Polymeric Structures and Dynamic Properties of the Bacterial Actin AlfA

Popp, David; Narita, Akihiro; Ghoshdastider, Umesh; Maéda, Kayo; Maéda, Yuichiro; Oda, Tatsuya; Fujisawa, Tetsuro; Onishi, Hirufumi; Ito, Kazuki; Robinson, Robert

doi:10.1016/j.jmb.2010.02.010

Cited by 36 publications

(44 citation statements)

References 29 publications

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“…Surprisingly, these filaments contain only a single strand, as opposed to the two strands present in F-actin and in the filaments formed by a number of bacterial actin-like proteins (9)(10)(11)(12)(13). We show that the crenactin filament is consistent with the single strand seen in crystals (7,8), and that this strand is quite similar to each of the two strands within F-actin.…”

mentioning

confidence: 65%

“…The remarkable diversity of filaments formed by bacterial actinlike proteins (such as the bacterial cell-shape-determining protein MreB, plasmid partitioning protein ParM, actin-like segregation protein AlfA, and magnetosome cytoskeleton protein MamK) has become clear (9)(10)(11)(12)(13)(27)(28)(29)(30)(31). This seems to reflect the large sequence divergence of the bacterial actin-like proteins (32), in striking contrast to the anomalous sequence conservation of eukaryotic actins.…”

Section: Discussionmentioning

confidence: 99%

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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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mentioning

confidence: 65%

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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“…In contrast, all force-generating motors known to be involved in segregating plasmids (ParM-R1, pSK41-ParM, and AlfA) were found to be helical polymers composed of two protofilaments gently winding around each other (2,(7)(8)(9)36). A double helical design has one major disadvantage, namely in its polar design, which can bind a plasmid only at one end.…”

Section: Discussionmentioning

confidence: 96%

“…In vivo, these components can form a linear assembly of multiple filaments (6), which positions pairs of plasmids at opposite ends of the rod-shaped bacteria by a polymerization mechanism, ensuring equal distribution of the plasmids between daughter cells (5). Other plasmid segregation motor systems that have been structurally characterized are pSK41-ParM (7) and AlfA (8,9). The currently known crystal structures of diverse Alp monomers are similar despite low sequence homology (ϳ20%) (7,10).…”

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confidence: 99%

Novel Actin-like Filament Structure from Clostridium tetani

Popp

Narita

Lee

et al. 2012

Journal of Biological Chemistry

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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: 94%

The evolution of compositionally and functionally distinct actin filaments

Gunning

Ghoshdastider

Whitaker

et al. 2015

Journal of Cell Science

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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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Polymeric Structures and Dynamic Properties of the Bacterial Actin AlfA

Cited by 36 publications

References 29 publications

Archaeal actin from a hyperthermophile forms a single-stranded filament

Archaeal actin from a hyperthermophile forms a single-stranded filament

Novel Actin-like Filament Structure from Clostridium tetani

The evolution of compositionally and functionally distinct actin filaments

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