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The bacterial cytoskeletonJoe Pogliano

Bacteria contain a complex cytoskeleton that is more diverse

than previously thought. Recent research provides insight into

how bacterial actins, tubulins, and ParA proteins participate in a

variety of cellular processes.

Addresses

Division of Biological Sciences, University of California San Diego, 9500

Gilman Drive, La Jolla, CA 92093-0377, United States

Corresponding author: Pogliano, Joe ([email protected])

Current Opinion in Cell Biology 2008, 20:19–27

This review comes from a themed issue on

Cell structure and dynamics

Edited by Yixian Zheng and Karen Oegema

0955-0674/$ – see front matter

Published by Elsevier Ltd.

DOI 10.1016/j.ceb.2007.12.006

IntroductionBacterial cells have a complex subcellular organization that

is established and maintained by a diverse set of polymer-

izing proteins that make up the bacterial cytoskeleton. At

least three general classes of dynamic polymers have been

identified: proteins with homology to the eukaryotic poly-

mers actin and tubulin, and members of the ParA/MinD

family. Among the bacterial actins, at least five different

familieshavebeencharacterizedandshowntoparticipate in

many processes, including cell division, maintaining cell

shape, positioning bacterial organelles, and catalyzing DNA

segregation. Most known bacterial tubulins are closely

related and are required for cell division, but recent work

has identified additional divergent members that partici-

pate in plasmid DNA replication or segregation. The ParA/

MinD superfamily of ATPases form a large and diverse set

ofproteins that relyupontheirdynamicassemblyproperties

to mediate the localization of many types of protein com-

plexes within the cell and for catalyzing the segregation of

both plasmid and chromosomal DNA. Several in-depth

reviews have recently focused on the bacterial cytoskeleton

[1–4]. This review highlights recent progress on these three

highly conserved classes of cytoskeletal proteins with an

emphasis on new insights into how they function and on the

identification of recently discovered family members.

Bacterial tubulinsFtsZ

One of the first cytoskeletal proteins recognized in bac-

teria was the tubulin homolog FtsZ. The sequences of

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FtsZ from bacteria and archaea form a family of highly

conserved proteins that are very divergent from eukar-

yotic tubulins, with only amino acids involved in GTP

binding and hydrolysis conserved between the two

families [5–8]. Despite this divergence the three-dimen-

sional structures of FtsZ and tubulin are very similar,

suggesting they evolved from a common ancestor [5–10].

Like tubulin, FtsZ polymerizes cooperatively and in a

GTP-dependent manner in vitro [7–12]. FtsZ is an essen-

tial component of the cell division apparatus, assembling

a cytokinetic ring at midcell required to recruit other

members of the cell division complex [5,8–10,13–16].

The FtsZ ring constricts with septum invagination and

reassembles at new division sites from spirals of FtsZ [17–

20]. In addition to recruiting septal biogenesis enzymes to

the cell midpoint, recent reports implicate FtsZ in affect-

ing peptidoglycan synthesis along the side wall as well

[21�,22�].

In vitro, purified FtsZ assembles protofilaments, tubes

and sheets under a variety of different polymerization

conditions, but how FtsZ polymers are arranged in vivohas been unclear. New techniques such as electron

cryotomography that allow high-resolution imaging of

cells in a near-native state [23,24,25�] promise to reveal

the in vivo structure of FtsZ and many other bacterial

cytoskeletal filaments. The first high-resolution glimpse

of the FtsZ ring of Caulobacter crescentus using electron

cryotomography was recently provided by Li et al.[26��]. FtsZ rings were observed to consist of multiple,

short (100 nm) overlapping protofilaments approxi-

mately 5-nm wide (Figure 1a). Surprisingly, these

filaments always occurred about 16 nm away from

the cell membrane, suggesting the existence of an

adaptor protein that links the filaments to the mem-

brane.

BtubA/BtubB

At least eight families of tubulin have been described in

eukaryotes, while in bacteria the only tubulin relative

recognized for many years was FtsZ. The availability of

genomic sequences recently led to the identification of

several additional families of tubulin-like proteins

encoded within bacterial and archaeal genomes

[8,27��,28–30]. A pair of tubulin homologs, BtubA and

BtubB, characterized from Prosthebacter dejoneii were

shown to be closely related to a and b tubulin and

assemble as a heterodimer into GTP-dependent poly-

mers in vitro [28–30]. BtubA/BtubB were probably

acquired from a eukaryotic cell by horizontal gene trans-

fer. The functions of the BtubA/BtubB polymers within

Prosthebacter are currently unknown [28–30].


mailto:[email protected]

http://dx.doi.org/10.1016/j.ceb.2007.12.006

20 Cell structure and dynamics

Figure 1

Progress in understanding the bacterial cytoskeleton is revealed in a collection of cell biology images from the last year. (a) A reconstruction of FtsZ

protofilaments (red) near the inner membrane (blue) based on electron cryotomography of C. crescentus. The outer membrane is shown in green. The panel

on the right shows the localization of FtsZ-GFP at the division site of C. crescentus. Reprinted from [26��] with permission from the publisher. (b) TubZ-GFP

assembles polymers required to stably maintain plasmid pBtoxis in Bacillus thuringiensis [27]. (c) Fluorescently labeled ParM (green) polymerizes between

two beads (yellow) coated with parC DNA bound with ParR, pushing the beads apart over time (s). The right two panels show electron microscopy images of

ParM filaments attached to the beads. Reprinted from [77��] with permission from the publisher. (d) A phylogenetic tree showing the relationship of several

of the known families of bacterial actins. The bottom panel shows that the B. subtilis plasmid segregation protein AlfA assembles polymers (green) extending

throughout the cell (red membranes). FRAP experiments (right two panels) show that AlfA-GFP filaments dynamically exchange subunits. Reprinted from

[80�] with permission from the publisher. (e) C. crescentus MipZ interacts with ParB at the cell poles and assembles a protein gradient (graph) that prevents

FtsZ from assembling near the poles, thereby favoring FtsZ assembly at midcell. Reprinted from [103��] with permission from the publisher. (f) V. cholerae

ParA1-GFP (red) migrates in front of the separating YFP-ParB-labeled origins (green), suggesting a mitotic mechanism in which ParA pulls the origins apart.

Panels I through VI show different cells at various stages of the cell cycle. Reprinted from [114] with permission from the publisher.

TubZ and RepX

Many bacteria and archaea encode relatives of tubulin

and FtsZ that are so vastly divergent that they do not fit

into either family [8,27��]. All of the divergent bacterial


tubulins identified thus far are encoded by large plasmids

in various species of Bacillus [27��]. Recent work demon-

strates that some of these proteins comprise a previously

unrecognized tubulin-based bacterial cytoskeleton. The


The bacterial cytoskeleton Pogliano 21

first member of this family shown to polymerize was

TubZ from Bacillus thuringiensis [27��]. TubZ is encoded

by pBtoxis, a virulence plasmid that carries several of the

insecticidal crystal toxins for which B. thuringiensis is well

known [31]. TubZ-GFP fusions assemble dynamic poly-

mers in B. thuringiensis that span the length of the cell

[27��] (Figure 1b). In time-lapse microscopy and FRAP

experiments, TubZ-GFP polymers are polarized with

plus and minus ends and translocate through the cell

by a treadmilling-type mechanism. TubZ can assemble

by itself in either B. thuringiensis or Escherichia coli, and

appears to have a critical concentration for assembly invivo.

TubZ appears to play an important role in stably main-

taining plasmid pBtoxis. A mutant TubZ protein

(TubZD269A) predicted to be defective in GTP hydroly-

sis assembles static rather than dynamic polymers. When

the mutant protein is expressed in trans from a compatible

plasmid, it coassembles with wild-type TubZ, trapping it

in a nonfunctional form, and this leads to loss of pBtoxis

from the cell [27��]. TubZ is encoded in an operon

together with TubR, a DNA-binding protein that

regulates TubZ expression. It therefore seems likely that

TubZ and TubR are essential components of a plasmid

maintenance machinery, but their precise roles are still

not understood. Given TubZ’s dynamic assembly proper-

ties, one possibility is that TubZ plays a role in plasmid

DNA segregation, potentially representing a very simple

and ancient tubulin-based mitotic apparatus. However, as

discussed below, these proteins might be also involved in

DNA replication.

How conserved are the polymerization properties of

TubZ? At least four other Bacillus plasmids encode tubu-

lin-like proteins, each very distantly related to the other

and to TubZ [27��]. One of these, RepX encoded by

plasmid pX01 of Bacillus anthracis, was identified as an

important component of plasmid replication [32��]. A

mini-replicon constructed from pX01 could only be intro-

duced into B. anthracis by electroporation if an intact copy

of RepX was present. A parallel finding was also made for

pBtoxis, where a mini-replicon containing TubZ and

TubR was constructed [33]. RepX was shown by electron

microscopy and dynamic light scattering to undergo

dynamic, GTP-dependent polymerization in vitro [34].

RepX has a GTPase activity that is required to establish

the plasmid in vivo during transformation experiments

[32��]. Taken together, it is now clear that these divergent

tubulins (TubZ and RepX) are important for plasmid

stability, functioning in replication, segregation, or

possibly both. It seems likely that these functions are

conserved among the TubZ-like proteins encoded by

plasmids in B. megaterium and B. cereus. A function in

DNA stability might also be conserved among the

archaeal TubZ-like proteins, many of which are also

plasmid-encoded. However, given the extreme diver-


gence of the archaeal proteins, they might have alterna-

tive functions, raising the possibility that divergent

tubulin homologs, like divergent bacterial actins, assem-

ble a variety of different types of polymers that participate

in many different aspects of cellular physiology.

Bacterial actinsMreB

Bacteria contain many proteins distantly related to eukar-

yotic actins. FtsA, MreB, and ParM were long ago recog-

nized to contain key amino acid motifs conserved within

the larger actin/hsp70/hexokinase superfamily [35]. Elu-

cidation of the crystal structure of MreB and the discovery

that it assembles filaments in vitro and in vivo demon-

strated that these divergent actins are part of an essential

bacterial cytoskeleton that probably arose billions of years

ago [9,36–39]. MreB and closely related proteins (such as

B. sutbilis Mbl and MreBH) assemble dynamic polymers

that move rapidly in a tight spiral pattern beneath the cell

membrane in many different organisms [37,38,40–44].

The mechanism of movement could be via treadmilling,

as reported for MreB-YFP in C. crescentus [45]. Purified

MreB from Thermotoga maritima assembles actin-like

polymers in the presence of either GTP or ATP

[36,39,46�].

Proteins of the MreB family have several important

functions, the most conserved being a direct role in

maintaining cell shape by influencing the position of

peptidoglycan synthesis [37,38,42,47–52]. Cell shape con-

trol requires the concerted actions of MreB with several

other proteins, including MreC, MreD, and Pbp2 [53–59].

Many bacteria contain only a single MreB protein, but in

B. subtilis, cell growth depends upon three closely related

proteins, MreB, MreBH, and Mbl, all of which colocalize

within the cell [37,48,60�]. MreBH interacts with a cell

wall hydrolyase (LytE) and directs its localization in a

helical pattern, providing a potential mechanism by

which MreBH can directly influence peptidoglycan struc-

ture [60�].

In addition to maintaining cell shape, MreB participates

in a number of other functions within the cell including

protein localization and chromosome segregation

(reviewed in [1,4]) [41,51,56,61–69]. The extent to which

MreB directly functions in chromosome segregation is

still being investigated in some organisms [66,68], but in

an elegant study of C. crescentus, a direct role for MreB in

chromosomal origin separation was established [67].

Using a small molecule inhibitor (A22) that allowed

the rapid inhibition of MreB function in synchronized

cell cultures [67], inactivation of MreB prevented segre-

gation of GFP-tagged chromosomal origins without

affecting DNA replication. Future studies using small

molecules to inhibit MreB and other cytoskeletal proteins

will probably be instrumental in deciphering the many

functions of these dynamic proteins.



ParM

ParM is a bacterial actin required for segregation of the E.coli plasmid R1 [70–72]. MreB and ParM have three-

dimensional structures similar to actin, though all three

share an incredibly low level of sequence similarity

(<12%) [36,73]. ParM assembles polymers that act

together with the ParR DNA-binding protein and its

cognate DNA recognition sites (clustered within a cen-

tromere-like region of DNA, parC) to segregate plasmid

DNA [74,75]. The polymerization dynamics of ParM are

very different from actin [76,77��]. Purified ParM displays

dynamic instability in vitro in which spontaneously

nucleated filaments extend bidirectionally at equal rates

and rapidly decay if not stabilized by interactions with

ParR/parC nucleoprotein complexes [76]. Remarkably,

this entire system was reconstituted in vitro with only

these three components [77��]. Fluorescently labeled

ParM assembled a radial array of dynamically unstable

polymers when added to beads coated with parC DNA

and ParR. When both ends of a dynamic polymer became

captured by parC/ParR complexes, polymerization con-

tinued by incorporation of new subunits adjacent to the

nucleoprotein complexes, driving the beads rapidly apart

[77��] (Figure 1c).

A refined model for ParM filaments recently demon-

strated that they have a left-handed twist rather than a

right-handed twist like actin [78��]. ParM, like other

actins, contains a central nucleotide-binding cleft formed

by two domains of the protein. The degree of opening

between the two domains of a single monomer is pro-

posed to contribute to the degree of filament twist

observed in vitro [78��]. The model generated suggests

that the subunit–subunit contacts within the ParM fila-

ments are different from that of F-actin. These new

results lead to the idea that divergent actin relatives

may assemble a variety of different structures. Given

the significant sequence divergence of many bacterial

actins, even within the MreB family, the implication is

that there may in fact be a large number of ways actin-like

proteins have evolved to assemble a polymer. Evidence

for this last point awaits the structural characterization of

additional divergent members of the bacterial actin super-

family.

How do ParM filaments attach to the plasmid DNA? An

elegant structure provided by Moller-Jensen [79��] now

provide a possible mechanism by which ParR may pro-

vide a link to the filament. The DNA binding N-terminus

of ParR forms a ribbon–helix–helix structure that binds

cooperatively to 10 sites within parC [75,79��]. Surpris-

ingly, ParR dimers assemble into a gently curved helix

with 12 dimers required to make one full turn. The DNA

recognition domains are positioned with a spacing of

3.5 nm on the outside of the ParR helix to make site-

specific contacts as the DNA wraps around. This helical

structure, which appears as a large donut when viewed on


end in the electron microscope, predicts that several

amino acids on the outer helix should be important for

DNA binding. Mutations in these amino acids eliminate

both DNA binding and segregation functions, providing

additional support for the model. Another surprising

aspect of the structure is the presence of a small

(�6 nm diameter) hole just large enough to accommodate

a ParM filament if amino acids of the flexible C-terminal

helix of ParR give way. These in vitro studies of ParM and

ParR suggest a detailed model for the architecture of the

plasmid partition complex in which ParM filaments inter-

act with the internal C-terminus of the ParR helix bound

to parC DNA. Two ends of spontaneously nucleated

ParM filaments become stabilized by ParR/parC, and as

ParM-ATP monomers add to both growing ends of a

filament, multiple sites of interaction with the ParR helix

increase processivity, driving plasmids apart without let-

ting go. An elegant feature of the ParR helix structure is

its complete symmetry, allowing ParM filaments to inter-

act with plasmids from either side.

AlfA

Another highly divergent actin relative, AlfA, was

recently shown to play a role in segregating plasmid

DNA during both vegetative growth and sporulation in

B. subtilis [80�]. The process of sporulation in B. subtilisposes a unique challenge for plasmid inheritance, because

plasmids must localize to one extreme end of the cell

before polar septation to be inherited by the spore [80�].Actin-like polymers that assemble between plasmids and

push them toward the cell pole would be ideally suited for

this function. AlfA assembles polymers that can extend

the entire length of the cell (Figure 1d). Fluorescence

recovery after photobleaching (FRAP) experiments

demonstrate that these polymers are highly dynamic,

rapidly exchanging subunits with a cytoplasmic pool.

Like many other plasmid segregation systems, a DNA-

binding protein, AlfB, is also required for segregation and

probably serves as an adaptor protein connecting the

filament to the DNA. Unlike ParM, dynamic instability

has yet to be observed for AlfA, raising the question of

how similar the mechanism of AlfA-mediated segregation

is to that described for ParM.

MamK

Magnetotactic bacteria synthesize unique organelles

called magnetosomes that they use to align themselves

in a geomagnetic field. In Magnetospirillum species, mag-

netosome formation depends upon a cytoskeletal network

composed at least in part of MamJ and MamK

[81��,82,83��,84��,85]. As visualized by electron cryoto-

mography, the actin homolog MamK assembles a series of

6-nm wide linear filaments that extend over much of the

length of the cell and provide a scaffold for the assembly

of membrane invaginations containing magnetite (mag-

netosomes). MamJ is thought to be required to attach

magnetosomes to the polymer [84��]. MamJ and MamK



directly interact and mutations in the genes encoding

either protein disrupt the linear arrangement of magneto-

somes [81��,83��,84��]. Purified MamK assembles into

bundles of filaments in vitro [85]. It will be interesting

to see a comparison of the biochemical and structural

properties of MamK with ParM, MreB, and AlfA.

FtsA

Sequence and structural data show that the cell division

protein FtsA forms a separate and divergent family of

bacterial actins [35,86]. FtsA localizes to the future site

of cell division by interacting with the C-terminus of

FtsZ and contributes to the recruitment of other mem-

bers of the cell division complex [10,13–15]. For many

other bacterial actins such as ParM, MreB, and AlfA, the

ability to assemble dynamic polymers is central to their

function, but for FtsA, the role of polymerization, if any,

is currently unclear. Recent studies have shown that S.pneumoniae FtsA assembles polymers in vitro [87],

suggesting that polymerization might also play an

important role in FtsA function, but this function

remains poorly defined.

Dynamic localization of proteins belonging tothe ParA/MinD superfamilyThe ParA/MinD family of P-loop ATPases [88] are highly

conserved in bacteria and are key components of the

bacterial cytoskeleton. Two different subfamilies, MinD

and ParA, play a multitude of roles in bacterial subcellular

organization. MinD and related proteins were recognized

long ago as spatial regulators of the site of cell division,

but only more recently were they found to assemble

polymers that oscillate rapidly within the cell. ParA

proteins form dynamic polymers that catalyze the segre-

gation of plasmid and chromosomal DNA, and more

recently have been shown to determine the position of

other protein complexes within the cell.

MinD

In E. coli, MinD works together with MinC and MinE

to determine the position of cell division by specifying

the assembly of FtsZ at the cell midpoint. MinD is a

polymerizing ATPase [89–91] that associates with the

membrane via its C-terminus [92–94] and also with

MinC to form a complex (MinC/MinD) that inhibits

FtsZ polymerization. MinC and MinD cycle from pole

to pole along the cell membrane, generating a temporal

protein gradient in which the highest time-averaged

concentration occurs near the cell pole thereby prevent-

ing polar FtsZ assembly [95–98]. Assembly of FtsZ over

the nucleoid is inhibited by SlmA in E. coli [99] and

Noc in B. subtilis [100]. Although MinC and MinD are

conserved in many bacteria, surprisingly, oscillation is

not. In B. subtilis, MinC and MinD localize statically to

the poles by interactions with DivIVA [101,102], mak-

ing it unclear whether dynamic polymerization is an

evolutionarily conserved feature of MinD function.


C. crescentus MipZ

An elegant strategy for determining the position of FtsZ

assembly independently of the Min system was recently

elucidated in C. crescentus, where the ParA family mem-

ber MipZ was shown to couple chromosome segregation

to cell division [103��]. At the beginning of the cell

cycle, MipZ localizes to the chromosomal origin of

replication (oriC) via the DNA-binding protein ParB.

After DNA replication, one of the daughter origins

migrates to the opposite cell pole simultaneously with

MipZ, which is also an inhibitor of FtsZ polymerization.

The arrival of MipZ and oriC at the opposite pole

stimulates the release of a pool of FtsZ from this

location, thereby coupling FtsZ assembly to DNA seg-

regation. MipZ localizes to both poles after oriC separ-

ation and establishes a protein gradient within the cell

that extends inward from each pole (Figure 1e), provid-

ing a mechanism for directing the assembly of FtsZ in

the center of the cell.

Plasmid DNA segregation by ParA

ParA ATPases are important for the efficient segregation

of both plasmid and chromosomal DNA in many bac-

teria [3,71]. ParA proteins usually occur in an operon

together with a DNA-binding protein, ParB, which

interacts with a set of specific DNA-binding sites that

form the equivalent of a simple centromere parC [3,71].

Plasmids with ParA partitioning systems such as F, P1,

and RK2, are positioned in the middle of the cell, where

they remain as the cell continues to grow. After replica-

tion, daughter plasmids are separated slightly and gen-

erate two distinct plasmid complexes that later rapidly

separate from each other at approximately 0.2 mm/min.

During the process of separation, daughter plasmids are

repositioned to the quarter-cell positions, that is, to what

will be the midcell positions of the future daughter

cells.

The ATPase activities of ParA proteins are presumed to

play a central role in targeting plasmids to midcell and in

driving plasmid separation, but the underlying mechan-

isms are still unclear. Recent studies from several differ-

ent systems show that plasmid ParA proteins assemble

polymers in vivo and in vitro [104,105,106��,107,108]. In

many instances, ParA-GFP fusions oscillate within the

cell and the cognate ParB/parC is required for this

dynamic localization [104,108–112]. These results have

led to a model in which ParA proteins assemble poly-

mers that cycle back and forth both between plasmids

and on either side of them, such that when the forces

generated by the polymers are balanced in all directions,

a single plasmid is held near the cell midpoint, while

two plasmids are held near the quarter cell positions

[107,108]. This model is strikingly different from the

ParM model, in which a single, linear filamentous struc-

ture (or bundles of filaments) mediates plasmid separ-

ation [74–76,77��].



Chromosome segregation by ParA proteins

A number of bacteria contain ParA proteins with a role in

chromosome segregation [113]. One recent example is

Vibrio cholerae, whose genome is divided into two

chromosomes (large and small) that replicate and segre-

gate separately from each other. Both chromosomes rely

upon proteins related to ParA for efficient segregation

[114��,115�,116]. ParA1 from V. cholerae mediates the

segregation of the origin of replication region of the large

chromosome from one cell pole to the other [114��]. Cells

depleted for ParA1 display chromosome I segregation

defects. ParA1-GFP assembles into a cytoplasmic haze

of fluorescence that, in time-lapse microscopy exper-

iments, migrates in front of the moving origin of replica-

tion (Figure 1f). These results suggest a model for

chromosome segregation in which ParA1 assembles a

mitotic machinery that pulls the daughter origins apart

[114��]. The smaller chromosome relies upon its own

ParA system (ParA2) to position the origin of replication

near the mid- and quarter cell positions [115�].

ParA and the localization of cytoplasmic protein

complexes

Members of the ParA family have probably evolved to

participate in localizing many different types of protein

complexes in bacteria [117,118��]. In R. sphaeroides, for

example, complexes of chemotaxis proteins localize to

the midcell and quarter cell positions [118��]. A ParA

homolog (PpfA) encoded within the chemotaxis operon

was found to be responsible for positioning these che-

motaxis complexes. In parA mutants, the complexes are

mislocalized and the cells are nonmotile, demonstrating

that positioning by PpfA is essential for their function.

The similarities between the localization behavior of

bacterial plasmids and the chemotaxis proteins suggest

a common positioning mechanism is at work.

CrescentinCrescentin is an intermediate filament protein identified

in C. crescentus in a screen for cell shape mutants [119].

Crescentin assembles a slightly curved filamentous struc-

ture that contributes to Caulobacter’s characteristic comma

shape appearance. In the absence of crescentin, cells

become rod-shaped but are otherwise viable. The dis-

pensability of intermediate filaments for Caulobactergrowth and their general absence from many bacteria

suggests that it serves a specialized role in these organ-

isms, perhaps contributing to formation of a cell shape

that provides a selective advantage as Caulobacter propels

itself through aqueous environments.

ConclusionsThe recent identification of many new families of bacterial

polymers (MreB, ParM, MamK, AlfA, TubZ, ParA, and

crescentin) suggests that the bacterial cytoskeleton is more

diverse and complex than previously thought. This point

was made beautifully most recently by Briegel et al. [25�].


Using electron cryotomography, they discovered at least

four distinct types of filaments within C. crescentus that

could be grouped based on their size and location within

the cell. Surprisingly, most of these filaments were still

present when known cytoskeletal proteins such as MreB

and crescentin were inactivated, indicating that many more

families of bacterial cytoskeletal proteins await discovery

[25�].

An emerging paradigm in bacterial cell biology is that

divergent actin relatives evolved in many different ways

to harness the mechanical properties of polymerization for

a variety of different processes, including cell division, cell

shape, and DNA segregation. This theme likely applies to

other families of dynamic polymers, including members of

the ParA/MinD family that use dynamic localization to

position protein and DNA molecules within the cell, and

possibly also applies to divergent bacterial tubulins, which

assemble dynamic cytoskeletal polymers required for plas-

mid maintenance. Our knowledge of cytoskeletal proteins

will continue to expand with the development of more

powerful fluorescence and electron microscopy tools.

AcknowledgementThis work was supported by a grant from the NIH (R01GM073898).

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17. Peters PC, Migocki MD, Thoni C, Harry EJ: A new assemblypathway for the cytokinetic Z ring from a dynamic helicalstructure in vegetatively growing cells of Bacillus subtilis.Mol Microbiol 2007, 64:487-499.

18. Thanedar S, Margolin W: FtsZ exhibits rapid movement andoscillation waves in helix-like patterns in Escherichia coli.Curr Biol 2004, 14:1167-1173.

19. Ben-Yehuda S, Losick R: Asymmetric cell division in B. subtilisinvolves a spiral-like intermediate of the cytokinetic proteinFtsZ. Cell 2002, 109:257-266.

20. Grantcharova N, Lustig U, Flardh K: Dynamics of FtsZ assemblyduring sporulation in Streptomyces coelicolor A3(2). J Bacteriol2005, 187:3227-3237.

21.�

Aaron M, Charbon G, Lam H, Schwarz H, Vollmer W, Jacobs-Wagner C: The tubulin homologue FtsZ contributes to cellelongation by guiding cell wall precursor synthesis inCaulobacter crescentus. Mol Microbiol 2007, 64:938-952.

This paper shows that C. crescentus FtsZ is required for medial localiza-tion of MurG, a cell wall precursor (lipid II) biosynthetic enzyme, andthereby contributes to controlling the spatial positioning of peptidoglycansynthesis during cell elongation.

22.�

Varma A, de Pedro MA, Young KD: FtsZ directs a second modeof peptidoglycan synthesis in Escherichia coli. J Bacteriol 2007,189:5692-5704.

This paper presents evidence for the intriguing idea that E. coli FtsZaffects side wall synthesis of peptidoglycan near the cell poles in certainmutants.

23. McIntosh JR: Electron microscopy of cells: a new beginning fora new century. J Cell Biol 2001, 153:F25-F32.

24. McIntosh R, Nicastro D, Mastronarde D: New views of cells in 3D:an introduction to electron tomography. Trends Cell Biol 2005,15:43-51.

25.�

Briegel A, Dias DP, Li Z, Jensen RB, Frangakis AS, Jensen GJ:Multiple large filament bundles observed in Caulobactercrescentus by electron cryotomography. Mol Microbiol 2006,62:5-14.

This paper presents the discovery of several types of cytoskeletal struc-tures in Caulobacter crescentus that do not correspond to known pro-teins, suggesting that additional classes of bacterial cytoskeletal proteinsawait discovery.

26.��

Li Z, Trimble MJ, Brun YV, Jensen GJ: The structure of FtsZfilaments in vivo suggests a force-generating role in celldivision. EMBO J 2007, 26:4694-4708.

The paper uses electron cryotomography to determine the arrangementof FtsZ protofilaments at the site of cell division.

27.��

Larsen RA, Cusumano C, Fujioka A, Lim-Fong G, Patterson P,Pogliano J: Treadmilling of a prokaryotic tubulin-like protein,TubZ, required for plasmid stability in Bacillus thuringiensis.Genes Dev 2007, 21:1340-1352.

This paper describes the identification of TubZ, a new type of tubulin-based cytoskeleton required for plasmid stability in Bacillus.

28. Jenkins C, Samudrala R, Anderson I, Hedlund BP, Petroni G,Michailova N, Pinel N, Overbeek R, Rosati G, Staley JT: Genes forthe cytoskeletal protein tubulin in the bacterial genusProsthecobacter. Proc Natl Acad Sci U S A 2002, 99:17049-17054.

29. Sontag CA, Staley JT, Erickson HP: In vitro assembly andGTPase hydrolysis by bacterial tubulins BtubA and BtubB.J Cell Biol 2005, 169:233-238.


30. Schlieper D, Oliva MA, Andreu JM, Lowe J: Structure of bacterialtubulin BtubA/B: evidence for horizontal gene transfer.Proc Natl Acad Sci U S A 2005, 102:9170-9175.

31. Berry C, O’Neil S, Ben-Dov E, Jones AF, Murphy L, Quail MA,Holden MT, Harris D, Zaritsky A, Parkhill J: Complete sequenceand organization of pBtoxis, the toxin-coding plasmid ofBacillus thuringiensis subsp. israelensis. Appl EnvironMicrobiol 2002, 68:5082-5095.

32.��

Tinsley E, Khan SA: A novel FtsZ-like protein is involved inreplication of the anthrax toxin-encoding pXO1 plasmid inBacillus anthracis. J Bacteriol 2006, 188:2829-2835.

This paper demonstrates that a distant tubulin relative, RepX, is requiredto construct a mini-pXO1 plasmid, suggesting that RepX is required forpX01 replication.

33. Tang M, Bideshi DK, Park HW, Federici BA: Minireplicon frompBtoxis of Bacillus thuringiensis subsp. israelensis.Appl Environ Microbiol 2006, 72:6948-6954.

34. Anand SP, Akhtar P, Tinsley E, Watkins SC, Khan SA: GTP-dependent polymerization of the tubulin-like RepX replicationprotein encoded by the pXO1 plasmid of Bacillus anthracis.Mol. Microbiol. 2008, 67:881-890.

35. Bork P, Sander C, Valencia A: An ATPase domain common toprokaryotic cell cycle proteins, sugar kinases, actin, andhsp70 heat shock proteins. Proc Natl Acad Sci U S A 1992,89:7290-7294.

36. van den Ent F, Amos L, Lowe J: Prokaryotic origin of the actincytoskeleton. Nature 2001, 413:39-44.

37. Jones L, Carballido-Lopez R, Errington J: Control of cell shape inbacteria: helical, actin-like filaments in Bacillus subtilis.Cell 2001, 104:913-922.

38. Carballido-Lopez R, Errington J: The bacterial cytoskeleton: invivo dynamics of the actin-like protein Mbl of Bacillus subtilis.Dev Cell 2003, 4:19-28.

39. Esue O, Cordero M, Wirtz D, Tseng Y: The assembly of MreB, aprokaryotic homolog of actin. J Biol Chem 2005, 280:2628-2635.

40. Defeu Soufo HJ, Graumann PL: Dynamic movement of actin-likeproteins within bacterial cells. EMBO Rep 2004, 5:789-794.

41. Gitai Z, Dye N, Shapiro L: An actin-like gene can determine cellpolarity in bacteria. Proc Natl Acad Sci U S A 2004, 101:8643-8648.

42. Figge RM, Divakaruni AV, Gober JW: MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wallmorphogenesis in Caulobacter crescentus. Mol Microbiol 2004,51:1321-1332.

43. Slovak PM, Wadhams GH, Armitage JP: Localization of MreB inRhodobacter sphaeroides under conditions causing changes incell shape and membrane structure. J Bacteriol 2005, 187:54-64.

44. Slovak PM, Porter SL, Armitage JP: Differential localization ofMre proteins with PBP2 in Rhodobacter sphaeroides.J Bacteriol 2006, 188:1691-1700.

45. Kim SY, Gitai Z, Kinkhabwala A, Shapiro L, Moerner WE:Single molecules of the bacterial actin MreB undergo directedtreadmilling motion in Caulobacter crescentus. Proc Natl AcadSci U S A 2006, 103:10929-10934.

46.�

Esue O, Wirtz D, Tseng Y: GTPase activity, structure, andmechanical properties of filaments assembled from bacterialcytoskeleton protein MreB. J Bacteriol 2006, 188:968-976.

This paper compares the biochemical properties of MreB filamentsassembled in the presence of various nucleotides and finds that bothGTP and ATP work equally well.

47. Doi M, Wachi M, Ishino F, Tomioka S, Ito M, Sakagami Y, Suzuki A,Matsuhashi M: Determinations of the DNA sequence of themreB gene and of the gene products of the mre region thatfunction in formation of the rod shape of Escherichia coli cells.J Bacteriol 1988, 170:4619-4624.

48. Daniel RA, Errington J: Control of cell morphogenesis inbacteria: two distinct ways to make a rod-shaped cell.Cell 2003, 113:767-776.



49. Hu B, Yang G, Zhao W, Zhang Y, Zhao J: MreB is important forcell shape but not for chromosome segregation of thefilamentous cyanobacterium Anabaena sp. PCC 7120.Mol Microbiol 2007, 63:1640-1652.

50. Scheffers DJ, Jones LJ, Errington J: Several distinct localizationpatterns for penicillin-binding proteins in Bacillus subtilis.Mol Microbiol 2004, 51:749-764.

51. Shih YL, Kawagishi I, Rothfield L: The MreB and Mincytoskeletal-like systems play independent roles inprokaryotic polar differentiation. Mol Microbiol 2005,58:917-928.

52. Mohammadi T, Karczmarek A, Crouvoisier M, Bouhss A,Mengin-Lecreulx D, den Blaauwen T: The essentialpeptidoglycan glycosyltransferase MurG forms a complexwith proteins involved in lateral envelope growth as well aswith proteins involved in cell division in Escherichia coli. MolMicrobiol 2007, 65:1106-1121.

53. Divakaruni AV, Loo RR, Xie Y, Loo JA, Gober JW: The cell-shapeprotein MreC interacts with extracytoplasmic proteinsincluding cell wall assembly complexes in Caulobactercrescentus. Proc Natl Acad Sci U S A 2005, 102:18602-18607.

54. Dye NA, Pincus Z, Theriot JA, Shapiro L, Gitai Z: Two independentspiral structures control cell shape in Caulobacter.Proc Natl Acad Sci U S A 2005, 102:18608-18613.

55. Leaver M, Errington J: Roles for MreC and MreD proteins inhelical growth of the cylindrical cell wall in Bacillus subtilis.Mol Microbiol 2005, 57:1196-1209.

56. Defeu Soufo HJ, Graumann PL: Bacillus subtilis actin-likeprotein MreB influences the positioning of the replicationmachinery and requires membrane proteins MreC/D and otheractin-like proteins for proper localization. BMC Cell Biol 2005,6:10.

57. Kruse T, Bork-Jensen J, Gerdes K: The morphogenetic MreBCDproteins of Escherichia coli form an essential membrane-bound complex. Mol Microbiol 2005, 55:78-89.

58. van den Ent F, Leaver M, Bendezu F, Errington J, de Boer P,Lowe J: Dimeric structure of the cell shape protein MreC andits functional implications. Mol Microbiol 2006, 62:1631-1642.

59. Divakaruni AV, Baida C, White CL, Gober JW: The cell shapeproteins MreB and MreC control cell morphogenesis bypositioning cell wall synthetic complexes. Mol Microbiol 2007,66:174-188.

60.�

Carballido-Lopez R, Formstone A, Li Y, Ehrlich SD, Noirot P,Errington J: Actin homolog MreBH governs cell morphogenesisby localization of the cell wall hydrolase LytE. Dev Cell 2006,11:399-409.

This paper shows that MreBH colocalizes with MreB and Mbl and that itinteracts with LytE, an extracellular endopeptidase. An intriguing model issuggested in which MreBH determines the helical localization pattern ofLytE by directing the location of its export to the periplasm.

61. Soufo HJ, Graumann PL: Actin-like proteins MreB and Mbl fromBacillus subtilis are required for bipolar positioning ofreplication origins. Curr Biol 2003, 13:1916-1920.

62. Kruse T, Moller-Jensen J, Lobner-Olesen A, Gerdes K:Dysfunctional MreB inhibits chromosome segregation inEscherichia coli. EMBO J 2003, 22:5283-5292.

63. Kruse T, Blagoev B, Lobner-Olesen A, Wachi M, Sasaki K, Iwai N,Mann M, Gerdes K: Actin homolog MreB and RNA polymeraseinteract and are both required for chromosome segregation inEscherichia coli. Genes Dev 2006, 20:113-124.

64. Kruse T, Gerdes K: Bacterial DNA segregation by the actin-likeMreB protein. Trends Cell Biol 2005, 15:343-345.

65. Srivastava P, Demarre G, Karpova TS, McNally J, Chattoraj DK:Changes in nucleoid morphology and origin localization uponinhibition or alteration of the actin homolog, MreB, of Vibriocholerae. J Bacteriol 2007, 189:7450-7463.

66. Karczmarek A, Martinez-Arteaga R, Alexeeva S, Hansen FG,Vicente M, Nanninga N, den Blaauwen T: DNA and origin regionsegregation are not affected by the transition from rod to


sphere after inhibition of Escherichia coli MreB by A22.Mol Microbiol 2007, 65:51-63.

67. Gitai Z, Dye NA, Reisenauer A, Wachi M, Shapiro L: MreB actin-mediated segregation of a specific region of a bacterialchromosome. Cell 2005, 120:329-341.

68. Formstone A, Errington J: A magnesium-dependent mreB nullmutant: implications for the role of mreB in Bacillus subtilis.Mol Microbiol 2005, 55:1646-1657.

69. Nilsen T, Yan AW, Gale G, Goldberg MB: Presence of multiplesites containing polar material in spherical Escherichia colicells that lack MreB. J Bacteriol 2005, 187:6187-6196.

70. Jensen RB, Gerdes K: Partitioning of plasmid R1. The ParMprotein exhibits ATPase activity and interacts with thecentromere-like ParR–parC complex. J Mol Biol 1997,269:505-513.

71. Jensen R, Lurz R, Gerdes K: Mechanism of DNA segregationin prokaryotes: replicon pairing by parC of plasmid R1.Proc Natl Acad Sci U S A 1998, 95:8550-8555.

72. Gerdes K, Moller-Jensen J, Ebersbach G, Kruse T, Nordstrom K:Bacterial mitotic machineries. Cell 2004, 116:359-366.

73. van den Ent F, Moller-Jensen J, Amos LA, Gerdes K, Lowe J:F-actin-like filaments formed by plasmid segregation proteinParM. EMBO J 2002, 21:6935-6943.

74. Moller-Jensen J, Jensen R, Lowe JKG: Prokaryotic DNAsegregation by an actin-like filament. EMBO J 2002,21:3119-3127.

75. Moller-Jensen J, Borch J, Dam M, Jensen RB, Roepstorff P,Gerdes K: Bacterial mitosis: ParM of plasmid R1 movesplasmid DNA by an actin-like insertional polymerizationmechanism. Mol Cell 2003, 12:1477-1487.

76. Garner EC, Campbell CS, Mullins RD: Dynamic instability in aDNA-segregating prokaryotic actin homolog. Science 2004,306:1021-1025.

77.��

Garner EC, Campbell CS, Weibel DB, Mullins RD: Reconstitutionof DNA segregation driven by assembly of a prokaryotic actinhomolog. Science 2007, 315:1270-1274.

This landmark paper describes the complete reconstitution of DNAsegregation from purified components and shows that ParM filamentscan push fluorescent beads apart.

78.��

Orlova A, Garner EC, Galkin VE, Heuser J, Mullins RD,Egelman EH: The structure of bacterial ParM filaments. NatStruct Mol Biol 2007, 14:921-926.

This paper provides a refined structure for ParM filaments and demon-strates that they are left-handed rather than right-handed like actin.

79.��

Moller-Jensen J, Ringgaard S, Mercogliano CP, Gerdes K, Lowe J:Structural analysis of the ParR/parC plasmid partitioncomplex. EMBO J 2007, 26:4413-4422.

The structure of the ParR/parC plasmid DNA complex provides insightinto the mechanism by which ParM filaments attach to the DNA.

80.�

Becker E, Herrera NC, Gunderson FQ, Derman AI, Dance AL,Sims J, Larsen RA, Pogliano J: DNA segregation by the bacterialactin AlfA during Bacillus subtilis growth and development.EMBO J 2006, 25:5919-5931.

This paper describes a new family of dynamic bacterial actins (AlfA)involved in plasmid segregation and demonstrates that Bacillus plasmidsenter the spore very early in the spore formation pathway.

81.��

Komeili A, Li Z, Newman DK, Jensen GJ: Magnetosomes are cellmembrane invaginations organized by the actin-like proteinMamK. Science 2006, 311:242-245.

This paper, along with 83, demonstrates that magnetosome organizationrelies upon an actin-like cytoskeletal protein.

82. Pradel N, Santini CL, Bernadac A, Fukumori Y, Wu LF: Biogenesisof actin-like bacterial cytoskeletal filaments destined forpositioning prokaryotic magnetic organelles. Proc Natl AcadSci U S A 2006, 103:17485-17489.

83.��

Scheffel A, Schuler D: The acidic repetitive domain of theMagnetospirillum gryphiswaldense MamJ protein displayshypervariability but is not required for magnetosome chainassembly. J Bacteriol 2007, 189:6437-6446.



This paper demonstrates that MamJ and MamK directly interact, provid-ing additional evidence for a model in which magnetosomes are anchoredto the MamK filament.

84.��

Scheffel A, Gruska M, Faivre D, Linaroudis A, Plitzko JM,Schuler D: An acidic protein aligns magnetosomes along afilamentous structure in magnetotactic bacteria. Nature 2006,440:110-114.

This paper, along with 80, demonstrates that magnetosomes require acytoskeleton for organization.

85. Taoka A, Asada R, Wu LF, Fukumori Y: The polymerization ofactin-like protein MamK associated with magnetosomes.J Bacteriol 2007, 189:8737-8740.

86. van den Ent F, Lowe J: Crystal structure of the cell divisionprotein FtsA from Thermotoga maritima. EMBO J 2000,19:5300-5307.

87. Lara B, Rico AI, Petruzzelli S, Santona A, Dumas J, Biton J,Vicente M, Mingorance J, Massidda O: Cell division in cocci:localization and properties of the Streptococcus pneumoniaeFtsA protein. Mol Microbiol 2005, 55:699-711.

88. Koonin EV: A superfamily of ATPases with diverse functionscontaining either classical or deviant ATP-binding motif.J Mol Biol 1993, 229:1165-1174.

89. de Boer PA, Crossley RE, Hand AR, Rothfield LI: The MinD proteinis a membrane ATPase required for the correct placement ofthe Escherichia coli division site. EMBO J 1991, 10:4371-4380.

90. Shih YL, Le T, Rothfield L: Division site selection in Escherichiacoli involves dynamic redistribution of Min proteins withincoiled structures that extend between the two cell poles.Proc Natl Acad Sci U S A 2003, 100:7865-7870.

91. Suefuji K, Valluzzi R, RayChaudhuri D: Dynamic assembly ofMinD into filament bundles modulated by ATP, phospholipids,and MinE. Proc Natl Acad Sci U S A 2002, 99:16776-16781.

92. Szeto TH, Rowland SL, Rothfield LI, King GF: Membranelocalization of MinD is mediated by a C-terminal motif that isconserved across eubacteria, archaea, and chloroplasts.Proc Natl Acad Sci U S A 2002, 99:15693-15698.

93. Hu Z, Lutkenhaus J: A conserved sequence at the C-terminus ofMinD is required for binding to the membrane and targetingMinC to the septum. Mol Microbiol 2003, 47:345-355.

94. Lackner LL, Raskin DM, de Boer PA: ATP-dependentinteractions between Escherichia coli Min proteins and thephospholipid membrane in vitro. J Bacteriol 2003, 185:735-749.

95. Hu Z, Lutkenhaus J: Topological regulation of cell division inEscherichia coli involves rapid pole to pole oscillation of thedivision inhibitor MinC under the control of MinD and MinE.Mol Microbiol 1999, 34:82-90.

96. Raskin DM, de Boer PA: MinDE-dependent pole-to-poleoscillation of division inhibitor MinC in Escherichia coli.J Bacteriol 1999, 181:6419-6424.

97. Raskin DM, de Boer PA: Rapid pole-to-pole oscillation of aprotein required for directing division to the middle ofEscherichia coli. Proc Natl Acad Sci U S A 1999, 96:4971-4976.

98. Hu Z, Lutkenhaus J: Topological regulation of cell division inE. coli spatiotemporal oscillation of MinD requires stimulationof its ATPase by MinE and phospholipid. Mol Cell 2001,7:1337-1343.

99. Bernhardt TG, de Boer PA: SlmA, a nucleoid-associated, FtsZbinding protein required for blocking septal ring assemblyover chromosomes in E. coli. Mol Cell 2005, 18:555-564.

100. Wu LJ, Errington J: Coordination of cell division andchromosome segregation by a nucleoid occlusion protein inBacillus subtilis. Cell 2004, 117:915-925.

101. Marston AL, Thomaides HB, Edwards DH, Sharpe ME, Errington J:Polar localization of the MinD protein of Bacillus subtilis andits role in selection of the mid-cell division site. Genes Dev1998, 12:3419-3430.

102. Marston AL, Errington J: Selection of the midcell division site inBacillus subtilis through MinD-dependent polar localizationand activation of MinC. Mol Microbiol 1999, 33:84-96.


103��

. Thanbichler M, Shapiro L: MipZ, a spatial regulator coordinatingchromosome segregation with cell division in Caulobacter.Cell 2006, 126:147-162.

This landmark paper describes how Caulobacter cells coordinate theassembly of FtsZ at midcell with chromosome segregation.

104. Hatano T, Yamaichi Y, Niki H: Oscillating focus of SopAassociated with filamentous structure guides partitioning of Fplasmid. Mol Microbiol 2007, 64:1198-1213.

105. Barilla D, Rosenberg MF, Nobbmann U, Hayes F: Bacterial DNAsegregation dynamics mediated by the polymerizing proteinParF. EMBO J 2005, 24:1453-1464.

106��

. Bouet JY, Ah-Seng Y, Benmeradi N, Lane D: Polymerization ofSopA partition ATPase: regulation by DNA binding and SopB.Mol Microbiol 2007, 63:468-481.

This paper demonstrates that SopA polymerization is regulated by DNAand the SopB DNA-binding protein, providing mechanistic insight intohow these polymers may be regulated within the cell.

107. Ebersbach G, Ringgaard S, Moller-Jensen J, Wang Q, Sherratt DJ,Gerdes K: Regular cellular distribution of plasmids byoscillating and filament-forming ParA ATPase of plasmidpB171. Mol Microbiol 2006, 61:1428-1442.

108. Lim GE, Derman AI, Pogliano J: Bacterial DNA segregation bydynamic SopA polymers. Proc Natl Acad Sci U S A 2005,102:17658-17663.

109. Marston AL, Errington J: Dynamic movement of the ParA-likeSoj protein of B. subtilis and its dual role in nucleoidorganization and developmental regulation. Mol Cell 1999,4:673-683.

110. Quisel JD, Lin DC, Grossman AD: Control of development byaltered localization of a transcription factor in B. subtilis.Mol Cell 1999, 4:665-672.

111. Ebersbach G, Gerdes K: The double par locus of virulencefactor pB171: DNA segregation is correlated with oscillation ofParA. Proc Natl Acad Sci U S A 2001, 98:15078-15083.

112. Ebersbach G, Gerdes K: Bacterial mitosis: partitioningprotein ParA oscillates in spiral-shaped structures andpositions plasmids at mid-cell. Mol Microbiol 2004, 52:385-398.

113. Draper GC, Gober JW: Bacterial chromosome segregation.Annu Rev Microbiol 2002, 56:567-597.

114��

. Fogel MA, Waldor MK: A dynamic, mitotic-like mechanism forbacterial chromosome segregation. Genes Dev 2006,20:3269-3282.

This paper describes a model for segregation of the V. cholerae largechromosome in which ParA1 assembles a mitotic apparatus that pulls thedaughter origins apart.

115�

. Yamaichi Y, Fogel MA, Waldor MK: par genes and the pathologyof chromosome loss in Vibrio cholerae. Proc Natl Acad Sci U S A2007, 104:630-635.

This paper demonstrates that ParA2, a homolog of plasmid partitioninggenes, is essential for segregation of chromosome II in V. cholerae.

116. Saint-Dic D, Frushour BP, Kehrl JH, Kahng LS: A parA homologselectively influences positioning of the large chromosomeorigin in Vibrio cholerae. J Bacteriol 2006, 188:5626-5631.

117. Atmakuri K, Cascales E, Burton OT, Banta LM, Christie PJ:Agrobacterium ParA/MinD-like VirC1 spatially coordinatesearly conjugative DNA transfer reactions. EMBO J 2007,26:2540-2551.

118��

. Thompson SR, Wadhams GH, Armitage JP: The positioning ofcytoplasmic protein clusters in bacteria. Proc Natl Acad Sci U SA 2006, 103:8209-8214.

A chromosomally encoded ParA protein is shown to position chemotaxisprotein complexes, demonstrating the generally important role of theseproteins in establishing and maintaining bacterial subcellular organiza-tion.

119. Ausmees N, Kuhn JR, Jacobs-Wagner C: The bacterialcytoskeleton: an intermediate filament-like function in cellshape. Cell 2003, 115:705-713.


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