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Page 1: Gogarten issol2014 version4

Molecular evolution before the ancestors of the bacterial and archaeal domains and before the Last

Universal Common Ancestor

Funded through the NASA Exobiology and NSF Assembling the Tree of Life Programs Origins 2014, Nara, Japan, July 6-11, 2014

J. Peter Gogarten University of Connecticut

Dept. of Molecular and Cell Biol.

Collaborators: Dr. Greg Fournier (UConn/MIT) Dr. Cheryl Andam (UConn/Harvard)

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Outline:

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•  Gene  duplica,ons  and  deep  molecular  phylogenies  •  Proper,es  of  the  Last  Universal  Common  Ancestor(s)  •  The  history  of  the  transla,on  machinery  during  the  expansion  of  the  gene,c  code  

•  The  ribosomal  tree  of  life  and  inferred  op,mal  growth  temperature    •  Tree  shape,  the  ar,fact  of  apparent  “lonely  ancestors”    •  Indica,ons  for  early  ex,nc,on  events  due  to  increased  environmental  temperature  

•  Phylogene,c  evidence  for  LUCA’s  compatriots    

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Catalytic subunits Non catalytic subunits

speciation

gene duplication time

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ATPase  /  ATPsynthase      ATP  binding  Subunits  

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N C

V-proteolipid

N C N C

A-proteolipids

Halobacterium Methanococcus

β

α α β

c

A

B A

A B

B

c

N C

F-proteolipid

V-type ATPase A-type ATPase

F-type ATPase

α β

Methanopyrus

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?

mesophilicthermophilic

Archaea Eukarya Bacteria

endosymbionts

1

2

3

4

5

A

B

C

D E

12  proteolipid  Ds  /  6  cataly,c  SU  =                                  2  H+(Na+)  /  ATP  

12  proteolipid  Ds  /  3  cataly,c  SU  =                                4H+(Na+)  /  ATP  

6  proteolipid  Ds  /  3  cataly,c  SU  =                                2H+(Na+)  /  ATP  

12  proteolipid  Ds  /  3  cataly,c  SU  =                                4H+(Na+)  /  ATP  

12  proteolipid  Ds  /  3  cataly,c  SU  =                                4H+(Na+)  /  ATP  

Reversible  Enzyme     Reversible  Enzyme    Dedicated  Ion  Pump  

Dedicated  Ion  Pump  

Reversible  Enzyme    

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   C.  R.  Woese  and  G.  E.  Fox  (1977)  J.  Mol.  Evol.  10,  1-­‐6:    “Eucaryotes  did  arise  from  procaryotes,  but  only  in  the  sense  that  the  procaryo6c  is  an  organiza6onal,  not  a  phylogene6c  dis6nc6on.  In  analogous  fashion  procaryotes  arose  from  simpler  en66es.  The  la<er  are  properly  called  progenotes,  because  they  are  s6ll  in  the  process  of  evolving  the  rela6onship  between  genotype  and  phenotype.”    

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According  to  Woese  and  Fox   According  to  V/F/A-­‐ATPases  

From:  GOGARTEN  J.P.,  OLENDZENSKI  L.,  (1999)  The  Progenote,    Encyclopedia  of  Molecular  Biology,  Thomas  Creighton,  ed.,  John  Wiley  and  Sons,  NY  (submieed  version  at  gogarten.uconn.edu)      

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In  R.P.  Mortlock:  (ed),  The  Evolu,on  of  Metabolic  Func,on  ,  CRC  Press,1992    

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Organisms  represented  by  the  root  of  the  universal  evolu,onary  tree  were    most  likely  complex  cells  with  a  sophis,cated  protein  transla,on  system  and  a  DNA  genome  encoding  hundreds  of  genes.    

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Outline:

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•  Gene  duplica,ons  and  deep  molecular  phylogenies  •  Proper,es  of  the  Last  Universal  Common  Ancestor(s)  •  The  history  of  the  transla:on  machinery  during  the  expansion  of  the  gene:c  code  

•  The  ribosomal  tree  of  life  and  inferred  op,mal  growth  temperature    •  Tree  shape,  the  ar,fact  of  apparent  “lonely  ancestors”    •  Indica,ons  for  early  ex,nc,on  events  due  to  increased  environmental  temperature  

•  Phylogene,c  evidence  for  LUCA’s  compatriots    

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A Radical Proposal by Eugene Koonin : Anthropic Chemical Evolution (The Logic of Chance – FT Press 2012)

•  Modern cosmologies postulate parallel worlds, for example assuming an eternal inflation period, resulting in an infinite number of universes (Villinkin, 2007).

•  Given an infinite number of universes, even unlikely events are bound to happen in some universes (and because we are made from two biopolymers, we are in one of the universes where this rare event occurred).

•  Koonin suggests that the assembly of the translation machinery is a candidate for such an unlikely event.

•  Finding exceedingly rare events in evolution would argue for a Multi World Cosmology.

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These  hypotheses  can  be  tested  by  examining  the  composi,on  of  reconstructed  ancestor  sequences  

Do  synthetase  paralogs  retain  evidence  of  pre-­‐LUCA  evolu,onary  events?  

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Hypothesis Testing

1-2: neofunctionalization 3: subfunctionalization 4: takeover (parafunctionalization)

Probability density graph of all positions with X+Y plurality consensus in ancestral reconstruction of cognate paralog ancestor.

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Results

• Majority of high-probabilitiy positions are resolved for Ile or Val • Supports both amino acids are specifically encoded at the time of the paralog ancestor, Parafunctionalization •  Large number of nondiscriminating positions between Ile and Val would support subfunctionalization • However, these positions are all low-probability, and match with the control simulation, so probably artifact of poorly conserved positions.

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"RNA  –  world"  (single  biopolymer  world)  Replica,on  Machinery    

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"RNA  –  world"  (single  biopolymer  world)  Replica,on  Machinery    

Rise  of  protein  as  second  biopolymer  tRNAs,  "RNA"  Ribosome,    RNA  based  tRNA  charging  mechanisms  

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"RNA  –  world"  (single  biopolymer  world)  Replica,on  Machinery    

Rise  of  protein  as  second  biopolymer  tRNAs,  "RNA"  Ribosome,    RNA  based  tRNA  charging  mechanisms  

Expansion  of  the  gene,c  code  to  include  Isoleucine  and  Valine  

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"RNA  –  world"  (single  biopolymer  world)  Replica,on  Machinery    

Rise  of  protein  as  second  biopolymer  tRNAs,  "RNA"  Ribosome,    RNA  based  tRNA  charging  mechanisms  

Expansion  of  the  gene,c  code  to  include  Isoleucine  and  Valine  

Takeover  of  charging  mechanism  by  proteins  (inven,on  of    aminoacyl  tRNA  synthetases)  

1IVS.pdb  valRS  +  tRNAval    

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"RNA  –  world"  (single  biopolymer  world)  Replica,on  Machinery    

Rise  of  protein  as  second  biopolymer  tRNAs,  "RNA"  Ribosome,    RNA  based  tRNA  charging  mechanisms  

Expansion  of  the  gene,c  code  to  include  Isoleucine  and  Valine  

Takeover  of  charging  mechanism  by  proteins  (inven,on  of    aminoacyl  tRNA  synthetases)  

Expansion  of  the  gene,c  code  to  include  Tryptophan  

1IVS.pdb  valRS  +  tRNAval    

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Conclusions 1st part

•  Extrapolation of ATPsynthase structure suggests that LUCA was able to use transmembrane ion gradients to synthesize ATP.

•  LUCA was not a progenote •  The expansion of the genetic code did not parallel the

divergence of aaRSs; rather aaRS acquired specificity in cells that were already able to charge tRNAs with their cognate aa through other means (likely exception tryptophan).

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Outline:

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•  Gene  duplica,ons  and  deep  molecular  phylogenies  •  Proper,es  of  the  Last  Universal  Common  Ancestor(s)  •  The  history  of  the  transla,on  machinery  during  the  expansion  of  the  gene,c  code  

•  The  ribosomal  tree  of  life  and  inferred  op:mal  growth  temperature    •  Tree  shape,  the  ar,fact  of  apparent  “lonely  ancestors”    •  Indica,ons  for  early  ex,nc,on  events  due  to  increased  environmental  temperature  

•  Phylogene,c  evidence  for  LUCA’s  compatriots    

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Evolution of the Ribosome

•  “Core” of ribosome consists of RNA + subset of ribosomal proteins universally conserved in all life (~29 proteins) (Harris et al., 2003)

•  Likely coevolved with genetic code within an RNA world (Wolf & Koonin, 2007)

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Compositional Stratigraphy

“We perform a compositional analysis of ribosomal proteins and ATPase subunits in bacterial and archaeal lineages, using conserved positions that came and remained under purifying selection before and up to the most recent common ancestor. An observable shift in amino acid usage at these conserved positions likely provides an untapped window into the history of protein sequence space, allowing events of genetic code expansion to be identified.”

Fournier GP, Gogarten JP. 2007. Signature of a primitive genetic code in ancient protein lineages. J Mol Evol. 65(4):425-436

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Roo,ng  the  Ribosomal  Tree  of  Life  using  an  Echo  from  the  Early  Expansion  of  the  Gene,c  Code  (Fournier and Gogarten, MBE 2010)

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Fig.  3.  The  classical  SSUrRNA  distance  tree,  presented  as  rooted  in  the  bacterial  branch.  Bold  lines  indicate  extreme  hyperthermophiles.  From  Steeer  (1996).  

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LUCA (located on the “bacterial branch”) was less thermophilic than the ancestor of the bacterial and archaeal domains

•  Boussau, B, Blanquart, S, Necsulea, A, Lartillot, N and Gouy, M (2008). Parallel adaptations to high temperatures in the Archaean eon. Nature 456(7224): 942-945���Reconstruction of ancestral protein and rRNA sequences ���Based on IVYWREL and rRNA stem G+C content LUCA was less thermophilic than the domain ancestors.

•  Galtier, N, Tourasse, N and Gouy, M (1999). A nonhyperthermophilic common ancestor to extant life forms. Science 283(5399): 220-221.8

•  rRNA 60°C!80°C ���IVYWREL (corrected for GC content) 20°C!70°C

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Outline:

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•  Gene  duplica,ons  and  deep  molecular  phylogenies  •  Proper,es  of  the  Last  Universal  Common  Ancestor(s)  •  The  history  of  the  transla,on  machinery  during  the  expansion  of  the  gene,c  code  

•  The  ribosomal  tree  of  life  and  inferred  op,mal  growth  temperature    •  Tree  shape,  the  ar:fact  of  apparent  “lonely  ancestors”    •  Indica:ons  for  early  ex:nc:on  events  due  to  increased  environmental  temperature  

•  Phylogene,c  evidence  for  LUCA’s  compatriots    

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Tree, Web, or Coral of Life?

Charles Darwin painted by George Richmond in the late 1830 Page B26 from Charles Darwin’s (1809-1882)

notebook (1837/38)

“The tree of life should perhaps be called the coral of life, base of branches dead”

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The Coral of Life (Darwin) ZHA

XY

BAY

EVA and G

OG

AR

TEN

(2004): C

ladogenesis, Coalescence and the E

volution of the Three Dom

ains of Life. Trends in G

enetics 20 (4): 182- 187

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The Coral of Life (Darwin) ZHA

XY

BAY

EVA and G

OG

AR

TEN

(2004): C

ladogenesis, Coalescence and the E

volution of the Three Dom

ains of Life. Trends in G

enetics 20 (4): 182- 187

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Coalescence  –  the  process  of  tracing  lineages  backwards  in  ,me  to  their  common  ancestors.  Every  two  extant  lineages  coalesce  to  their  most  recent  common  ancestor.    Eventually,  all  lineages  coalesce  to  the  cenancestor.    

t/2  

(Kingman,    1982)  

Illustra,on  is  from  J.  Felsenstein,  “Inferring  Phylogenies”,  Sinauer,  2003  

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EXTA

NT  LINEA

GES  FO

R  TH

E  SIMULATIONS  OF  50  LINEA

GES  

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Bacterial  16SrRNA  based  phylogeny  (from  P.  D.  Schloss  and  J.  Handelsman,  Microbiology  and  Molecular  Biology  Reviews,  December  2004.)    

The  devia,on  from  the  “long  branches  at  the  base”  paeern  could  be  due  to    •   under  sampling  •   an  actual  radia,on    

•   due  to  an  inven,on  that  was  not  transferred  •   following  a  mass  ex,nc,on  

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Near  frustra,on  of  early  life  

From:  Gogarten-­‐Boekels  M,  Hilario  E,  Gogarten  JP.  Orig  Life  Evol  Biosph.  1995  Jun;25(1-­‐3):251-­‐64.  The  effects  of  heavy  meteorite  bombardment  on  the  early  evolu:on  —the  emergence  of  the  three  domains  of  life.  

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From:  he

p://www.origin-­‐life.gr.jp/3603/3603055/3603055.htm

l    

Alterna,ve:  tail  of  early  heavy  bombardment  –  Nicolle  Zellner’s  talk  on  Tuesday  See  Marchi  et  al.  Nature  2014  for  a  recent  update.        

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Outline:

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•  Gene  duplica,ons  and  deep  molecular  phylogenies  •  Proper,es  of  the  Last  Universal  Common  Ancestor(s)  •  The  history  of  the  transla,on  machinery  during  the  expansion  of  the  gene,c  code  

•  The  ribosomal  tree  of  life  and  inferred  op,mal  growth  temperature    •  Tree  shape,  the  ar,fact  of  apparent  “lonely  ancestors”    •  Indica,ons  for  early  ex,nc,on  events  due  to  increased  environmental  temperature  

•  Phylogene:c  evidence  for  LUCA’s  compatriots    

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Molecular  Phylogenies  "            Lonely  Ancestors    

           From:  hep://itol.embl.de/                  iTol  The  interac,ve  Tree  of  Life    Ciccarelli  et  al,  Science.  2006  311  :1283-­‐7  

•  Tree  topology  averaged  over  many  genes  (mainly  ribosomal  proteins).  

•  No  re,cula,ons.  •  Branches  do  not  

reflect  ,me.  •  Only  extant  organisms  

and  their  lucky  ancestors  are  includes  

Noteworthy:    

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The Coral of Life (Darwin) ZHA

XY

BAY

EVA and G

OG

AR

TEN

(2004): C

ladogenesis, Coalescence and the E

volution of the Three Dom

ains of Life. Trends in G

enetics 20 (4): 182- 187

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The Coral of Life (Darwin) ZHA

XY

BAY

EVA and G

OG

AR

TEN

(2004): C

ladogenesis, Coalescence and the E

volution of the Three Dom

ains of Life. Trends in G

enetics 20 (4): 182- 187

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Molecular  phylogenies  of  aaRSs    reveal  other  lineages  that  coexisted  with  LUCA  and/or  the  domain  ancestors  and  transferred  some  of  their  genes  into  extant  lineages.    

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Pyrrolysine (Pyl) #  22nd genetically encoded amino acid to be discovered

#  Uses dedicated aminoacyl-tRNA synthetase (PylS) and a UAG-recognizing tRNA.

#  Found only within Methanosarcinae, Desulfitobacterium hafniense and a single marine worm symbiont delta-proteobacteria.

#  Used exclusively at the catalytic site of three enzymes responsible for the initial step of methylotrophic methanogenesis from methylamines.

MtmB structure with Pyl residue in catalytic core (Hao et al., 2002)

Synthesized from Pro and Lys Contains a peptide bond in the side chain

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Class II aaRS Phylogeny

LUCA -nodes

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Horizontal Gene Transfer ●  Pyl evolved and had a pervasive biological role in an ancient sister group to the

MRCA.

●  Transfer of cassette encoding methyltransferases and pyrrolysine system, selected for by the transfer of the methyltransferase genes.

●  Subsequent extinction of the entire donor lineage

Genetic Life Raft

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Ancient  origin  of  the  divergent  form

s  of  leucyl-­‐tRNA  synthetases  

in  the  Halobacteriales  Cheryl  P  Andam

,  Timothy  J  

Harlow,  R  Thane  Papke  and    

J  Peter  Gogarten  BM

C  Evolu6onary  Biology  12:85  

leucyl-tRNA synthetase (class I) phylogeny

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Homeoalleles  

•  Variants that have the same general function, but can have distinct characteristics.

•  Gene pool contains different homeoalleles, but individual strains and species usually contain only one of the alleles.

•  Can be brought together temporarily in a lineage through HGT

Andam, Williams, Gogarten 2010 PNAS

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Andam  and  Gogarten  2011  

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Phylogeny of selected class II amino acyl tRNA synthetases

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Andam  and  Gogarten  2011  

Distribu:on  of  rare  SerRS  in  

Archaea  

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thrRS and serRS phylogeny Eukaryotes  

Euryachaeota  Crenarchaeota  

Bacteria  

Alignment  with  PRANK  and  SATé,  tree  with  phyml  (WAG,  gamma  +I)  

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Conclusion 2nd part

•  Tree shape and amino acid composition of ancestral sequences suggest a bottleneck due to increased environmental temperature at the base of the bacterial and archaeal domains.

•  Studies of horizontal gene transfers of aaRSs suggest that more than two lineages passed through this bottleneck.

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References    

•  Andam  CP,  Gogarten  JP.  2011.  Biased  gene  transfer  in  microbial  evolu,on.  Nat.  Rev.  Microbiol.  9:543–555.    

•  Andam  CP,  Harlow  TJ,  Papke  RT,  Gogarten  JP.  2012.  Ancient  origin  of  the  divergent  forms  of  leucyl-­‐tRNA  synthetases  in  the  Halobacteriales.  BMC  Evol.  Biol.  12:85.    

•  Andam  CP,  Williams  D,  Gogarten  JP.  2010.  Biased  gene  transfer  mimics  paeerns  created  through  shared  ancestry.  Proc.  Natl.  Acad.  Sci.  U.  S.  A.  107:10679–10684.    

•  Boussau  B,  Blanquart  S,  Necsulea  A,  Lar,llot  N,  Gouy  M.  2008.  Parallel  adapta,ons  to  high  temperatures  in  the  Archaean  eon.  Nature  456:942–945.    

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