnellldquoSingle-molecule analysis reveals that the lagging strandincreases replisome processivity but slows replication forkprogressionrdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 106 no 32 pp 13236ndash132412009

[107] U Hubscher G Maga and S Spadari ldquoEukaryotic DNA poly-merasesrdquo Annual Review of Biochemistry vol 71 pp 133ndash1632002

[108] F Boudsocq S Iwai F Hanaoka and R Woodgate ldquoSulfolobussolfataricus P2 DNA polymerase IV (Dp04) an archaeal DinB-like DNA polymerase with lesion-bypass properties akin toeukaryotic pol120578rdquo Nucleic Acids Research vol 29 no 22 pp4607ndash4616 2001

[109] L-J Lin A Yoshinaga Y Lin et al ldquoMolecular analyses ofan unusual translesion DNA polymerase fromMethanosarcinaacetivorans C2Ardquo Journal of Molecular Biology vol 397 no 1pp 13ndash30 2010

[110] I K O Cann S Ishino NNomura Y Sako andY Ishino ldquoTwofamily B DNA polymerases from Aeropyrum pernix an aerobichyperthermophilic crenarchaeoterdquo Journal of Bacteriology vol181 no 19 pp 5984ndash5992 1999

[111] T Uemori Y Ishino H Doi and I Kato ldquoThe hyperther-mophilic archaeon Pyrodictium occultum has two 120572-like DNApolymerasesrdquo Journal of Bacteriology vol 177 no 8 pp 2164ndash2177 1995

[112] T Uemori Y Ishino H Toh K Asada and I Kato ldquoOrgani-zation and nucleotide sequence of the DNA polymerase genefrom the archaeon Pyrococcus furiosusrdquo Nucleic Acids Researchvol 21 no 2 pp 259ndash265 1993

[113] B A Connolly ldquoRecognition of deaminated bases by archaealfamily-B DNA polymerasesrdquo Biochemical Society Transactionsvol 37 no 1 pp 65ndash68 2009

[114] B A Connolly M J Fogg G Shuttleworth and B T WilsonldquoUracil recognition by archaeal family B DNA polymerasesrdquoBiochemical Society Transactions vol 31 no 3 pp 699ndash7022003

[115] T T Richardson X Wu B J Keith P Heslop A C Jones andB A Connolly ldquoUnwinding of primer-templates by archaealfamily-B DNA polymerases in response to template-stranduracilrdquo Nucleic Acids Research vol 41 no 4 pp 2466ndash24782013

[116] T Lindahl ldquoInstability and decay of the primary structure ofDNArdquo Nature vol 362 no 6422 pp 709ndash715 1993

[117] I B Rogozin K S Makarova Y I Pavlov and E V Koonin ldquoAhighly conserved family of inactivated archaeal B family DNApolymerasesrdquo Biology Direct vol 3 article 32 2008

[118] M Imamura T Uemori I Kato and Y Ishino ldquoA non-120572-like DNA polymerase from the hyperthermophilic archaeonPyrococcus furiosusrdquoBiological andPharmaceutical Bulletin vol18 no 12 pp 1647ndash1652 1995

[119] I K O Cann K Komori H Toh S Kanai and Y IshinoldquoA heterodimeric DNA polymerase evidence that members ofEuryarchaeota possess a distinct DNA polymeraserdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 95 no 24 pp 14250ndash14255 1998

[120] L Aravind D D Leipe and E V Koonin ldquoToprimmdasha con-served catalytic domain in type IA and II topoisomerases

14 Archaea

DnaG-type primases OLD family nucleases and RecR pro-teinsrdquo Nucleic Acids Research vol 26 no 18 pp 4205ndash42131998

[121] M Jokela A Eskelinen H Pospiech J Rouvinen and J ESyvaoja ldquoCharacterization of the 31015840 exonuclease subunit DP1of Methanococcus jannaschii replicative DNA polymerase DrdquoNucleic Acids Research vol 32 no 8 pp 2430ndash2440 2004

[122] T Uemori Y Sato I Kato H Doi and Y Ishino ldquoA novel DNApolymerase in the hyperthermophilic archaeon Pyrococcus fur-iosus gene cloning expression and characterizationrdquo Genes toCells vol 2 no 8 pp 499ndash512 1997

[123] Y Shen K Musti M Hiramoto H Kikuchi Y Kawarabayashiand I Matsui ldquoInvariant Asp-1122 and Asp-1124 are essentialresidues for polymerization catalysis of family D DNA poly-merase from Pyrococcus horikoshiirdquo The Journal of BiologicalChemistry vol 276 no 29 pp 27376ndash27383 2001

[124] G Henneke D Flament U Hubscher J Querellou and J-P Raffin ldquoThe hyperthermophilic euryarchaeota Pyrococcusabyssi likely requires the two DNA polymerases D and B forDNA replicationrdquo Journal of Molecular Biology vol 350 no 1pp 53ndash64 2005

[125] L Cubonova T Richardson B W Burkhart et al ldquoArchaealDNA polymerase D but not DNA polymerase B is required forgenome replication in Thermococcus kodakarensisrdquo Journal ofBacteriology vol 195 no 10 pp 2322ndash2328 2013

[126] C Rouillon G Henneke D Flament J Querellou and J-PRaffin ldquoDNA polymerase switching on homotrimeric PCNA atthe replication fork of the euryarchaea Pyrococcus abyssirdquo Jour-nal of Molecular Biology vol 369 no 2 pp 343ndash355 2007

[127] G Henneke ldquoIn vitro reconstitution of RNA primer removal inArchaea reveals the existence of two pathwaysrdquoTheBiochemicalJournal vol 447 no 2 pp 271ndash280 2012

[128] G-LMoldovan B Pfander and S Jentsch ldquoPCNA themaestroof the replication forkrdquo Cell vol 129 no 4 pp 665ndash679 2007

[129] X-P Kong R Onrust M OrsquoDonnell and J Kuriyan ldquoThree-dimensional structure of the 120573 subunit of E coli DNA poly-merase III holoenzyme a sliding DNA clamprdquo Cell vol 69 no3 pp 425ndash437 1992

[130] K Daimon Y Kawarabayasi H Kikuchi Y Sako and Y IshinoldquoThree proliferating cell nuclear antigen-like proteins foundin the hyperthermophilic archaeon Aeropyrum pemix interac-tions with the two DNA polymerasesrdquo Journal of Bacteriologyvol 184 no 3 pp 687ndash694 2002

[131] I Dionne R K Nookala S P Jackson A J Doherty andS D Bell ldquoA heterotrimeric PCNA in the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Cell vol 11 no 1pp 275ndash282 2003

[132] E Warbrick ldquoPCNA binding through a conserved motifrdquoBioEssays vol 20 no 3 pp 195ndash199 1998

[133] H Nishida K Mayanagi S Kiyonari et al ldquoStructural deter-minant for switching between the polymerase and exonucleasemodes in the PCNA-replicative DNA polymerase complexrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 106 no 49 pp 20693ndash20698 2009

[134] K Mayanagi S Kiyonari H Nishida et al ldquoArchitecture of theDNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complexrdquo Proceedings of the National Academy ofSciences of the United States of America vol 108 no 5 pp 1845ndash1849 2011

[135] B Castrec C Rouillon G Henneke D Flament J Querellouand J-P Raffin ldquoBinding to PCNA in Euryarchaeal DNA

replication requires two PIP motifs for DNA polymerase D andone PIP motif for DNA polymerase Brdquo Journal of MolecularBiology vol 394 no 2 pp 209ndash218 2009

[136] P F Pluchon T Fouqueau C Creze et al ldquoAn extendednetworkof genomic maintenance in the archaeon Pyrococcus abyssihighlights unexpected associations between eucaryotic homo-logsrdquo PLoS One vol 8 no 11 Article ID e79707 2013

[137] J E Ladner M Pan J Hurwitz and Z Kelman ldquoCrystalstructures of two active proliferating cell nuclear antigens(PCNAs) encoded byThermococcus kodakaraensisrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2711ndash2716 2011

[138] Y Kuba S Ishino T Yamagami et al ldquoComparative analyses ofthe two proliferating cell nuclear antigens from the hyperther-mophilic archaeonThermococcus kodakarensisrdquo Genes to Cellsvol 17 no 11 pp 923ndash937 2012

[139] T Fukui H Atomi T Kanai R Matsumi S Fujiwara andT Imanaka ldquoComplete genome sequence of the hyperther-mophilic archaeon Thermococcus kodakaraensis KOD1 andcomparison with Pyrococcus genomesrdquo Genome Research vol15 no 3 pp 352ndash363 2005

[140] D Jeruzalmi O Yurieva Y Zhao et al ldquoMechanism of proces-sivity clamp opening by the delta subunit wrench of the clamploader complex of E coliDNApolymerase IIIrdquoCell vol 106 no4 pp 417ndash428 2001

[141] Y Shiomi J Usukura Y Masamura et al ldquoATP-dependentstructural change of the eukaryotic clamp-loader protein repli-cation factor Crdquo Proceedings of the National Academy of Sciencesof the United States of America vol 97 no 26 pp 14127ndash141322000

[142] T Miyata T Oyama K Mayanagi S Ishino Y Ishino and KMorikawa ldquoThe clamp-loading complex for processive DNAreplicationrdquoNature Structural andMolecular Biology vol 11 no7 pp 632ndash636 2004

[143] T Oyama Y Ishino I K O Cann S Ishino and K MorikawaldquoAtomic structure of the clamp loader small subunit fromPyrococcus furiosusrdquo Molecular Cell vol 8 no 2 pp 455ndash4632001

[144] A Seybert D J Scott S Scaife M R Singleton and DB Wigley ldquoBiochemical characterisation of the clampclamploader proteins from the euryarchaeon Archaeoglobus fulgidusrdquoNucleic Acids Research vol 30 no 20 pp 4329ndash4338 2002

[145] Y-H Chen Y Lin A Yoshinaga et al ldquoMolecular analyses of athree-subunit euryarchaeal clamp loader complex from Meth-anosarcina acetivoransrdquo Journal of Bacteriology vol 191 no 21pp 6539ndash6549 2009

[146] Y-H Chen S A Kocherginskaya Y Lin et al ldquoBiochemicaland mutational analyses of a unique clamp loader complex inthe archaeon Methanosarcina acetivoransrdquo The Journal of Bio-logical Chemistry vol 280 no 51 pp 41852ndash41863 2005

[147] F Matsunaga C Norais P Forterre and H Myllykallio ldquoIden-tification of short ldquoeukaryoticrdquo Okazaki fragments synthesizedfrom a prokaryotic replication originrdquo EMBO Reports vol 4no 2 pp 154ndash158 2003

[148] H Kochiwa M Tomita and A Kanai ldquoEvolution of ribonucle-ase H genes in prokaryotes to avoid inheritance of redundantgenesrdquo BMC Evolutionary Biology vol 7 article 128 2007

[149] N OhtaniMHarukiMMorikawa and S Kanaya ldquoMoleculardiversities of RNases Hrdquo Journal of Bioscience and Bioengineer-ing vol 88 no 1 pp 12ndash19 1999

Archaea 15

[150] N Ohtani M Haruki M Morikawa R J Crouch M Itayaand S Kanaya ldquoIdentification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII fromBacillus subtilis classification of RNases H into three familiesrdquoBiochemistry vol 38 no 2 pp 605ndash618 1999

[151] N Ohtani H Yanagawa M Tomita and M Itaya ldquoIdentifi-cation of the first archaeal type 1 RNase H gene from Halobac-terium sp NRC-1 archaeal RNase HI can cleave an RNA-DNAjunctionrdquoThe Biochemical Journal vol 381 no 3 pp 795ndash8022004

[152] N Ohtani H Yanagawa M Tomita and M Itaya ldquoCleavage ofdouble-stranded RNA by RNase HI from a thermoacidophilicarchaeon Sulfolobus tokodaii 7rdquo Nucleic Acids Research vol 32no 19 pp 5809ndash5819 2004

[153] M A Nowak M C Boerlijst J Cooke and J M SmithldquoEvolution of genetic redundancyrdquo Nature vol 388 no 6638pp 167ndash170 1997

[154] A E Tomkinson S Vijayakumar J M Pascal and T Ellen-berger ldquoDNA ligases structure reactionmechanism and func-tionrdquo Chemical Reviews vol 106 no 2 pp 687ndash699 2006

[155] M Nakatani S Ezaki H Atomi and T Imanaka ldquoA DNAligase from a hyperthermophilic archaeon with unique cofactorspecificityrdquo Journal of Bacteriology vol 182 no 22 pp 6424ndash6433 2000

[156] Y Sun M S Seo J H Kim et al ldquoNovel DNA ligase with broadnucleotide cofactor specificity from the hyperthermophilic cre-narchaeon Sulfophobococcus zilligii influence of ancestral DNAligase on cofactor utilizationrdquo Environmental Microbiology vol10 no 12 pp 3212ndash3224 2008

[157] T R Beattie and S D Bell ldquoCoordination of multiple enzymeactivities by a single PCNA in archaeal Okazaki fragmentmaturationrdquo The EMBO Journal vol 31 no 6 pp 1556ndash15672012

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

12 Archaea

[58] M Krupovic S Gribaldo D H Bamford and P Forterre ldquoTheevolutionary history of archaeal MCM helicases a case study ofvertical evolution combined with hitchhiking of mobile geneticelementsrdquo Molecular Biology and Evolution vol 27 no 12 pp2716ndash2732 2010

[59] ADWalters and J P J Chong ldquoAn archaeal orderwithmultipleminichromosome maintenance genesrdquo Microbiology vol 156part 5 pp 1405ndash1414 2010

[60] A DWalters and J P J Chong ldquoMethanococcusmaripaludis anarchaeon with multiple functional MCM proteinsrdquo Biochemi-cal Society Transactions vol 37 no 1 pp 1ndash6 2009

[61] Q Xia E L Hendrickson Y Zhang et al ldquoQuantitative pro-teomics of the archaeon Methanococcus maripaludis validatedbymicroarray analysis and real time PCRrdquoMolecularampCellularProteomics vol 5 no 5 pp 868ndash881 2006

[62] F Sarmiento J Mrazek and W B Whitman ldquoGenome-scaleanalysis of gene function in the hydrogenotrophic methano-genic archaeon Methanococcus maripaludisrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 110 no 12 pp 4726ndash4731 2013

[63] M Pan T J Santangelo Z Li J N Reeve and Z KelmanldquoThermococcus kodakarensis encodes threeMCMhomologs butonly one is essentialrdquo Nucleic Acids Research vol 39 no 22 pp9671ndash9680 2011

[64] S Ishino S Fujino H Tomita et al ldquoBiochemical and geneticalanalyses of the three mcm genes from the hyperthermophilicarchaeon Thermococcus kodakarensisrdquo Genes to Cells vol 16no 12 pp 1176ndash1189 2011

[65] K S Makarova Y I Wolf S L Mekhedov B G Mirkin and EV Koonin ldquoAncestral paralogs and pseudoparalogs and theirrole in the emergence of the eukaryotic cellrdquo Nucleic AcidsResearch vol 33 no 14 pp 4626ndash4638 2005

[66] N Marinsek E R Barry K S Makarova I Dionne E VKoonin and S D Bell ldquoGINS a central nexus in the archaealDNA replication forkrdquo EMBOReports vol 7 no 5 pp 539ndash5452006

[67] T Yoshimochi R Fujikane M Kawanami F Matsunaga and YIshino ldquoTheGINS complex from Pyrococcus furiosus stimulatesthe MCM helicase activityrdquoThe Journal of Biological Chemistryvol 283 no 3 pp 1601ndash1609 2008

[68] T Oyama S Ishino S Fujino et al ldquoArchitectures of archaealGINS complexes essential DNA replication initiation factorsrdquoBMC Biology vol 9 article 28 2011

[69] H Ogino S Ishino K Mayanagi et al ldquoThe GINS com-plex from the thermophilic archaeon Thermoplasma aci-dophilummay function as a homotetramer inDNA replicationrdquoExtremophiles vol 15 no 4 pp 529ndash539 2011

[70] L Sanchez-Pulido and C P Ponting ldquoCdc45 the missing recjortholog in eukaryotesrdquoBioinformatics vol 27 no 14 pp 1885ndash1888 2011

[71] Z Li T J Santangelo L Cubonova J N Reeve and Z KelmanldquoAffinity purification of an archaeal DNA replication proteinnetworkrdquomBio vol 1 no 5 2010

[72] Z Li M Pan T J Santangelo et al ldquoA novel DNA nucleaseis stimulated by association with the GINS complexrdquo NucleicAcids Research vol 39 no 14 pp 6114ndash6123 2011

[73] L A Rajman and S T Lovett ldquoA thermostable single-strandDNase from Methanococcus jannaschii related to the RecJrecombination and repair exonuclease from Escherichia colirdquoJournal of Bacteriology vol 182 no 3 pp 607ndash612 2000

[74] K RWilliams J B Murphy and JW Chase ldquoCharacterizationof the structural and functional defect in the Escherichia colisingle-stranded DNA binding protein encoded by the ssb-1 mutant gene Expression of the ssb-1 gene under 120582p(L)regulationrdquoThe Journal of Biological Chemistry vol 259 no 19pp 11804ndash11811 1984

[75] S Dąbrowski M Olszewski R Pitek and J Kur ldquoNovel ther-mostable ssDNA-binding proteins fromThermus thermophilusand T aquaticus-expression and purificationrdquo Protein Expres-sion and Purification vol 26 no 1 pp 131ndash138 2002

[76] C Iftode Y Daniely and J A Borowiec ldquoReplication proteinA (RPA) the eukaryotic SSBrdquo Critical Reviews in Biochemistryand Molecular Biology vol 34 no 3 pp 141ndash180 1999

[77] A G Murzin ldquoOB(oligonucleotideoligosaccharide binding)-fold common structural and functional solution for non-hom-ologous sequencesrdquo The EMBO Journal vol 12 no 3 pp 861ndash867 1993

[78] C A Haseltine and S C Kowalczykowski ldquoA distinctive single-stranded DNA-binding protein from the Archaeon Sulfolobussolfataricusrdquo Molecular Microbiology vol 43 no 6 pp 1505ndash1515 2002

[79] R I M Wadsworth and M F White ldquoIdentification and pro-perties of the crenarchaeal single-stranded DNA binding pro-tein from Sulfolobus solfataricusrdquoNucleic Acids Research vol 29no 4 pp 914ndash920 2001

[80] I D Kerr R I M Wadsworth L Cubeddu W Blankenfeldt JHNaismith andM FWhite ldquoInsights into ssDNA recognitionby the OB fold from a structural and thermodynamic study ofSulfolobus SSB proteinrdquo The EMBO Journal vol 22 no 11 pp2561ndash2570 2003

[81] X Luo U Schwarz-Linek C H Botting R Hensel B Siebersand M F White ldquoCC1 a novel crenarchaeal DNA binding pro-teinrdquo Journal of Bacteriology vol 189 no 2 pp 403ndash409 2007

[82] T J Kelly P Simancek and G S Brush ldquoIdentification andcharacterization of a single-stranded DNA-binding proteinfrom the archaeonMethanococcus jannaschiirdquoProceedings of theNational Academy of Sciences of theUnited States of America vol95 no 25 pp 14634ndash14639 1998

[83] Z Kelman S Pietrokovski and J Hurwitz ldquoIsolation and cha-racterization of a split B-type DNA polymerase from the arch-aeonMethanobacterium thermoautotrophicumΔHrdquoTheJournalof Biological Chemistry vol 274 no 40 pp 28751ndash28761 1999

[84] K Komori and Y Ishino ldquoReplication protein A in Pyrococcusfuriosus is involved in homologous DNA recombinationrdquo TheJournal of Biological Chemistry vol 276 no 28 pp 25654ndash25660 2001

[85] J B Robbins M C Murphy B A White R I Mackie THa and I K O Cann ldquoFunctional analysis of multiple single-stranded DNA-binding proteins from Methanosarcina acetivo-rans and their effects on DNA synthesis by DNA polymeraseBIrdquoThe Journal of Biological Chemistry vol 279 no 8 pp 6315ndash6326 2004

[86] Y Lin L-J Lin P Sriratana et al ldquoEngineering of functionalreplication protein a homologs based on insights into the evolu-tion of oligonucleotideoligosaccharide-binding foldsrdquo Journalof Bacteriology vol 190 no 17 pp 5766ndash5780 2008

[87] D N Frick and C C Richardson ldquoDNA primasesrdquo AnnualReview of Biochemistry vol 70 pp 39ndash80 2001

[88] G Desogus S Onesti P Brick M Rossi and F M PisanildquoIdentification and characterization of a DNA primase fromthe hyperthermophilic archaeon Methanococcus jannaschiirdquoNucleic Acids Research vol 27 no 22 pp 4444ndash4450 1999

Archaea 13

[89] A A Bocquier L Liu I K O Cann K Komori D Kohda andY Ishino ldquoArchaeal primase bridging the gap between RNAand DNA polymerasesrdquo Current Biology vol 11 no 6 pp 452ndash456 2001

[90] L Liu K Komori S Ishino et al ldquoThe archaeal DNA primasebiochemical characterization of the p41-p46 complex fromPyrococcus furiosusrdquo The Journal of Biological Chemistry vol276 no 48 pp 45484ndash45490 2001

[91] E Matsui M Nishio H Yokoyama K Harata S Darnisand I Matsui ldquoDistinct domain functions regulating de novoDNA synthesis of thermostable DNA primase from hyperther-mophile Pyrococcus horikoshiirdquo Biochemistry vol 42 no 50 pp14968ndash14976 2003

[92] N Ito I Matsui and EMatsui ldquoMolecular basis for the subunitassembly of the primase from an archaeon Pyrococcus hori-koshiirdquoThe FEBS Journal vol 274 no 5 pp 1340ndash1351 2007

[93] M le Breton G Henneke C Norais et al ldquoThe heterodimericprimase from the euryarchaeon Pyrococcus abyssi a multifunc-tional enzyme for initiation and repairrdquo Journal of MolecularBiology vol 374 no 5 pp 1172ndash1185 2007

[94] S-H Lao-Sirieix and S D Bell ldquoThe heterodimeric primaseof the hyperthermophilic archaeon Sulfolobus solfataricus pos-sesses DNA and RNA primase polymerase and 31015840-terminalnucleotidyl transferase activitiesrdquo Journal of Molecular Biologyvol 344 no 5 pp 1251ndash1263 2004

[95] S-H Lao-Sirieix L Pellegrini and S D Bell ldquoThe promiscuousprimaserdquo Trends in Genetics vol 21 no 10 pp 568ndash572 2005

[96] J Hu L Guo K Wu B Liu S Lang and L Huang ldquoTemplate-dependent polymerization across discontinuous templatesby the heterodimeric primase from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquoNucleic Acids Research vol 40no 8 pp 3470ndash3483 2012

[97] E Evguenieva-Hackenberg P Walter E Hochleitner FLottspeich and G Klug ldquoAn exosome-like complex in Sulfolo-bus solfataricusrdquo EMBOReports vol 4 no 9 pp 889ndash893 2003

[98] P Walter F Klein E Lorentzen A Ilchmann G Klug andE Evguenieva-Hackenberg ldquoCharacterization of native andreconstituted exosome complexes from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Microbiology vol62 no 4 pp 1076ndash1089 2006

[99] Z Zuo C J Rodgers A L Mikheikin and M A Trak-selis ldquoCharacterization of a functional DnaG-type primase inarchaea implications for a dual-primase systemrdquo Journal ofMolecular Biology vol 397 no 3 pp 664ndash676 2010

[100] B R Berquist P DasSarma and S DasSarma ldquoEssential andnon-essential DNA replication genes in the model halophilicArchaeon Halobacterium sp NRC-1rdquo BMC Genetics vol 8article 31 2007

[101] D K Braithwaite and J Ito ldquoCompilation alignment andphylogenetic relationships of DNA polymerasesrdquo Nucleic AcidsResearch vol 21 no 4 pp 787ndash802 1993

[102] I K O Cann and Y Ishino ldquoArchaeal DNA replication iden-tifying the pieces to solve a puzzlerdquo Genetics vol 152 no 4 pp1249ndash1267 1999

[103] G Lipps S Rother C Hart and G Krauss ldquoA novel typeof replicative enzyme harbouring ATpase primase and DNApolymerase activityrdquo The EMBO Journal vol 22 no 10 pp2516ndash2525 2003

[104] J Yamtich and J B Sweasy ldquoDNA polymerase family X func-tion structure and cellular rolesrdquoBiochimica et BiophysicaActavol 1804 no 5 pp 1136ndash1150 2010

[105] H Ohmori E C Friedberg R P P Fuchs et al ldquoThe Y-familyof DNA polymerasesrdquoMolecular Cell vol 8 no 1 pp 7ndash8 2001

[106] N Y Yao R E Georgescu J Finkelstein and M E OrsquoDonnellldquoSingle-molecule analysis reveals that the lagging strandincreases replisome processivity but slows replication forkprogressionrdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 106 no 32 pp 13236ndash132412009

[107] U Hubscher G Maga and S Spadari ldquoEukaryotic DNA poly-merasesrdquo Annual Review of Biochemistry vol 71 pp 133ndash1632002

[108] F Boudsocq S Iwai F Hanaoka and R Woodgate ldquoSulfolobussolfataricus P2 DNA polymerase IV (Dp04) an archaeal DinB-like DNA polymerase with lesion-bypass properties akin toeukaryotic pol120578rdquo Nucleic Acids Research vol 29 no 22 pp4607ndash4616 2001

[109] L-J Lin A Yoshinaga Y Lin et al ldquoMolecular analyses ofan unusual translesion DNA polymerase fromMethanosarcinaacetivorans C2Ardquo Journal of Molecular Biology vol 397 no 1pp 13ndash30 2010

[110] I K O Cann S Ishino NNomura Y Sako andY Ishino ldquoTwofamily B DNA polymerases from Aeropyrum pernix an aerobichyperthermophilic crenarchaeoterdquo Journal of Bacteriology vol181 no 19 pp 5984ndash5992 1999

[111] T Uemori Y Ishino H Doi and I Kato ldquoThe hyperther-mophilic archaeon Pyrodictium occultum has two 120572-like DNApolymerasesrdquo Journal of Bacteriology vol 177 no 8 pp 2164ndash2177 1995

[112] T Uemori Y Ishino H Toh K Asada and I Kato ldquoOrgani-zation and nucleotide sequence of the DNA polymerase genefrom the archaeon Pyrococcus furiosusrdquo Nucleic Acids Researchvol 21 no 2 pp 259ndash265 1993

[113] B A Connolly ldquoRecognition of deaminated bases by archaealfamily-B DNA polymerasesrdquo Biochemical Society Transactionsvol 37 no 1 pp 65ndash68 2009

[114] B A Connolly M J Fogg G Shuttleworth and B T WilsonldquoUracil recognition by archaeal family B DNA polymerasesrdquoBiochemical Society Transactions vol 31 no 3 pp 699ndash7022003

[115] T T Richardson X Wu B J Keith P Heslop A C Jones andB A Connolly ldquoUnwinding of primer-templates by archaealfamily-B DNA polymerases in response to template-stranduracilrdquo Nucleic Acids Research vol 41 no 4 pp 2466ndash24782013

[116] T Lindahl ldquoInstability and decay of the primary structure ofDNArdquo Nature vol 362 no 6422 pp 709ndash715 1993

[117] I B Rogozin K S Makarova Y I Pavlov and E V Koonin ldquoAhighly conserved family of inactivated archaeal B family DNApolymerasesrdquo Biology Direct vol 3 article 32 2008

[118] M Imamura T Uemori I Kato and Y Ishino ldquoA non-120572-like DNA polymerase from the hyperthermophilic archaeonPyrococcus furiosusrdquoBiological andPharmaceutical Bulletin vol18 no 12 pp 1647ndash1652 1995

[119] I K O Cann K Komori H Toh S Kanai and Y IshinoldquoA heterodimeric DNA polymerase evidence that members ofEuryarchaeota possess a distinct DNA polymeraserdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 95 no 24 pp 14250ndash14255 1998

[120] L Aravind D D Leipe and E V Koonin ldquoToprimmdasha con-served catalytic domain in type IA and II topoisomerases

14 Archaea

DnaG-type primases OLD family nucleases and RecR pro-teinsrdquo Nucleic Acids Research vol 26 no 18 pp 4205ndash42131998

[121] M Jokela A Eskelinen H Pospiech J Rouvinen and J ESyvaoja ldquoCharacterization of the 31015840 exonuclease subunit DP1of Methanococcus jannaschii replicative DNA polymerase DrdquoNucleic Acids Research vol 32 no 8 pp 2430ndash2440 2004

[122] T Uemori Y Sato I Kato H Doi and Y Ishino ldquoA novel DNApolymerase in the hyperthermophilic archaeon Pyrococcus fur-iosus gene cloning expression and characterizationrdquo Genes toCells vol 2 no 8 pp 499ndash512 1997

[123] Y Shen K Musti M Hiramoto H Kikuchi Y Kawarabayashiand I Matsui ldquoInvariant Asp-1122 and Asp-1124 are essentialresidues for polymerization catalysis of family D DNA poly-merase from Pyrococcus horikoshiirdquo The Journal of BiologicalChemistry vol 276 no 29 pp 27376ndash27383 2001

[124] G Henneke D Flament U Hubscher J Querellou and J-P Raffin ldquoThe hyperthermophilic euryarchaeota Pyrococcusabyssi likely requires the two DNA polymerases D and B forDNA replicationrdquo Journal of Molecular Biology vol 350 no 1pp 53ndash64 2005

[125] L Cubonova T Richardson B W Burkhart et al ldquoArchaealDNA polymerase D but not DNA polymerase B is required forgenome replication in Thermococcus kodakarensisrdquo Journal ofBacteriology vol 195 no 10 pp 2322ndash2328 2013

[126] C Rouillon G Henneke D Flament J Querellou and J-PRaffin ldquoDNA polymerase switching on homotrimeric PCNA atthe replication fork of the euryarchaea Pyrococcus abyssirdquo Jour-nal of Molecular Biology vol 369 no 2 pp 343ndash355 2007

[127] G Henneke ldquoIn vitro reconstitution of RNA primer removal inArchaea reveals the existence of two pathwaysrdquoTheBiochemicalJournal vol 447 no 2 pp 271ndash280 2012

[128] G-LMoldovan B Pfander and S Jentsch ldquoPCNA themaestroof the replication forkrdquo Cell vol 129 no 4 pp 665ndash679 2007

[129] X-P Kong R Onrust M OrsquoDonnell and J Kuriyan ldquoThree-dimensional structure of the 120573 subunit of E coli DNA poly-merase III holoenzyme a sliding DNA clamprdquo Cell vol 69 no3 pp 425ndash437 1992

[130] K Daimon Y Kawarabayasi H Kikuchi Y Sako and Y IshinoldquoThree proliferating cell nuclear antigen-like proteins foundin the hyperthermophilic archaeon Aeropyrum pemix interac-tions with the two DNA polymerasesrdquo Journal of Bacteriologyvol 184 no 3 pp 687ndash694 2002

[131] I Dionne R K Nookala S P Jackson A J Doherty andS D Bell ldquoA heterotrimeric PCNA in the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Cell vol 11 no 1pp 275ndash282 2003

[132] E Warbrick ldquoPCNA binding through a conserved motifrdquoBioEssays vol 20 no 3 pp 195ndash199 1998

[133] H Nishida K Mayanagi S Kiyonari et al ldquoStructural deter-minant for switching between the polymerase and exonucleasemodes in the PCNA-replicative DNA polymerase complexrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 106 no 49 pp 20693ndash20698 2009

[134] K Mayanagi S Kiyonari H Nishida et al ldquoArchitecture of theDNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complexrdquo Proceedings of the National Academy ofSciences of the United States of America vol 108 no 5 pp 1845ndash1849 2011

[135] B Castrec C Rouillon G Henneke D Flament J Querellouand J-P Raffin ldquoBinding to PCNA in Euryarchaeal DNA

replication requires two PIP motifs for DNA polymerase D andone PIP motif for DNA polymerase Brdquo Journal of MolecularBiology vol 394 no 2 pp 209ndash218 2009

[136] P F Pluchon T Fouqueau C Creze et al ldquoAn extendednetworkof genomic maintenance in the archaeon Pyrococcus abyssihighlights unexpected associations between eucaryotic homo-logsrdquo PLoS One vol 8 no 11 Article ID e79707 2013

[137] J E Ladner M Pan J Hurwitz and Z Kelman ldquoCrystalstructures of two active proliferating cell nuclear antigens(PCNAs) encoded byThermococcus kodakaraensisrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2711ndash2716 2011

[138] Y Kuba S Ishino T Yamagami et al ldquoComparative analyses ofthe two proliferating cell nuclear antigens from the hyperther-mophilic archaeonThermococcus kodakarensisrdquo Genes to Cellsvol 17 no 11 pp 923ndash937 2012

[139] T Fukui H Atomi T Kanai R Matsumi S Fujiwara andT Imanaka ldquoComplete genome sequence of the hyperther-mophilic archaeon Thermococcus kodakaraensis KOD1 andcomparison with Pyrococcus genomesrdquo Genome Research vol15 no 3 pp 352ndash363 2005

[140] D Jeruzalmi O Yurieva Y Zhao et al ldquoMechanism of proces-sivity clamp opening by the delta subunit wrench of the clamploader complex of E coliDNApolymerase IIIrdquoCell vol 106 no4 pp 417ndash428 2001

[141] Y Shiomi J Usukura Y Masamura et al ldquoATP-dependentstructural change of the eukaryotic clamp-loader protein repli-cation factor Crdquo Proceedings of the National Academy of Sciencesof the United States of America vol 97 no 26 pp 14127ndash141322000

[142] T Miyata T Oyama K Mayanagi S Ishino Y Ishino and KMorikawa ldquoThe clamp-loading complex for processive DNAreplicationrdquoNature Structural andMolecular Biology vol 11 no7 pp 632ndash636 2004

[143] T Oyama Y Ishino I K O Cann S Ishino and K MorikawaldquoAtomic structure of the clamp loader small subunit fromPyrococcus furiosusrdquo Molecular Cell vol 8 no 2 pp 455ndash4632001

[144] A Seybert D J Scott S Scaife M R Singleton and DB Wigley ldquoBiochemical characterisation of the clampclamploader proteins from the euryarchaeon Archaeoglobus fulgidusrdquoNucleic Acids Research vol 30 no 20 pp 4329ndash4338 2002

[145] Y-H Chen Y Lin A Yoshinaga et al ldquoMolecular analyses of athree-subunit euryarchaeal clamp loader complex from Meth-anosarcina acetivoransrdquo Journal of Bacteriology vol 191 no 21pp 6539ndash6549 2009

[146] Y-H Chen S A Kocherginskaya Y Lin et al ldquoBiochemicaland mutational analyses of a unique clamp loader complex inthe archaeon Methanosarcina acetivoransrdquo The Journal of Bio-logical Chemistry vol 280 no 51 pp 41852ndash41863 2005

[147] F Matsunaga C Norais P Forterre and H Myllykallio ldquoIden-tification of short ldquoeukaryoticrdquo Okazaki fragments synthesizedfrom a prokaryotic replication originrdquo EMBO Reports vol 4no 2 pp 154ndash158 2003

[148] H Kochiwa M Tomita and A Kanai ldquoEvolution of ribonucle-ase H genes in prokaryotes to avoid inheritance of redundantgenesrdquo BMC Evolutionary Biology vol 7 article 128 2007

[149] N OhtaniMHarukiMMorikawa and S Kanaya ldquoMoleculardiversities of RNases Hrdquo Journal of Bioscience and Bioengineer-ing vol 88 no 1 pp 12ndash19 1999

Archaea 15

[150] N Ohtani M Haruki M Morikawa R J Crouch M Itayaand S Kanaya ldquoIdentification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII fromBacillus subtilis classification of RNases H into three familiesrdquoBiochemistry vol 38 no 2 pp 605ndash618 1999

[151] N Ohtani H Yanagawa M Tomita and M Itaya ldquoIdentifi-cation of the first archaeal type 1 RNase H gene from Halobac-terium sp NRC-1 archaeal RNase HI can cleave an RNA-DNAjunctionrdquoThe Biochemical Journal vol 381 no 3 pp 795ndash8022004

[152] N Ohtani H Yanagawa M Tomita and M Itaya ldquoCleavage ofdouble-stranded RNA by RNase HI from a thermoacidophilicarchaeon Sulfolobus tokodaii 7rdquo Nucleic Acids Research vol 32no 19 pp 5809ndash5819 2004

[153] M A Nowak M C Boerlijst J Cooke and J M SmithldquoEvolution of genetic redundancyrdquo Nature vol 388 no 6638pp 167ndash170 1997

[154] A E Tomkinson S Vijayakumar J M Pascal and T Ellen-berger ldquoDNA ligases structure reactionmechanism and func-tionrdquo Chemical Reviews vol 106 no 2 pp 687ndash699 2006

[155] M Nakatani S Ezaki H Atomi and T Imanaka ldquoA DNAligase from a hyperthermophilic archaeon with unique cofactorspecificityrdquo Journal of Bacteriology vol 182 no 22 pp 6424ndash6433 2000

[156] Y Sun M S Seo J H Kim et al ldquoNovel DNA ligase with broadnucleotide cofactor specificity from the hyperthermophilic cre-narchaeon Sulfophobococcus zilligii influence of ancestral DNAligase on cofactor utilizationrdquo Environmental Microbiology vol10 no 12 pp 3212ndash3224 2008

[157] T R Beattie and S D Bell ldquoCoordination of multiple enzymeactivities by a single PCNA in archaeal Okazaki fragmentmaturationrdquo The EMBO Journal vol 31 no 6 pp 1556ndash15672012

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Archaea 13

[89] A A Bocquier L Liu I K O Cann K Komori D Kohda andY Ishino ldquoArchaeal primase bridging the gap between RNAand DNA polymerasesrdquo Current Biology vol 11 no 6 pp 452ndash456 2001

[90] L Liu K Komori S Ishino et al ldquoThe archaeal DNA primasebiochemical characterization of the p41-p46 complex fromPyrococcus furiosusrdquo The Journal of Biological Chemistry vol276 no 48 pp 45484ndash45490 2001

[91] E Matsui M Nishio H Yokoyama K Harata S Darnisand I Matsui ldquoDistinct domain functions regulating de novoDNA synthesis of thermostable DNA primase from hyperther-mophile Pyrococcus horikoshiirdquo Biochemistry vol 42 no 50 pp14968ndash14976 2003

[92] N Ito I Matsui and EMatsui ldquoMolecular basis for the subunitassembly of the primase from an archaeon Pyrococcus hori-koshiirdquoThe FEBS Journal vol 274 no 5 pp 1340ndash1351 2007

[93] M le Breton G Henneke C Norais et al ldquoThe heterodimericprimase from the euryarchaeon Pyrococcus abyssi a multifunc-tional enzyme for initiation and repairrdquo Journal of MolecularBiology vol 374 no 5 pp 1172ndash1185 2007

[94] S-H Lao-Sirieix and S D Bell ldquoThe heterodimeric primaseof the hyperthermophilic archaeon Sulfolobus solfataricus pos-sesses DNA and RNA primase polymerase and 31015840-terminalnucleotidyl transferase activitiesrdquo Journal of Molecular Biologyvol 344 no 5 pp 1251ndash1263 2004

[95] S-H Lao-Sirieix L Pellegrini and S D Bell ldquoThe promiscuousprimaserdquo Trends in Genetics vol 21 no 10 pp 568ndash572 2005

[96] J Hu L Guo K Wu B Liu S Lang and L Huang ldquoTemplate-dependent polymerization across discontinuous templatesby the heterodimeric primase from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquoNucleic Acids Research vol 40no 8 pp 3470ndash3483 2012

[97] E Evguenieva-Hackenberg P Walter E Hochleitner FLottspeich and G Klug ldquoAn exosome-like complex in Sulfolo-bus solfataricusrdquo EMBOReports vol 4 no 9 pp 889ndash893 2003

[98] P Walter F Klein E Lorentzen A Ilchmann G Klug andE Evguenieva-Hackenberg ldquoCharacterization of native andreconstituted exosome complexes from the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Microbiology vol62 no 4 pp 1076ndash1089 2006

[99] Z Zuo C J Rodgers A L Mikheikin and M A Trak-selis ldquoCharacterization of a functional DnaG-type primase inarchaea implications for a dual-primase systemrdquo Journal ofMolecular Biology vol 397 no 3 pp 664ndash676 2010

[100] B R Berquist P DasSarma and S DasSarma ldquoEssential andnon-essential DNA replication genes in the model halophilicArchaeon Halobacterium sp NRC-1rdquo BMC Genetics vol 8article 31 2007

[101] D K Braithwaite and J Ito ldquoCompilation alignment andphylogenetic relationships of DNA polymerasesrdquo Nucleic AcidsResearch vol 21 no 4 pp 787ndash802 1993

[102] I K O Cann and Y Ishino ldquoArchaeal DNA replication iden-tifying the pieces to solve a puzzlerdquo Genetics vol 152 no 4 pp1249ndash1267 1999

[103] G Lipps S Rother C Hart and G Krauss ldquoA novel typeof replicative enzyme harbouring ATpase primase and DNApolymerase activityrdquo The EMBO Journal vol 22 no 10 pp2516ndash2525 2003

[104] J Yamtich and J B Sweasy ldquoDNA polymerase family X func-tion structure and cellular rolesrdquoBiochimica et BiophysicaActavol 1804 no 5 pp 1136ndash1150 2010

[105] H Ohmori E C Friedberg R P P Fuchs et al ldquoThe Y-familyof DNA polymerasesrdquoMolecular Cell vol 8 no 1 pp 7ndash8 2001

[106] N Y Yao R E Georgescu J Finkelstein and M E OrsquoDonnellldquoSingle-molecule analysis reveals that the lagging strandincreases replisome processivity but slows replication forkprogressionrdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 106 no 32 pp 13236ndash132412009

[107] U Hubscher G Maga and S Spadari ldquoEukaryotic DNA poly-merasesrdquo Annual Review of Biochemistry vol 71 pp 133ndash1632002

[108] F Boudsocq S Iwai F Hanaoka and R Woodgate ldquoSulfolobussolfataricus P2 DNA polymerase IV (Dp04) an archaeal DinB-like DNA polymerase with lesion-bypass properties akin toeukaryotic pol120578rdquo Nucleic Acids Research vol 29 no 22 pp4607ndash4616 2001

[109] L-J Lin A Yoshinaga Y Lin et al ldquoMolecular analyses ofan unusual translesion DNA polymerase fromMethanosarcinaacetivorans C2Ardquo Journal of Molecular Biology vol 397 no 1pp 13ndash30 2010

[110] I K O Cann S Ishino NNomura Y Sako andY Ishino ldquoTwofamily B DNA polymerases from Aeropyrum pernix an aerobichyperthermophilic crenarchaeoterdquo Journal of Bacteriology vol181 no 19 pp 5984ndash5992 1999

[111] T Uemori Y Ishino H Doi and I Kato ldquoThe hyperther-mophilic archaeon Pyrodictium occultum has two 120572-like DNApolymerasesrdquo Journal of Bacteriology vol 177 no 8 pp 2164ndash2177 1995

[112] T Uemori Y Ishino H Toh K Asada and I Kato ldquoOrgani-zation and nucleotide sequence of the DNA polymerase genefrom the archaeon Pyrococcus furiosusrdquo Nucleic Acids Researchvol 21 no 2 pp 259ndash265 1993

[113] B A Connolly ldquoRecognition of deaminated bases by archaealfamily-B DNA polymerasesrdquo Biochemical Society Transactionsvol 37 no 1 pp 65ndash68 2009

[114] B A Connolly M J Fogg G Shuttleworth and B T WilsonldquoUracil recognition by archaeal family B DNA polymerasesrdquoBiochemical Society Transactions vol 31 no 3 pp 699ndash7022003

[115] T T Richardson X Wu B J Keith P Heslop A C Jones andB A Connolly ldquoUnwinding of primer-templates by archaealfamily-B DNA polymerases in response to template-stranduracilrdquo Nucleic Acids Research vol 41 no 4 pp 2466ndash24782013

[116] T Lindahl ldquoInstability and decay of the primary structure ofDNArdquo Nature vol 362 no 6422 pp 709ndash715 1993

[117] I B Rogozin K S Makarova Y I Pavlov and E V Koonin ldquoAhighly conserved family of inactivated archaeal B family DNApolymerasesrdquo Biology Direct vol 3 article 32 2008

[118] M Imamura T Uemori I Kato and Y Ishino ldquoA non-120572-like DNA polymerase from the hyperthermophilic archaeonPyrococcus furiosusrdquoBiological andPharmaceutical Bulletin vol18 no 12 pp 1647ndash1652 1995

[119] I K O Cann K Komori H Toh S Kanai and Y IshinoldquoA heterodimeric DNA polymerase evidence that members ofEuryarchaeota possess a distinct DNA polymeraserdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 95 no 24 pp 14250ndash14255 1998

[120] L Aravind D D Leipe and E V Koonin ldquoToprimmdasha con-served catalytic domain in type IA and II topoisomerases

14 Archaea

DnaG-type primases OLD family nucleases and RecR pro-teinsrdquo Nucleic Acids Research vol 26 no 18 pp 4205ndash42131998

[121] M Jokela A Eskelinen H Pospiech J Rouvinen and J ESyvaoja ldquoCharacterization of the 31015840 exonuclease subunit DP1of Methanococcus jannaschii replicative DNA polymerase DrdquoNucleic Acids Research vol 32 no 8 pp 2430ndash2440 2004

[122] T Uemori Y Sato I Kato H Doi and Y Ishino ldquoA novel DNApolymerase in the hyperthermophilic archaeon Pyrococcus fur-iosus gene cloning expression and characterizationrdquo Genes toCells vol 2 no 8 pp 499ndash512 1997

[123] Y Shen K Musti M Hiramoto H Kikuchi Y Kawarabayashiand I Matsui ldquoInvariant Asp-1122 and Asp-1124 are essentialresidues for polymerization catalysis of family D DNA poly-merase from Pyrococcus horikoshiirdquo The Journal of BiologicalChemistry vol 276 no 29 pp 27376ndash27383 2001

[124] G Henneke D Flament U Hubscher J Querellou and J-P Raffin ldquoThe hyperthermophilic euryarchaeota Pyrococcusabyssi likely requires the two DNA polymerases D and B forDNA replicationrdquo Journal of Molecular Biology vol 350 no 1pp 53ndash64 2005

[125] L Cubonova T Richardson B W Burkhart et al ldquoArchaealDNA polymerase D but not DNA polymerase B is required forgenome replication in Thermococcus kodakarensisrdquo Journal ofBacteriology vol 195 no 10 pp 2322ndash2328 2013

[126] C Rouillon G Henneke D Flament J Querellou and J-PRaffin ldquoDNA polymerase switching on homotrimeric PCNA atthe replication fork of the euryarchaea Pyrococcus abyssirdquo Jour-nal of Molecular Biology vol 369 no 2 pp 343ndash355 2007

[127] G Henneke ldquoIn vitro reconstitution of RNA primer removal inArchaea reveals the existence of two pathwaysrdquoTheBiochemicalJournal vol 447 no 2 pp 271ndash280 2012

[128] G-LMoldovan B Pfander and S Jentsch ldquoPCNA themaestroof the replication forkrdquo Cell vol 129 no 4 pp 665ndash679 2007

[129] X-P Kong R Onrust M OrsquoDonnell and J Kuriyan ldquoThree-dimensional structure of the 120573 subunit of E coli DNA poly-merase III holoenzyme a sliding DNA clamprdquo Cell vol 69 no3 pp 425ndash437 1992

[130] K Daimon Y Kawarabayasi H Kikuchi Y Sako and Y IshinoldquoThree proliferating cell nuclear antigen-like proteins foundin the hyperthermophilic archaeon Aeropyrum pemix interac-tions with the two DNA polymerasesrdquo Journal of Bacteriologyvol 184 no 3 pp 687ndash694 2002

[131] I Dionne R K Nookala S P Jackson A J Doherty andS D Bell ldquoA heterotrimeric PCNA in the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Cell vol 11 no 1pp 275ndash282 2003

[132] E Warbrick ldquoPCNA binding through a conserved motifrdquoBioEssays vol 20 no 3 pp 195ndash199 1998

[133] H Nishida K Mayanagi S Kiyonari et al ldquoStructural deter-minant for switching between the polymerase and exonucleasemodes in the PCNA-replicative DNA polymerase complexrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 106 no 49 pp 20693ndash20698 2009

[134] K Mayanagi S Kiyonari H Nishida et al ldquoArchitecture of theDNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complexrdquo Proceedings of the National Academy ofSciences of the United States of America vol 108 no 5 pp 1845ndash1849 2011

[135] B Castrec C Rouillon G Henneke D Flament J Querellouand J-P Raffin ldquoBinding to PCNA in Euryarchaeal DNA

replication requires two PIP motifs for DNA polymerase D andone PIP motif for DNA polymerase Brdquo Journal of MolecularBiology vol 394 no 2 pp 209ndash218 2009

[136] P F Pluchon T Fouqueau C Creze et al ldquoAn extendednetworkof genomic maintenance in the archaeon Pyrococcus abyssihighlights unexpected associations between eucaryotic homo-logsrdquo PLoS One vol 8 no 11 Article ID e79707 2013

[137] J E Ladner M Pan J Hurwitz and Z Kelman ldquoCrystalstructures of two active proliferating cell nuclear antigens(PCNAs) encoded byThermococcus kodakaraensisrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2711ndash2716 2011

[138] Y Kuba S Ishino T Yamagami et al ldquoComparative analyses ofthe two proliferating cell nuclear antigens from the hyperther-mophilic archaeonThermococcus kodakarensisrdquo Genes to Cellsvol 17 no 11 pp 923ndash937 2012

[139] T Fukui H Atomi T Kanai R Matsumi S Fujiwara andT Imanaka ldquoComplete genome sequence of the hyperther-mophilic archaeon Thermococcus kodakaraensis KOD1 andcomparison with Pyrococcus genomesrdquo Genome Research vol15 no 3 pp 352ndash363 2005

[140] D Jeruzalmi O Yurieva Y Zhao et al ldquoMechanism of proces-sivity clamp opening by the delta subunit wrench of the clamploader complex of E coliDNApolymerase IIIrdquoCell vol 106 no4 pp 417ndash428 2001

[141] Y Shiomi J Usukura Y Masamura et al ldquoATP-dependentstructural change of the eukaryotic clamp-loader protein repli-cation factor Crdquo Proceedings of the National Academy of Sciencesof the United States of America vol 97 no 26 pp 14127ndash141322000

[142] T Miyata T Oyama K Mayanagi S Ishino Y Ishino and KMorikawa ldquoThe clamp-loading complex for processive DNAreplicationrdquoNature Structural andMolecular Biology vol 11 no7 pp 632ndash636 2004

[143] T Oyama Y Ishino I K O Cann S Ishino and K MorikawaldquoAtomic structure of the clamp loader small subunit fromPyrococcus furiosusrdquo Molecular Cell vol 8 no 2 pp 455ndash4632001

[144] A Seybert D J Scott S Scaife M R Singleton and DB Wigley ldquoBiochemical characterisation of the clampclamploader proteins from the euryarchaeon Archaeoglobus fulgidusrdquoNucleic Acids Research vol 30 no 20 pp 4329ndash4338 2002

[145] Y-H Chen Y Lin A Yoshinaga et al ldquoMolecular analyses of athree-subunit euryarchaeal clamp loader complex from Meth-anosarcina acetivoransrdquo Journal of Bacteriology vol 191 no 21pp 6539ndash6549 2009

[146] Y-H Chen S A Kocherginskaya Y Lin et al ldquoBiochemicaland mutational analyses of a unique clamp loader complex inthe archaeon Methanosarcina acetivoransrdquo The Journal of Bio-logical Chemistry vol 280 no 51 pp 41852ndash41863 2005

[147] F Matsunaga C Norais P Forterre and H Myllykallio ldquoIden-tification of short ldquoeukaryoticrdquo Okazaki fragments synthesizedfrom a prokaryotic replication originrdquo EMBO Reports vol 4no 2 pp 154ndash158 2003

[148] H Kochiwa M Tomita and A Kanai ldquoEvolution of ribonucle-ase H genes in prokaryotes to avoid inheritance of redundantgenesrdquo BMC Evolutionary Biology vol 7 article 128 2007

[149] N OhtaniMHarukiMMorikawa and S Kanaya ldquoMoleculardiversities of RNases Hrdquo Journal of Bioscience and Bioengineer-ing vol 88 no 1 pp 12ndash19 1999

Archaea 15

[150] N Ohtani M Haruki M Morikawa R J Crouch M Itayaand S Kanaya ldquoIdentification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII fromBacillus subtilis classification of RNases H into three familiesrdquoBiochemistry vol 38 no 2 pp 605ndash618 1999

[151] N Ohtani H Yanagawa M Tomita and M Itaya ldquoIdentifi-cation of the first archaeal type 1 RNase H gene from Halobac-terium sp NRC-1 archaeal RNase HI can cleave an RNA-DNAjunctionrdquoThe Biochemical Journal vol 381 no 3 pp 795ndash8022004

[152] N Ohtani H Yanagawa M Tomita and M Itaya ldquoCleavage ofdouble-stranded RNA by RNase HI from a thermoacidophilicarchaeon Sulfolobus tokodaii 7rdquo Nucleic Acids Research vol 32no 19 pp 5809ndash5819 2004

[153] M A Nowak M C Boerlijst J Cooke and J M SmithldquoEvolution of genetic redundancyrdquo Nature vol 388 no 6638pp 167ndash170 1997

[154] A E Tomkinson S Vijayakumar J M Pascal and T Ellen-berger ldquoDNA ligases structure reactionmechanism and func-tionrdquo Chemical Reviews vol 106 no 2 pp 687ndash699 2006

[155] M Nakatani S Ezaki H Atomi and T Imanaka ldquoA DNAligase from a hyperthermophilic archaeon with unique cofactorspecificityrdquo Journal of Bacteriology vol 182 no 22 pp 6424ndash6433 2000

[156] Y Sun M S Seo J H Kim et al ldquoNovel DNA ligase with broadnucleotide cofactor specificity from the hyperthermophilic cre-narchaeon Sulfophobococcus zilligii influence of ancestral DNAligase on cofactor utilizationrdquo Environmental Microbiology vol10 no 12 pp 3212ndash3224 2008

[157] T R Beattie and S D Bell ldquoCoordination of multiple enzymeactivities by a single PCNA in archaeal Okazaki fragmentmaturationrdquo The EMBO Journal vol 31 no 6 pp 1556ndash15672012

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

14 Archaea

DnaG-type primases OLD family nucleases and RecR pro-teinsrdquo Nucleic Acids Research vol 26 no 18 pp 4205ndash42131998

[121] M Jokela A Eskelinen H Pospiech J Rouvinen and J ESyvaoja ldquoCharacterization of the 31015840 exonuclease subunit DP1of Methanococcus jannaschii replicative DNA polymerase DrdquoNucleic Acids Research vol 32 no 8 pp 2430ndash2440 2004

[122] T Uemori Y Sato I Kato H Doi and Y Ishino ldquoA novel DNApolymerase in the hyperthermophilic archaeon Pyrococcus fur-iosus gene cloning expression and characterizationrdquo Genes toCells vol 2 no 8 pp 499ndash512 1997

[123] Y Shen K Musti M Hiramoto H Kikuchi Y Kawarabayashiand I Matsui ldquoInvariant Asp-1122 and Asp-1124 are essentialresidues for polymerization catalysis of family D DNA poly-merase from Pyrococcus horikoshiirdquo The Journal of BiologicalChemistry vol 276 no 29 pp 27376ndash27383 2001

[124] G Henneke D Flament U Hubscher J Querellou and J-P Raffin ldquoThe hyperthermophilic euryarchaeota Pyrococcusabyssi likely requires the two DNA polymerases D and B forDNA replicationrdquo Journal of Molecular Biology vol 350 no 1pp 53ndash64 2005

[125] L Cubonova T Richardson B W Burkhart et al ldquoArchaealDNA polymerase D but not DNA polymerase B is required forgenome replication in Thermococcus kodakarensisrdquo Journal ofBacteriology vol 195 no 10 pp 2322ndash2328 2013

[126] C Rouillon G Henneke D Flament J Querellou and J-PRaffin ldquoDNA polymerase switching on homotrimeric PCNA atthe replication fork of the euryarchaea Pyrococcus abyssirdquo Jour-nal of Molecular Biology vol 369 no 2 pp 343ndash355 2007

[127] G Henneke ldquoIn vitro reconstitution of RNA primer removal inArchaea reveals the existence of two pathwaysrdquoTheBiochemicalJournal vol 447 no 2 pp 271ndash280 2012

[128] G-LMoldovan B Pfander and S Jentsch ldquoPCNA themaestroof the replication forkrdquo Cell vol 129 no 4 pp 665ndash679 2007

[129] X-P Kong R Onrust M OrsquoDonnell and J Kuriyan ldquoThree-dimensional structure of the 120573 subunit of E coli DNA poly-merase III holoenzyme a sliding DNA clamprdquo Cell vol 69 no3 pp 425ndash437 1992

[130] K Daimon Y Kawarabayasi H Kikuchi Y Sako and Y IshinoldquoThree proliferating cell nuclear antigen-like proteins foundin the hyperthermophilic archaeon Aeropyrum pemix interac-tions with the two DNA polymerasesrdquo Journal of Bacteriologyvol 184 no 3 pp 687ndash694 2002

[131] I Dionne R K Nookala S P Jackson A J Doherty andS D Bell ldquoA heterotrimeric PCNA in the hyperthermophilicarchaeon Sulfolobus solfataricusrdquo Molecular Cell vol 11 no 1pp 275ndash282 2003

[132] E Warbrick ldquoPCNA binding through a conserved motifrdquoBioEssays vol 20 no 3 pp 195ndash199 1998

[133] H Nishida K Mayanagi S Kiyonari et al ldquoStructural deter-minant for switching between the polymerase and exonucleasemodes in the PCNA-replicative DNA polymerase complexrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 106 no 49 pp 20693ndash20698 2009

[134] K Mayanagi S Kiyonari H Nishida et al ldquoArchitecture of theDNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complexrdquo Proceedings of the National Academy ofSciences of the United States of America vol 108 no 5 pp 1845ndash1849 2011

[135] B Castrec C Rouillon G Henneke D Flament J Querellouand J-P Raffin ldquoBinding to PCNA in Euryarchaeal DNA

replication requires two PIP motifs for DNA polymerase D andone PIP motif for DNA polymerase Brdquo Journal of MolecularBiology vol 394 no 2 pp 209ndash218 2009

[136] P F Pluchon T Fouqueau C Creze et al ldquoAn extendednetworkof genomic maintenance in the archaeon Pyrococcus abyssihighlights unexpected associations between eucaryotic homo-logsrdquo PLoS One vol 8 no 11 Article ID e79707 2013

[137] J E Ladner M Pan J Hurwitz and Z Kelman ldquoCrystalstructures of two active proliferating cell nuclear antigens(PCNAs) encoded byThermococcus kodakaraensisrdquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2711ndash2716 2011

[138] Y Kuba S Ishino T Yamagami et al ldquoComparative analyses ofthe two proliferating cell nuclear antigens from the hyperther-mophilic archaeonThermococcus kodakarensisrdquo Genes to Cellsvol 17 no 11 pp 923ndash937 2012

[139] T Fukui H Atomi T Kanai R Matsumi S Fujiwara andT Imanaka ldquoComplete genome sequence of the hyperther-mophilic archaeon Thermococcus kodakaraensis KOD1 andcomparison with Pyrococcus genomesrdquo Genome Research vol15 no 3 pp 352ndash363 2005

[140] D Jeruzalmi O Yurieva Y Zhao et al ldquoMechanism of proces-sivity clamp opening by the delta subunit wrench of the clamploader complex of E coliDNApolymerase IIIrdquoCell vol 106 no4 pp 417ndash428 2001

[141] Y Shiomi J Usukura Y Masamura et al ldquoATP-dependentstructural change of the eukaryotic clamp-loader protein repli-cation factor Crdquo Proceedings of the National Academy of Sciencesof the United States of America vol 97 no 26 pp 14127ndash141322000

[142] T Miyata T Oyama K Mayanagi S Ishino Y Ishino and KMorikawa ldquoThe clamp-loading complex for processive DNAreplicationrdquoNature Structural andMolecular Biology vol 11 no7 pp 632ndash636 2004

[143] T Oyama Y Ishino I K O Cann S Ishino and K MorikawaldquoAtomic structure of the clamp loader small subunit fromPyrococcus furiosusrdquo Molecular Cell vol 8 no 2 pp 455ndash4632001

[144] A Seybert D J Scott S Scaife M R Singleton and DB Wigley ldquoBiochemical characterisation of the clampclamploader proteins from the euryarchaeon Archaeoglobus fulgidusrdquoNucleic Acids Research vol 30 no 20 pp 4329ndash4338 2002

[145] Y-H Chen Y Lin A Yoshinaga et al ldquoMolecular analyses of athree-subunit euryarchaeal clamp loader complex from Meth-anosarcina acetivoransrdquo Journal of Bacteriology vol 191 no 21pp 6539ndash6549 2009

[146] Y-H Chen S A Kocherginskaya Y Lin et al ldquoBiochemicaland mutational analyses of a unique clamp loader complex inthe archaeon Methanosarcina acetivoransrdquo The Journal of Bio-logical Chemistry vol 280 no 51 pp 41852ndash41863 2005

[147] F Matsunaga C Norais P Forterre and H Myllykallio ldquoIden-tification of short ldquoeukaryoticrdquo Okazaki fragments synthesizedfrom a prokaryotic replication originrdquo EMBO Reports vol 4no 2 pp 154ndash158 2003

[148] H Kochiwa M Tomita and A Kanai ldquoEvolution of ribonucle-ase H genes in prokaryotes to avoid inheritance of redundantgenesrdquo BMC Evolutionary Biology vol 7 article 128 2007

[149] N OhtaniMHarukiMMorikawa and S Kanaya ldquoMoleculardiversities of RNases Hrdquo Journal of Bioscience and Bioengineer-ing vol 88 no 1 pp 12ndash19 1999

Archaea 15

[150] N Ohtani M Haruki M Morikawa R J Crouch M Itayaand S Kanaya ldquoIdentification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII fromBacillus subtilis classification of RNases H into three familiesrdquoBiochemistry vol 38 no 2 pp 605ndash618 1999

[151] N Ohtani H Yanagawa M Tomita and M Itaya ldquoIdentifi-cation of the first archaeal type 1 RNase H gene from Halobac-terium sp NRC-1 archaeal RNase HI can cleave an RNA-DNAjunctionrdquoThe Biochemical Journal vol 381 no 3 pp 795ndash8022004

[152] N Ohtani H Yanagawa M Tomita and M Itaya ldquoCleavage ofdouble-stranded RNA by RNase HI from a thermoacidophilicarchaeon Sulfolobus tokodaii 7rdquo Nucleic Acids Research vol 32no 19 pp 5809ndash5819 2004

[153] M A Nowak M C Boerlijst J Cooke and J M SmithldquoEvolution of genetic redundancyrdquo Nature vol 388 no 6638pp 167ndash170 1997

[154] A E Tomkinson S Vijayakumar J M Pascal and T Ellen-berger ldquoDNA ligases structure reactionmechanism and func-tionrdquo Chemical Reviews vol 106 no 2 pp 687ndash699 2006

[155] M Nakatani S Ezaki H Atomi and T Imanaka ldquoA DNAligase from a hyperthermophilic archaeon with unique cofactorspecificityrdquo Journal of Bacteriology vol 182 no 22 pp 6424ndash6433 2000

[156] Y Sun M S Seo J H Kim et al ldquoNovel DNA ligase with broadnucleotide cofactor specificity from the hyperthermophilic cre-narchaeon Sulfophobococcus zilligii influence of ancestral DNAligase on cofactor utilizationrdquo Environmental Microbiology vol10 no 12 pp 3212ndash3224 2008

[157] T R Beattie and S D Bell ldquoCoordination of multiple enzymeactivities by a single PCNA in archaeal Okazaki fragmentmaturationrdquo The EMBO Journal vol 31 no 6 pp 1556ndash15672012

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Archaea 15

[150] N Ohtani M Haruki M Morikawa R J Crouch M Itayaand S Kanaya ldquoIdentification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII fromBacillus subtilis classification of RNases H into three familiesrdquoBiochemistry vol 38 no 2 pp 605ndash618 1999

[151] N Ohtani H Yanagawa M Tomita and M Itaya ldquoIdentifi-cation of the first archaeal type 1 RNase H gene from Halobac-terium sp NRC-1 archaeal RNase HI can cleave an RNA-DNAjunctionrdquoThe Biochemical Journal vol 381 no 3 pp 795ndash8022004

[152] N Ohtani H Yanagawa M Tomita and M Itaya ldquoCleavage ofdouble-stranded RNA by RNase HI from a thermoacidophilicarchaeon Sulfolobus tokodaii 7rdquo Nucleic Acids Research vol 32no 19 pp 5809ndash5819 2004

[153] M A Nowak M C Boerlijst J Cooke and J M SmithldquoEvolution of genetic redundancyrdquo Nature vol 388 no 6638pp 167ndash170 1997

[154] A E Tomkinson S Vijayakumar J M Pascal and T Ellen-berger ldquoDNA ligases structure reactionmechanism and func-tionrdquo Chemical Reviews vol 106 no 2 pp 687ndash699 2006

[155] M Nakatani S Ezaki H Atomi and T Imanaka ldquoA DNAligase from a hyperthermophilic archaeon with unique cofactorspecificityrdquo Journal of Bacteriology vol 182 no 22 pp 6424ndash6433 2000

[156] Y Sun M S Seo J H Kim et al ldquoNovel DNA ligase with broadnucleotide cofactor specificity from the hyperthermophilic cre-narchaeon Sulfophobococcus zilligii influence of ancestral DNAligase on cofactor utilizationrdquo Environmental Microbiology vol10 no 12 pp 3212ndash3224 2008

[157] T R Beattie and S D Bell ldquoCoordination of multiple enzymeactivities by a single PCNA in archaeal Okazaki fragmentmaturationrdquo The EMBO Journal vol 31 no 6 pp 1556ndash15672012

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology