Prokaryotic DNA segregation by an actin-like filament

Møller‐Jensen, Jakob; Jensen, Rasmus Bugge; Löwe, Jan; Gerdes, Kenn

doi:10.1093/emboj/cdf320

Cited by 239 publications

(235 citation statements)

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“…ParM (64,65) and AlfA(66) assemble actin-like filaments (probably forming bi-polar filament bundles) that bind a plasmid at each end and push them to opposite poles, thus achieving efficient segregation of low-copy-number plasmids. ParM and AlfA are as distantly related to each other as they are to actin, FtsA and MreB.…”

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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Section: Evolution Of Mreb and Actinmentioning

confidence: 99%

Evolution of the cytoskeleton

2007

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“…These results show that the mamK gene alone is sufficient to direct the synthesis and assembly of MamK into a linear structure in a heterologous organism without assistance of other magnetosome-specific proteins. In contrast to MamK filaments, the ParM polymerization requires the presence of the cognate ParR and parC in a host cell (13). parC is a stretch of centromeric DNA, and ParR is a repressor protein that binds to the parC locus (20).…”

Section: Mamk Alone Is Sufficient For Directing Synthesis Of Straightmentioning

confidence: 99%

“…Purified ParM polymerized in an ATP-dependent manner (13) into two-stranded helical filaments similar to conventional actin filaments (14). Electron microscopy of polymeric ParM revealed well separated, individual filaments (13,14).…”

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confidence: 95%

“…The ParM protein binds specifically to the ParR-parC complex, and the ParM filament assembly depends on this complex (12). In vivo, ParM filaments form a bundle that extends the length of the bacterium, with plasmid DNA localized at each ends, and polymerization of ParM has been postulated to provide enough force to push plasmids to opposite poles of the cell (12,13). Purified ParM polymerized in an ATP-dependent manner (13) into two-stranded helical filaments similar to conventional actin filaments (14).…”

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confidence: 99%

“…In vivo, ParM filaments form a bundle that extends the length of the bacterium, with plasmid DNA localized at each ends, and polymerization of ParM has been postulated to provide enough force to push plasmids to opposite poles of the cell (12,13). Purified ParM polymerized in an ATP-dependent manner (13) into two-stranded helical filaments similar to conventional actin filaments (14). Electron microscopy of polymeric ParM revealed well separated, individual filaments (13,14).…”

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Biogenesis of actin-like bacterial cytoskeletal filaments destined for positioning prokaryotic magnetic organelles

Pradel

Santini

Bernadac

et al. 2006

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

100

108

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Magnetosomes comprise a magnetic nanocrystal surrounded by a lipid bilayer membrane. These unique prokaryotic organelles align inside magnetotactic bacterial cells and serve as an intracellular compass allowing the bacteria to navigate along the geomagnetic field in aquatic environments. Cryoelectron tomography of Magnetospirillum strains has revealed that the magnetosome chain is surrounded by a network of filaments that may be composed of MamK given that the filaments are absent in the mamK mutant cells. The process of the MamK filament assembly is unknown. Here we prove the authenticity of the MamK filaments and show that MamK exhibits linear distribution inside Magnetospirillum sp. cells even in the area without magnetosomes. The mamK gene alone is sufficient to direct the synthesis of straight filaments in Escherichia coli, and one extremity of the MamK filaments is located at the cellular pole. By using dual fluorescent labeling of MamK, we found that MamK nucleates at multiple sites and assembles into mosaic filaments. Time-lapse experiments reveal that the assembly of the MamK filaments is a highly dynamic and kinetically asymmetrical process. MamK bundles might initiate the formation of a new filament or associate to one preexistent filament. Our results demonstrate the mechanism of biogenesis of prokaryotic cytoskeletal filaments that are structurally and functionally distinct from the known MreB and ParM filaments. In addition to positioning magnetosomes, other hypothetical functions of the MamK filaments in magnetotaxis might include anchoring magnetosomes and being involved in magnetic reception.assembly ͉ magnetosomes ͉ prokaryote ͉ magnetic reception

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Plasmids

Chattoraj¹

2006

Encyclopedia of Molecular Cell Biology and Molecular Medicine

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Prokaryotic DNA segregation by an actin-like filament

Cited by 239 publications

References 45 publications

Evolution of the cytoskeleton

Evolution of the cytoskeleton

Biogenesis of actin-like bacterial cytoskeletal filaments destined for positioning prokaryotic magnetic organelles

Plasmids

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