Structure of the ParM filament at 8.5Å resolution

Gayathri, P.; Fujii, Takashi; Namba, Keiichi; Löwe, Jan

doi:10.1016/j.jsb.2013.02.010

Cited by 21 publications

(32 citation statements)

References 46 publications

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“…From the ΔCcMreBdh co-crystal structures with ADP and AMPPNP, it is clear that the active site could well accommodate a guanidine instead of an adenine as the major contacts are with the ribose and phosphate moieties of the nucleotide, a feature, again, shared with ParM (Gayathri et al, 2013). …”

Section: Discussionmentioning

confidence: 99%

Bacterial actin MreB forms antiparallel double filaments

Ent

Izoré

Bharat

et al. 2014

eLife

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156

304

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Filaments of all actin-like proteins known to date are assembled from pairs of protofilaments that are arranged in a parallel fashion, generating polarity. In this study, we show that the prokaryotic actin homologue MreB forms pairs of protofilaments that adopt an antiparallel arrangement in vitro and in vivo. We provide an atomic view of antiparallel protofilaments of Caulobacter MreB as apparent from crystal structures. We show that a protofilament doublet is essential for MreB's function in cell shape maintenance and demonstrate by in vivo site-specific cross-linking the antiparallel orientation of MreB protofilaments in E. coli. 3D cryo-EM shows that pairs of protofilaments of Caulobacter MreB tightly bind to membranes. Crystal structures of different nucleotide and polymerisation states of Caulobacter MreB reveal conserved conformational changes accompanying antiparallel filament formation. Finally, the antimicrobial agents A22/MP265 are shown to bind close to the bound nucleotide of MreB, presumably preventing nucleotide hydrolysis and destabilising double protofilaments.DOI: http://dx.doi.org/10.7554/eLife.02634.001

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Section: Discussionmentioning

confidence: 99%

Bacterial actin MreB forms antiparallel double filaments

Ent

Izoré

Bharat

et al. 2014

eLife

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156

304

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“…S3), which was surprising if it is assumed that they formed similar filaments. A paper reporting a reconstruction of a ParM filament (33) has suggested that there is a conservation of subunit-subunit contacts between ParM and actin, but this involves arguments such as that residues in a helix in ParM (Arg257 and Lys258) are equivalent to residues in a loop in actin (Glu270 and Gly268) that has the opposite polarity, raising questions about this equivalence. When ParM is aligned to actin and the longitudinal interfacial residues in both are mapped onto this alignment (Fig.…”

Section: Discussionmentioning

confidence: 99%

Archaeal actin from a hyperthermophile forms a single-stranded filament

Braun

Orlova

Valegård

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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The prokaryotic origins of the actin cytoskeleton have been firmly established, but it has become clear that the bacterial actins form a wide variety of different filaments, different both from each other and from eukaryotic F-actin. We have used electron cryomicroscopy (cryo-EM) to examine the filaments formed by the protein crenactin (a crenarchaeal actin) from Pyrobaculum calidifontis, an organism that grows optimally at 90°C. Although this protein only has ∼20% sequence identity with eukaryotic actin, phylogenetic analyses have placed it much closer to eukaryotic actin than any of the bacterial homologs. It has been assumed that the crenactin filament is double-stranded, like F-actin, in part because it would be hard to imagine how a single-stranded filament would be stable at such high temperatures. We show that not only is the crenactin filament single-stranded, but that it is remarkably similar to each of the two strands in F-actin. A large insertion in the crenactin sequence would prevent the formation of an F-actin-like double-stranded filament. Further, analysis of two existing crystal structures reveals six different subunit-subunit interfaces that are filament-like, but each is different from the others in terms of significant rotations. This variability in the subunit-subunit interface, seen at atomic resolution in crystals, can explain the large variability in the crenactin filaments observed by cryo-EM and helps to explain the variability in twist that has been observed for eukaryotic actin filaments.helical polymers | variable twist | cytoskeletal filaments | crenactin A ctin is one of the most highly conserved as well as abundant eukaryotic proteins. From chickens to humans, an evolutionary separation of ∼350 million years, there are no amino acid changes in the skeletal muscle isoform of actin (1). There are at least six different mammalian isoforms that are quite similar to each other, and all seem to have diverged from a common ancestral actin gene (2). In contrast, we now know that bacteria have actin-like proteins that share a common fold (3-5) but have vanishingly little sequence similarity both among themselves and to eukaryotic actin (6).Two recent crystal structures of a crenarchaeal actin, crenactin (7, 8), raise interesting questions about the structure of the crenactin filament and its evolutionary relationship to F-actin. In both crystals (with two different space groups) crenactin forms a single-stranded filament with eight subunits per ∼420-Å righthanded turn, with a rise and rotation per subunit, therefore, of ∼53 Å and 45°, respectively. In contrast, in F-actin there is a rise and rotation of ∼55 Å and ∼27°along each of the two long-pitch right-handed strands. It was stated (9) that outside of the crystal the crenactin filaments are double-stranded, based upon the suggestion (8) that a single-stranded filament would unlikely be stable and that power spectra from crenactin filaments showed a strong layer line at ∼1/(210 Å), half of the repeat in the crystals.We have been able to ...

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“…These highly divergent ParM amino acid sequences ( Fig. 1) have recently been shown to translate into equally divergent filament architectures (Gayathri et al, 2013;Popp et al, 2010a;Popp et al, 2012;Popp et al, 2010b), which adds some weight to the hypothesis that an element of positive selection to diverge might have existed between selected ParMs.…”

Section: Bacterial Actinsmentioning

confidence: 93%

“…For instance, the timing and location of assembly of the plasmid-segregation filament ParM will be different to those required for cell wall synthesis and cell division, and thus for MreB and FtsA. The divergence of the bacterial actins has ensured that they will form independent homopolymers, as protomer interfaces and helical parameters are variable among the classes of actin-like filaments (Gayathri et al, 2013;Popp and Robinson, 2011;Szwedziak et al, 2012;van den Ent et al, 2001). Thus accomplishment of a specific biological function has provided the context in which the host actins (MreB and FtsA) have diverged and have become optimized for their specialized function.…”

Section: Bacterial Actinsmentioning

confidence: 99%

The evolution of compositionally and functionally distinct actin filaments

Gunning

Ghoshdastider

Whitaker

et al. 2015

Journal of Cell Science

261

198

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The actin filament is astonishingly well conserved across a diverse set of eukaryotic species. It has essentially remained unchanged in the billion years that separate yeast, Arabidopsis and man. In contrast, bacterial actin-like proteins have diverged to the extreme, and many of them are not readily identified from sequence-based homology searches. Here, we present phylogenetic analyses that point to an evolutionary drive to diversify actin filament composition across kingdoms. Bacteria use a one-filament-one-function system to create distinct filament systems within a single cell. In contrast, eukaryotic actin is a universal force provider in a wide range of processes. In plants, there has been an expansion of the number of closely related actin genes, whereas in fungi and metazoa diversification in tropomyosins has increased the compositional variety in actin filament systems. Both mechanisms dictate the subset of actin-binding proteins that interact with each filament type, leading to specialization in function. In this Hypothesis, we thus propose that different mechanisms were selected in bacteria, plants and metazoa, which achieved actin filament compositional variation leading to the expansion of their functional diversity.

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Structure of the ParM filament at 8.5Å resolution

Cited by 21 publications

References 46 publications

Bacterial actin MreB forms antiparallel double filaments

Bacterial actin MreB forms antiparallel double filaments

Archaeal actin from a hyperthermophile forms a single-stranded filament

The evolution of compositionally and functionally distinct actin filaments

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