Cytoskeletal elements in bacteria.

All cytoskeletal elements known from eukaryotic cells are also present in bacteria, where they perform vital tasks in many aspects of the physiology of the cell. Bacterial tubulin (FtsZ), actin (MreB), and intermediate filament (IF) proteins are key elements in cell division, chromosome and plasmid segregation, and maintenance of proper cell shape, as well as in maintenance of cell polarity and assembly of intracellular organelle-like structures. Although similar tasks are performed by eukaryotic cytoskeletal elements, the individual functions of FtsZ, MreBs, and IFs are different from those performed by their eukaryotic orthologs, revealing a striking evolutional plasticity of cytoskeletal proteins. However, similar to the functions of their eukaryotic counterparts, the functions conferred by bacterial cytoskeletal proteins are driven by their ability to form dynamic filamentous structures. Therefore, the cytoskeleton was a prokaryotic invention, and additional bacteria-specific cytoskeletal elements, such as fibril and MinD-type ATPases, that confer various functions in cell morphology and during the cell cycle have been observed in prokaryotes. The investigation of these elements will give fundamental information for all types of cells and can reveal the molecular mode of action of cytoskeletal, filament-forming proteins.

[1]  M. Rosenberg,et al.  Bacterial DNA segregation dynamics mediated by the polymerizing protein ParF , 2005, The EMBO journal.

[2]  C. Hale,et al.  Direct Binding of FtsZ to ZipA, an Essential Component of the Septal Ring Structure That Mediates Cell Division in E. coli , 1997, Cell.

[3]  O. Massidda,et al.  Cell division in cocci: localization and properties of the Streptococcus pneumoniae FtsA protein , 2004, Molecular microbiology.

[4]  Akira Ishihama,et al.  Two types of localization of the DNA‐binding proteins within the Escherichia coli nucleoid , 2000, Genes to cells : devoted to molecular & cellular mechanisms.

[5]  J. Errington,et al.  A magnesium‐dependent mreB null mutant: implications for the role of mreB in Bacillus subtilis , 2005, Molecular microbiology.

[6]  W. Margolin,et al.  FtsZ Dynamics during the Division Cycle of LiveEscherichia coli Cells , 1998, Journal of bacteriology.

[7]  W. Margolin,et al.  A gain-of-function mutation in ftsA bypasses the requirement for the essential cell division gene zipA in Escherichia coli , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[8]  P. Graumann,et al.  Dynamic movement of actin‐like proteins within bacterial cells , 2004, EMBO reports.

[9]  J. Errington,et al.  Control of Cell Morphogenesis in Bacteria Two Distinct Ways to Make a Rod-Shaped Cell , 2003, Cell.

[10]  R. B. Jensen,et al.  Prokaryotic DNA segregation by an actin‐like filament , 2002, The EMBO journal.

[11]  Jan Löwe,et al.  Structural insights into FtsZ protofilament formation , 2004, Nature Structural &Molecular Biology.

[12]  R. Losick,et al.  Morphological coupling in development: lessons from prokaryotes. , 2001, Developmental cell.

[13]  S. Ishikawa,et al.  A new FtsZ‐interacting protein, YlmF, complements the activity of FtsA during progression of cell division in Bacillus subtilis , 2006, Molecular microbiology.

[14]  Peter Roepstorff,et al.  Bacterial mitosis: ParM of plasmid R1 moves plasmid DNA by an actin-like insertional polymerization mechanism. , 2003, Molecular cell.

[15]  Judith P. Armitage,et al.  Differential Localization of Mre Proteins with PBP2 in Rhodobacter sphaeroides , 2006, Journal of bacteriology.

[16]  J. Löwe,et al.  A bacterial dynamin-like protein , 2006, Nature.

[17]  J. Lutkenhaus,et al.  Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[18]  J. Lutkenhaus,et al.  Bacterial cell division and the Z ring. , 1997, Annual review of biochemistry.

[19]  Lucy Shapiro,et al.  Dynamic Spatial Regulation in the Bacterial Cell , 2000, Cell.

[20]  M. Mann,et al.  Actin homolog MreB and RNA polymerase interact and are both required for chromosome segregation in Escherichia coli. , 2006, Genes & development.

[21]  P. D. de Boer,et al.  ZipA-Induced Bundling of FtsZ Polymers Mediated by an Interaction between C-Terminal Domains , 2000, Journal of bacteriology.

[22]  D. Wirtz,et al.  The Assembly of MreB, a Prokaryotic Homolog of Actin* , 2005, Journal of Biological Chemistry.

[23]  S. Tamaki,et al.  Mutant isolation and molecular cloning of mre genes, which determine cell shape, sensitivity to mecillinam, and amount of penicillin-binding proteins in Escherichia coli , 1987, Journal of bacteriology.

[24]  A. Grossman,et al.  Localization of bacterial DNA polymerase: evidence for a factory model of replication. , 1998, Science.

[25]  P. Graumann,et al.  Actin-like Proteins MreB and Mbl from Bacillus subtilis Are Required for Bipolar Positioning of Replication Origins , 2003, Current Biology.

[26]  Damien Faivre,et al.  An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria , 2006, Nature.

[27]  P. Graumann,et al.  Specific polar localization of ribosomes in Bacillus subtilis depends on active transcription , 2001, EMBO reports.

[28]  Zemer Gitai,et al.  MreB Actin-Mediated Segregation of a Specific Region of a Bacterial Chromosome , 2005, Cell.

[29]  Achilleas S. Frangakis,et al.  Cryo-Electron Tomography Reveals the Cytoskeletal Structure of Spiroplasma melliferum , 2005, Science.

[30]  C. Santini,et al.  Biogenesis of actin-like bacterial cytoskeletal filaments destined for positioning prokaryotic magnetic organelles , 2006, Proceedings of the National Academy of Sciences.

[31]  S. Hiraga,et al.  Different localization of SeqA‐bound nascent DNA clusters and MukF–MukE–MukB complex in Escherichia coli cells , 2001, Molecular microbiology.

[32]  J. Lutkenhaus,et al.  Organization of genes in the ftsA-envA region of the Escherichia coli genetic map and identification of a new fts locus (ftsZ) , 1980, Journal of bacteriology.

[33]  Jan Löwe,et al.  F‐actin‐like filaments formed by plasmid segregation protein ParM , 2002, The EMBO journal.

[34]  Ram Samudrala,et al.  Genes for the cytoskeletal protein tubulin in the bacterial genus Prosthecobacter , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Grant J. Jensen,et al.  Magnetosomes Are Cell Membrane Invaginations Organized by the Actin-Like Protein MamK , 2006, Science.

[36]  C. Jacobs-Wagner,et al.  The Bacterial Cytoskeleton An Intermediate Filament-Like Function in Cell Shape , 2003, Cell.

[37]  J. Izard,et al.  Tomographic reconstruction of treponemal cytoplasmic filaments reveals novel bridging and anchoring components , 2003, Molecular microbiology.

[38]  A. Grossman,et al.  Chromosome arrangement within a bacterium , 1998, Current Biology.

[39]  F. Lafuma,et al.  A biomimetic motility assay provides insight into the mechanism of actin-based motility , 2003, The Journal of cell biology.

[40]  Gilles P van Wezel,et al.  MreB of Streptomyces coelicolor is not essential for vegetative growth but is required for the integrity of aerial hyphae and spores , 2006, Molecular microbiology.

[41]  L. Wu Structure and segregation of the bacterial nucleoid. , 2004, Current opinion in genetics & development.

[42]  J. Gober,et al.  MreB, the cell shape‐determining bacterial actin homologue, co‐ordinates cell wall morphogenesis in Caulobacter crescentus , 2004, Molecular microbiology.

[43]  R. Losick,et al.  Asymmetric Cell Division in B. subtilis Involves a Spiral-like Intermediate of the Cytokinetic Protein FtsZ , 2002, Cell.

[44]  M. Omary,et al.  Cellular integrity plus: organelle-related and protein-targeting functions of intermediate filaments. , 2005, Trends in cell biology.

[45]  Zemer Gitai,et al.  An actin-like gene can determine cell polarity in bacteria. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[46]  H. Niki,et al.  migS, a cis‐acting site that affects bipolar positioning of oriC on the Escherichia coli chromosome , 2004, The EMBO journal.

[47]  James T. Staley,et al.  In vitro assembly and GTP hydrolysis by bacterial tubulins BtubA and BtubB , 2005, The Journal of cell biology.

[48]  J. Lutkenhaus,et al.  FtsZ‐spirals and ‐arcs determine the shape of the invaginating septa in some mutants of Escherichia coli , 1996, Molecular microbiology.

[49]  O. Espéli,et al.  SetB: an integral membrane protein that affects chromosome segregation in Escherichia coli , 2003, Molecular microbiology.

[50]  R. Leapman,et al.  Mass Distribution and Spatial Organization of the Linear Bacterial Motor of Spiroplasma citri R8A2 , 2003, Journal of bacteriology.

[51]  Patrick T. McGrath,et al.  Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[52]  P. Graumann Cytoskeletal elements in bacteria. , 2004, Current opinion in microbiology.

[53]  Jan Kok,et al.  Subcellular sites for bacterial protein export , 2004, Molecular microbiology.

[54]  J. Errington,et al.  Compartmentalization of transcription and translation in Bacillus subtilis , 2000, The EMBO journal.

[55]  T. Kruse,et al.  Dysfunctional MreB inhibits chromosome segregation in Escherichia coli , 2003, The EMBO journal.

[56]  J. Izard,et al.  Cytoplasmic Filament-Deficient Mutant ofTreponema denticola Has Pleiotropic Defects , 2001, Journal of bacteriology.

[57]  Jan Löwe,et al.  Structure of bacterial tubulin BtubA/B: evidence for horizontal gene transfer. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[58]  U. Göbel,et al.  Filamentous structures in adherent Mycoplasma pneumoniae cells treated with nonionic detergents , 1981, The Journal of cell biology.

[59]  S. Trachtenberg,et al.  The bacterial linear motor of Spiroplasma melliferum BC3: from single molecules to swimming cells , 2003, Molecular microbiology.

[60]  L. Amos,et al.  Structural/functional homology between the bacterial and eukaryotic cytoskeletons. , 2004, Current opinion in cell biology.

[61]  R. Losick,et al.  Does RNA polymerase help drive chromosome segregation in bacteria? , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Judith P. Armitage,et al.  Localization of MreB in Rhodobacter sphaeroides under Conditions Causing Changes in Cell Shape and Membrane Structure , 2005, Journal of bacteriology.

[63]  A. Yamagishi,et al.  An Actin Homolog of the Archaeon Thermoplasma acidophilum That Retains the Ancient Characteristics of Eukaryotic Actin , 2006, Journal of bacteriology.

[64]  Daniel P. Haeusser,et al.  EzrA prevents aberrant cell division by modulating assembly of the cytoskeletal protein FtsZ , 2004, Molecular microbiology.

[65]  J. Errington,et al.  Roles for MreC and MreD proteins in helical growth of the cylindrical cell wall in Bacillus subtilis , 2005, Molecular microbiology.

[66]  P A de Boer,et al.  Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[67]  J. Izard,et al.  Genetic and Structural Analyses of Cytoplasmic Filaments of Wild-Type Treponema phagedenis and a Flagellar Filament-Deficient Mutant , 1999, Journal of bacteriology.

[68]  L. Amos,et al.  Crystal structure of the bacterial cell-division protein FtsZ , 1998, Nature.

[69]  R. Losick,et al.  A three‐protein inhibitor of polar septation during sporulation in Bacillus subtilis , 2001, Molecular microbiology.

[70]  P. Graumann,et al.  Bacillus subtilis actin-like protein MreB influences the positioning of the replication machinery and requires membrane proteins MreC/D and other actin-like proteins for proper localization , 2005, BMC Cell Biology.

[71]  J. Errington,et al.  Coordination of Cell Division and Chromosome Segregation by a Nucleoid Occlusion Protein in Bacillus subtilis , 2004, Cell.

[72]  P. Graumann,et al.  Dynamic localization and interaction with other Bacillus subtilis actin‐like proteins are important for the function of MreB , 2006, Molecular microbiology.

[73]  Y. Sakagami,et al.  Determinations of the DNA sequence of the mreB gene and of the gene products of the mre region that function in formation of the rod shape of Escherichia coli cells , 1988, Journal of bacteriology.

[74]  D. Wirtz,et al.  GTPase Activity, Structure, and Mechanical Properties of Filaments Assembled from Bacterial Cytoskeleton Protein MreB , 2006, Journal of bacteriology.

[75]  K. Gerdes,et al.  Bacterial mitosis: partitioning protein ParA oscillates in spiral‐shaped structures and positions plasmids at mid‐cell , 2004, Molecular microbiology.

[76]  P Bork,et al.  An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[77]  P. Graumann,et al.  An intracellular actin motor in bacteria? , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[78]  Leigh G. Monahan,et al.  Trapping of a Spiral-Like Intermediate of the Bacterial Cytokinetic Protein FtsZ , 2006, Journal of bacteriology.

[79]  W. Margolin,et al.  FtsZ Exhibits Rapid Movement and Oscillation Waves in Helix-like Patterns in Escherichia coli , 2004, Current Biology.

[80]  Y. Kasahara,et al.  Two separate DNA sequences within oriC participate in accurate chromosome segregation in Bacillus subtilis , 2002, Molecular microbiology.

[81]  Frederico J. Gueiros-Filho,et al.  A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. , 2002, Genes & development.

[82]  M. Buttner,et al.  Identification and characterization of the mre gene region of Streptomyces coelicolor A3(2) , 2000, Molecular and General Genetics MGG.

[83]  Ruifeng Yang,et al.  AglZ Is a Filament-Forming Coiled-Coil Protein Required for Adventurous Gliding Motility of Myxococcus xanthus , 2004, Journal of bacteriology.

[84]  H. Erickson,et al.  Atomic structures of tubulin and FtsZ. , 1998, Trends in cell biology.

[85]  George Oster,et al.  Polymer Motors: Pushing out the Front and Pulling up the Back , 2003, Current Biology.

[86]  J. Pogliano,et al.  Bacterial DNA segregation by dynamic SopA polymers. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[87]  E. Bi,et al.  FtsZ ring structure associated with division in Escherichia coli , 1991, Nature.

[88]  P. D. de Boer,et al.  SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over Chromosomes in E. coli. , 2005, Molecular cell.

[89]  D. Schüler Molecular analysis of a subcellular compartment: the magnetosome membrane in Magnetospirillum gryphiswaldense , 2003, Archives of Microbiology.

[90]  Jan Löwe,et al.  Prokaryotic origin of the actin cytoskeleton , 2001, Nature.

[91]  F. Hartl,et al.  Crystal structure of an archaeal actin homolog. , 2006, Journal of molecular biology.

[92]  J. Gober,et al.  The cell-shape protein MreC interacts with extracytoplasmic proteins including cell wall assembly complexes in Caulobacter crescentus. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[93]  J. Lutkenhaus,et al.  Topological regulation of cell division in E. coli. spatiotemporal oscillation of MinD requires stimulation of its ATPase by MinE and phospholipid. , 2001, Molecular cell.

[94]  S. Ehrlich,et al.  Actin homolog MreBH governs cell morphogenesis by localization of the cell wall hydrolase LytE. , 2006, Developmental cell.

[95]  J. Errington,et al.  Cytokinesis in Bacteria , 2003, Microbiology and Molecular Biology Reviews.

[96]  J. Lutkenhaus,et al.  Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli , 2002, The EMBO journal.

[97]  J. Bové,et al.  Nucleotide sequence of the Spiroplasma citri fibril protein gene , 1991, Journal of bacteriology.

[98]  Jan Löwe,et al.  Crystal structure of the cell division protein FtsA from Thermotoga maritima , 2000, The EMBO journal.

[99]  A. Strunnikov,et al.  Cell cycle‐dependent localization of two novel prokaryotic chromosome segregation and condensation proteins in Bacillus subtilis that interact with SMC protein , 2002, The EMBO journal.

[100]  E. Garner,et al.  Dynamic Instability in a DNA-Segregating Prokaryotic Actin Homolog , 2004, Science.

[101]  R. Losick,et al.  Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ , 1994, Molecular microbiology.

[102]  Yu-Ling Shih,et al.  Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[103]  J. Errington,et al.  Several distinct localization patterns for penicillin‐binding proteins in Bacillus subtilis , 2003, Molecular microbiology.

[104]  Jeff Errington,et al.  The bacterial cytoskeleton: in vivo dynamics of the actin-like protein Mbl of Bacillus subtilis. , 2003, Developmental cell.

[105]  J. Lutkenhaus,et al.  The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[106]  A. Driessen,et al.  Immediate GTP hydrolysis upon FtsZ polymerization , 2002, Molecular microbiology.

[107]  R. Valluzzi,et al.  Dynamic assembly of MinD into filament bundles modulated by ATP, phospholipids, and MinE , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[108]  W. Margolin,et al.  FtsZ and the division of prokaryotic cells and organelles , 2005, Nature Reviews Molecular Cell Biology.

[109]  J. Pogliano,et al.  DNA segregation by the bacterial actin AlfA during Bacillus subtilis growth and development , 2006, The EMBO journal.

[110]  J. Errington,et al.  Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. , 1998, Genes & development.

[111]  Thomas Kruse,et al.  The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane‐bound complex , 2004, Molecular microbiology.

[112]  J. Errington,et al.  Control of Cell Shape in Bacteria Helical, Actin-like Filaments in Bacillus subtilis , 2001, Cell.

[113]  A. Grossman,et al.  Movement of replicating DNA through a stationary replisome. , 2000, Molecular cell.

[114]  M. Goldberg,et al.  Presence of Multiple Sites Containing Polar Material in Spherical Escherichia coli Cells That Lack MreB , 2005, Journal of Bacteriology.

[115]  R. B. Jensen,et al.  Multiple large filament bundles observed in Caulobacter crescentus by electron cryotomography , 2006, Molecular microbiology.

[116]  D. Sherratt,et al.  Regular cellular distribution of plasmids by oscillating and filament‐forming ParA ATPase of plasmid pB171 , 2006, Molecular microbiology.

[117]  Alexander van Oudenaarden,et al.  Biomimetic Systems for Studying Actin-Based Motility , 2003, Current Biology.

[118]  A. Grossman,et al.  Subcellular localization of the Bacillus subtilis structural maintenance of chromosomes (SMC) protein , 2002, Molecular microbiology.

[119]  H. Erickson,et al.  Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[120]  G. Weinstock,et al.  Characterization of the cytoplasmic filament protein gene (cfpA) of Treponema pallidum subsp. pallidum , 1996, Journal of bacteriology.

[121]  Harvey T. McMahon,et al.  The dynamin superfamily: universal membrane tubulation and fission molecules? , 2004, Nature Reviews Molecular Cell Biology.

[122]  E. Salmon,et al.  Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[123]  A. Görg,et al.  Defining the mycoplasma 'cytoskeleton': the protein composition of the Triton X-100 insoluble fraction of the bacterium Mycoplasma pneumoniae determined by 2-D gel electrophoresis and mass spectrometry. , 2001, Microbiology.

[124]  Zemer Gitai,et al.  Single molecules of the bacterial actin MreB undergo directed treadmilling motion in Caulobacter crescentus. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[125]  E. Biondi,et al.  Extended phenotype of an mreB-like mutant in Azospirillum brasilense. , 2004, Microbiology.

[126]  Borrelia burgdorferi ftsZ Plays a Role in Cell Division , 2006, Journal of bacteriology.

[127]  Patrick England,et al.  The Scc Spirochetal Coiled-Coil Protein Forms Helix-Like Filaments and Binds to Nucleic Acids Generating Nucleoprotein Structures , 2006, Journal of bacteriology.

[128]  Zachary Pincus,et al.  Two independent spiral structures control cell shape in Caulobacter. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[129]  P A de Boer,et al.  Dynamic localization cycle of the cell division regulator MinE in Escherichia coli , 2001, The EMBO journal.

[130]  D. Rudner,et al.  Imaging peptidoglycan biosynthesis in Bacillus subtilis with fluorescent antibiotics. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[131]  Thomas Kruse,et al.  Bacterial Mitotic Machineries , 2004, Cell.

[132]  J. Lutkenhaus,et al.  Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichia coli. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[133]  G. Stewart,et al.  Bacillus subtilis possesses a second determinant with extensive sequence similarity to the Escherichia coli mreB morphogene , 1995, Journal of bacteriology.

[134]  Yuichiro Maéda,et al.  Concerning the dynamic instability of actin homolog ParM. , 2007, Biochemical and biophysical research communications.

[135]  J. Lutkenhaus,et al.  Dynamic proteins in bacteria. , 2002, Current opinion in microbiology.

[136]  J. Lutkenhaus,et al.  The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli , 1992, Journal of bacteriology.

[137]  H. Niki,et al.  Dynamic organization of chromosomal DNA in Escherichia coli. , 2000, Genes & development.

[138]  Y. Okada,et al.  New mre genes mreC and mreD, responsible for formation of the rod shape of Escherichia coli cells , 1989, Journal of bacteriology.