Crystal Structure of an Archaeal Actin Homolog

Roeben, Annette; Kofler, Christine; Nagy, István; Nickell, Stephan; Hartl, F. Ulrich; Bracher, A.

doi:10.1016/j.jmb.2006.01.096

Cited by 48 publications

(53 citation statements)

References 44 publications

(42 reference statements)

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“…Very recently, the crystal structure of a predicted actin homologue, Ta0583, of the thermophilic bacterium Thermoplasma acidophilum was determined at a 2.1-Å resolution (137). The structure of Ta0583 showed that it clearly belongs to the actin superfamily.…”

Section: Ta0583mentioning

confidence: 99%

The Bacterial Actin-Like Cytoskeleton

Carballido-López

2006

Microbiol Mol Biol Rev

176

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SUMMARY Recent advances have shown conclusively that bacterial cells possess distant but true homologues of actin (MreB, ParM, and the recently uncovered MamK protein). Despite weak amino acid sequence similarity, MreB and ParM exhibit high structural homology to actin. Just like F-actin in eukaryotes, MreB and ParM assemble into highly dynamic filamentous structures in vivo and in vitro. MreB-like proteins are essential for cell viability and have been implicated in major cellular processes, including cell morphogenesis, chromosome segregation, and cell polarity. ParM (a plasmid-encoded actin homologue) is responsible for driving plasmid-DNA partitioning. The dynamic prokaryotic actin-like cytoskeleton is thought to serve as a central organizer for the targeting and accurate positioning of proteins and nucleoprotein complexes, thereby (and by analogy to the eukaryotic cytoskeleton) spatially and temporally controlling macromolecular trafficking in bacterial cells. In this paper, the general properties and known functions of the actin orthologues in bacteria are reviewed.

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Section: Ta0583mentioning

confidence: 99%

The Bacterial Actin-Like Cytoskeleton

Carballido-López

2006

Microbiol Mol Biol Rev

176

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“…To test this hypothesis, we treated cells with A22 (33). A small-molecule chemical inhibitor of MreB function (9), A22 is thought to interact directly with the MreB ATP-binding pocket, leading to disruption of MreB filaments and consequently diffuse MreB-YFP fluorescence (9); moreover, A22 perturbs the in vitro polymerization of an archaeal MreB homolog (34). When cells were incubated with 10 g͞ml A22, stationary molecules were not observed (see Movie 2, which is published as supporting information on the PNAS web site).…”

Section: Polymerized and Unpolymerized Mreb Can Be Distinctly Visualimentioning

confidence: 99%

Single molecules of the bacterial actin MreB undergo directed treadmilling motion in Caulobacter crescentus

Kim

Gitai

Kinkhabwala

et al. 2006

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

194

241

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The actin cytoskeleton represents a key regulator of multiple essential cellular functions in both eukaryotes and prokaryotes. In eukaryotes, these functions depend on the orchestrated dynamics of actin filament assembly and disassembly. However, the dynamics of the bacterial actin homolog MreB have yet to be examined in vivo. In this study, we observed the motion of single fluorescent MreB-yellow fluorescent protein fusions in living Caulobacter cells in a background of unlabeled MreB. With time-lapse imaging, polymerized MreB [filamentous MreB (fMreB)] and unpolymerized MreB [globular MreB (gMreB)] monomers could be distinguished: gMreB showed fast motion that was characteristic of Brownian diffusion, whereas the labeled molecules in fMreB displayed slow, directed motion. This directional movement of labeled MreB in the growing polymer provides an indication that, like actin, MreB monomers treadmill through MreB filaments by preferential polymerization at one filament end and depolymerization at the other filament end. From these data, we extract several characteristics of single MreB filaments, including that they are, on average, much shorter than the cell length and that the direction of their polarized assembly seems to be independent of the overall cellular polarity. Thus, MreB, like actin, exhibits treadmilling behavior in vivo, and the long MreB structures that have been visualized in multiple bacterial species seem to represent bundles of short filaments that lack a uniform global polarity.bacteria ͉ cytoskeleton ͉ single-molecule fluorescence I n both eukaryotic and prokaryotic cells, actin mediates essential cellular processes. A quantitative understanding of the kinetic dynamics and ultrastructural architecture of actin's polymerized filaments has helped elucidate the mechanisms by which eukaryotic actin functions. For example, high-resolution imaging and the in vivo and in vitro dissection of the kinetics of its assembly have demonstrated how actin polymerization at the tips of a rigid, crosslinked actin meshwork can drive cell motility at the leading edge of Dictyostelium (1, 2). In budding yeast, the polarized assembly of actin cables provides both a road and direction signs for the directed transport of proteins to the tip of growing buds (3).There are two known bacterial actin homologs, the widely conserved, chromosomally encoded MreB family of proteins and the plasmid-specific ParM family of proteins. ParM functions to partition plasmid DNA by polymerizing in between two sister plasmids, thereby generating a tension rod that physically pushes them apart (4). MreB is essential in most bacteria and has been shown to form a lengthwise spiral that contributes to cell shape, chromosome segregation, and polar protein localization in multiple species, including Caulobacter crescentus, Escherichia coli, and Bacillus subtilis (5-10). The mechanism by which MreB executes its functions remains largely unknown (11).In vitro studies of the dynamics of eukaryotic actin filament assembly have demonstrated th...

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“…Roeben et al (61) have argued that these archaeal MreBs likely came from horizontal gene transfers. In this case, MreB may have been lost from the archaeal line early in its development, and re-acquired sporadically by horizontal gene transfer.…”

Section: Evolution Of Mreb and Actinmentioning

confidence: 99%

“…In this case, MreB may have been lost from the archaeal line early in its development, and re-acquired sporadically by horizontal gene transfer. An archaeal MreB from Thermoplasma has structural characteristics very similar to bacterial MreBs, (61,62) but it constitutes only 0.04% of the total cell protein. Interestingly, Thermoplasma does have a robust cytoskeleton, (63) but this MreB appears to be too scarce to be its source.…”

Section: Evolution Of Mreb and Actinmentioning

confidence: 99%

Evolution of the cytoskeleton

2007

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SummaryThe eukaryotic cytoskeleton appears to have evolved from ancestral precursors related to prokaryotic FtsZ and MreB. FtsZ and MreB show 40−50% sequence identity across different bacterial and archaeal species. Here I suggest that this represents the limit of divergence that is consistent with maintaining their functions for cytokinesis and cell shape. Previous analyses have noted that tubulin and actin are highly conserved across eukaryotic species, but so divergent from their prokaryotic relatives as to be hardly recognizable from sequence comparisons. One suggestion for this extreme divergence of tubulin and actin is that it occurred as they evolved very different functions from FtsZ and MreB. I will present new arguments favoring this suggestion, and speculate on pathways. Moreover, the extreme conservation of tubulin and actin across eukaryotic species is not due to an intrinsic lack of variability, but is attributed to their acquisition of elaborate mechanisms for assembly dynamics and their interactions with multiple motor and binding proteins. A new structure-based sequence alignment identifies amino acids that are conserved from FtsZ to tubulins. The highly conserved amino acids are not those forming the subunit core or protofilament interface, but those involved in binding and hydrolysis of GTP. Historical introduction Discoveries of the prokaryotic cytoskeletonBefore 1990, the cytoskeleton was thought to have evolved only in eukaryotes. Relatives or homologs of actin, tubulin or intermediate filaments were unknown in bacteria or archaea. There were sporadic reports of candidates for bacterial actin and tubulin in the 1970s and 1980s but, apart from some intriguing images of microtubules in certain bacteria,(1) these turned out to be wrong and/or were not followed up.The first suggestions of a bacterial homolog of tubulin appeared in 1992. Three groups independently discovered that the bacterial cell division protein FtsZ bound and hydrolyzed GTP, as does tubulin, and had a seven-amino-acid sequence, GGGTGTG, virtually identical to the "tubulin signature sequence".(2-4) Mukherjee and Lutkenhaus(37) then extended the sequence alignment to find a dozen additional amino acids that were completely conserved in FtsZ and in α, β and γ tubulins. They also showed that FtsZ assembled in vitro into filamentous structures. Erickson et al. (5) found that FtsZ assembled into protofilaments that could adopt two conformations, straight and curved, similar to the straight protofilaments of the microtubule wall and the tubulin rings that peel away from microtubules during disassembly. Any question of homology was resolved when tubulin and FtsZ were found to have virtually identical structures at the level of protein folding.(6,7)If one looks for bacterial relatives of tubulin or actin using a simple computer search for sequence similarity, nothing will be found. In 1992 Bork et al.(8) used a sophisticated structurebased sequence alignment, and they discovered that bacteria did have genes related to actin. Actin is...

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Crystal Structure of an Archaeal Actin Homolog

Cited by 48 publications

References 44 publications

The Bacterial Actin-Like Cytoskeleton

The Bacterial Actin-Like Cytoskeleton

Single molecules of the bacterial actin MreB undergo directed treadmilling motion in Caulobacter crescentus

Evolution of the cytoskeleton

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