Available online at www.sciencedirect.com
The bacterial cytoskeleton
Joe 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
Introduction
Bacterial cells have a complex subcellular organization that
is established and maintained by a diverse set of polymerizing proteins that make up the bacterial cytoskeleton. At
least three general classes of dynamic polymers have been
identified: proteins with homology to the eukaryotic polymers actin and tubulin, and members of the ParA/MinD
family. Among the bacterial actins, at least five different
families have been characterized and shown to participate 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 participate in plasmid DNA replication or segregation. The ParA/
MinD superfamily of ATPases form a large and diverse set
of proteins that rely upon their dynamic assembly properties
to mediate the localization of many types of protein complexes 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 tubulins
FtsZ
One of the first cytoskeletal proteins recognized in bacteria 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 eukaryotic tubulins, with only amino acids involved in GTP
binding and hydrolysis conserved between the two
families [5–8]. Despite this divergence the three-dimensional 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 essential 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 affecting 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 vivo
has 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 approximately 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 membrane.
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 polymers in vitro [28–30]. BtubA/BtubB were probably
acquired from a eukaryotic cell by horizontal gene transfer. The functions of the BtubA/BtubB polymers within
Prosthebacter are currently unknown [28–30].
Current Opinion in Cell Biology 2008, 20:19–27
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
Current Opinion in Cell Biology 2008, 20:19–27
tubulins identified thus far are encoded by large plasmids
in various species of Bacillus [27]. Recent work demonstrates that some of these proteins comprise a previously
unrecognized tubulin-based bacterial cytoskeleton. The
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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 polymers 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 in
vivo.
TubZ appears to play an important role in stably maintaining plasmid pBtoxis. A mutant TubZ protein
(TubZD269A) predicted to be defective in GTP hydrolysis 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 properties, 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 tubulin-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 introduced 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 diverwww.sciencedirect.com
gence of the archaeal proteins, they might have alternative functions, raising the possibility that divergent
tubulin homologs, like divergent bacterial actins, assemble a variety of different types of polymers that participate
in many different aspects of cellular physiology.
Bacterial actins
MreB
Bacteria contain many proteins distantly related to eukaryotic actins. FtsA, MreB, and ParM were long ago recognized to contain key amino acid motifs conserved within
the larger actin/hsp70/hexokinase superfamily [35]. Elucidation of the crystal structure of MreB and the discovery
that it assembles filaments in vitro and in vivo demonstrated 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 control 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 structure [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 segregation 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.
Current Opinion in Cell Biology 2008, 20:19–27
22 Cell structure and dynamics
ParM
ParM is a bacterial actin required for segregation of the E.
coli plasmid R1 [70–72]. MreB and ParM have threedimensional 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 centromere-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 continued 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 demonstrated 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 proposed to contribute to the degree of filament twist
observed in vitro [78]. The model generated suggests
that the subunit–subunit contacts within the ParM filaments 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 superfamily.
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 interact 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 letting go. An elegant feature of the ParR helix structure is
its complete symmetry, allowing ParM filaments to interact 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. subtilis
poses 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 DNAbinding 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
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 provide 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]. Surprisingly, 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 sitespecific contacts as the DNA wraps around. This helical
structure, which appears as a large donut when viewed on
Current Opinion in Cell Biology 2008, 20:19–27
Magnetotactic bacteria synthesize unique organelles
called magnetosomes that they use to align themselves
in a geomagnetic field. In Magnetospirillum species, magnetosome formation depends upon a cytoskeletal network
composed at least in part of MamJ and MamK
[81,82,83,84,85]. As visualized by electron cryotomography, 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 (magnetosomes). MamJ is thought to be required to attach
magnetosomes to the polymer [84]. MamJ and MamK
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The bacterial cytoskeleton Pogliano 23
directly interact and mutations in the genes encoding
either protein disrupt the linear arrangement of magnetosomes [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 members 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 to
the ParA/MinD superfamily
The 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 segregation 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 preventing 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], making it unclear whether dynamic polymerization is an
evolutionarily conserved feature of MinD function.
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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 member 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 segregation. MipZ localizes to both poles after oriC separation and establishes a protein gradient within the cell
that extends inward from each pole (Figure 1e), providing 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 bacteria [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 replication, daughter plasmids are separated slightly and generate 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 mechanisms are still unclear. Recent studies from several different 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 polymers 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 structure (or bundles of filaments) mediates plasmid separation [74–76,77].
Current Opinion in Cell Biology 2008, 20:19–27
24 Cell structure and dynamics
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 segregate 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 experiments, migrates in front of the moving origin of replication (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 chemotaxis 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.
Crescentin
Crescentin is an intermediate filament protein identified
in C. crescentus in a screen for cell shape mutants [119].
Crescentin assembles a slightly curved filamentous structure that contributes to Caulobacter’s characteristic comma
shape appearance. In the absence of crescentin, cells
become rod-shaped but are otherwise viable. The dispensability of intermediate filaments for Caulobacter
growth and their general absence from many bacteria
suggests that it serves a specialized role in these organisms, perhaps contributing to formation of a cell shape
that provides a selective advantage as Caulobacter propels
itself through aqueous environments.
Conclusions
The 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].
Current Opinion in Cell Biology 2008, 20:19–27
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 plasmid maintenance. Our knowledge of cytoskeletal proteins
will continue to expand with the development of more
powerful fluorescence and electron microscopy tools.
Acknowledgement
This work was supported by a grant from the NIH (R01GM073898).
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