Bacterial chromosome segregation.

Dividing cells have mechanisms to ensure that their genomes are faithfully segregated into daughter cells. In bacteria, the description of these mechanisms has been considerably improved in the recent years. This review focuses on the different aspects of bacterial chromosome segregation that can be understood thanks to the studies performed with model organisms: Escherichia coli, Bacillus subtilis, Caulobacter crescentus and Vibrio cholerae. We describe the global positionning of the nucleoid in the cell and the specific localization and dynamics of different chromosomal loci, kinetic and biophysic aspects of chromosome segregation are presented. Finally, a presentation of the key proteins involved in the chromosome segregation is made.

[1]  Flemming G. Hansen,et al.  Dynamics of Escherichia coli Chromosome Segregation during Multifork Replication , 2007, Journal of bacteriology.

[2]  F. Hansen,et al.  Progressive segregation of the Escherichia coli chromosome , 2006, Molecular microbiology.

[3]  William Dowhan,et al.  Effects of Phospholipid Composition on MinD-Membrane Interactions in Vitro and in Vivo* , 2003, Journal of Biological Chemistry.

[4]  D J MASON,et al.  NUCLEAR DIVISION AS OBSERVED IN LIVE BACTERIA BY A NEW TECHNIQUE , 1956, Journal of bacteriology.

[5]  Meriem El Karoui,et al.  KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase , 2005, The EMBO journal.

[6]  Ivan Junier,et al.  Spatial and Topological Organization of DNA Chains Induced by Gene Co-localization , 2010, PLoS Comput. Biol..

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

[8]  Z. M. Petrushenko,et al.  DNA Reshaping by MukB RIGHT-HANDED KNOTTING, LEFT-HANDED SUPERCOILING* , 2006, Journal of Biological Chemistry.

[9]  A. Murray,et al.  Chromosome and Low Copy Plasmid Segregation in E. coli: Visual Evidence for Distinct Mechanisms , 1997, Cell.

[10]  Nelly Dubarry,et al.  Multiple regions along the Escherichia coli FtsK protein are implicated in cell division , 2010, Molecular microbiology.

[11]  S. Hiraga,et al.  Dynamic events of sister chromosomes in the cell cycle of Escherichia coli , 2008, Genes to cells : devoted to molecular & cellular mechanisms.

[12]  D. Sherratt,et al.  Modulation of Escherichia coli sister chromosome cohesion by topoisomerase IV. , 2008, Genes & development.

[13]  M. Rossignol,et al.  Macrodomain organization of the Escherichia coli chromosome , 2004, The EMBO journal.

[14]  A. Grossman,et al.  The extrusion-capture model for chromosome partitioning in bacteria. , 2001, Genes & development.

[15]  Ralf Everaers,et al.  Structure and Dynamics of Interphase Chromosomes , 2008, PLoS Comput. Biol..

[16]  C. Woldringh,et al.  Structural and physical aspects of bacterial chromosome segregation. , 2006, Journal of structural biology.

[17]  R. B. Jensen Analysis of the Terminus Region of the Caulobacter crescentus Chromosome and Identification of the dif Site , 2006, Journal of bacteriology.

[18]  Martin A. White,et al.  Non-random segregation of sister chromosomes in Escherichia coli , 2008, Nature.

[19]  Omar A Saleh,et al.  Fast, DNA‐sequence independent translocation by FtsK in a single‐molecule experiment , 2004, The EMBO journal.

[20]  S. Kennedy,et al.  Delayed activation of Xer recombination at dif by FtsK during septum assembly in Escherichia coli , 2008, Molecular microbiology.

[21]  Andrew Wright,et al.  Entropy as the driver of chromosome segregation , 2010, Nature Reviews Microbiology.

[22]  Guohua Yang,et al.  MreB is important for cell shape but not for chromosome segregation of the filamentous cyanobacterium Anabaena sp. PCC 7120 , 2007, Molecular microbiology.

[23]  Itzhak Fishov,et al.  Visualization of membrane domains in Escherichia coli , 1999, Molecular microbiology.

[24]  S. Brenner,et al.  [On the regulation of DNA synthesis in bacteria: the hypothesis of the replicon]. , 1963, Comptes rendus hebdomadaires des seances de l'Academie des sciences.

[25]  P. Schaeffer,et al.  [Cytologic classification, by their blockage stage, of sporulation mutants of Bacillus subtilis Marburg]. , 1966, Annales de l'Institut Pasteur.

[26]  J. Errington,et al.  Recruitment of Condensin to Replication Origin Regions by ParB/SpoOJ Promotes Chromosome Segregation in B. subtilis , 2009, Cell.

[27]  Stéphane Robin,et al.  The MatP/matS Site-Specific System Organizes the Terminus Region of the E. coli Chromosome into a Macrodomain , 2008, Cell.

[28]  C. D. Hardy,et al.  Topological challenges to DNA replication: Conformations at the fork , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[29]  A. Grossman,et al.  Bipolar Localization of the Replication Origin Regions of Chromosomes in Vegetative and Sporulating Cells of B. subtilis , 1997, Cell.

[30]  A. Grossman,et al.  Identification and Characterization of a Bacterial Chromosome Partitioning Site , 1998, Cell.

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

[32]  M. Waldor,et al.  par genes and the pathology of chromosome loss in Vibrio cholerae , 2007, Proceedings of the National Academy of Sciences.

[33]  B. Peter,et al.  The Structure of Supercoiled Intermediates in DNA Replication , 1998, Cell.

[34]  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.

[35]  Ian Grainge,et al.  Tracking of controlled Escherichia coli replication fork stalling and restart at repressor‐bound DNA in vivo , 2006, The EMBO journal.

[36]  Stuart Austin,et al.  The segregation of the Escherichia coli origin and terminus of replication , 2002, Molecular microbiology.

[37]  Kim Nasmyth,et al.  Cohesin: its roles and mechanisms. , 2009, Annual review of genetics.

[38]  Andrew W. Murray,et al.  GFP tagging of budding yeast chromosomes reveals that protein–protein interactions can mediate sister chromatid cohesion , 1996, Current Biology.

[39]  P. Kuempel,et al.  Sister Chromatid Exchange Frequencies inEscherichia coli Analyzed by Recombination at thedif Resolvase Site , 1998, Journal of bacteriology.

[40]  L. Shapiro,et al.  A spindle-like apparatus guides bacterial chromosome segregation , 2010, Nature Cell Biology.

[41]  C. Jacobs-Wagner,et al.  Cell cycle coordination and regulation of bacterial chromosome segregation dynamics by polarly localized proteins , 2010, The EMBO journal.

[42]  D. Sherratt,et al.  MukB colocalizes with the oriC region and is required for organization of the two Escherichia coli chromosome arms into separate cell halves , 2007, Molecular microbiology.

[43]  S. Hiraga,et al.  Sister chromosome cohesion of Escherichia coli , 2001, Molecular microbiology.

[44]  C. Woldringh,et al.  Single-particle tracking of oriC-GFP fluorescent spots during chromosome segregation in Escherichia coli. , 2005, Journal of structural biology.

[45]  Nelly Dubarry,et al.  Fully efficient chromosome dimer resolution in Escherichia coli cells lacking the integral membrane domain of FtsK , 2010, The EMBO journal.

[46]  R. Losick,et al.  RacA, a Bacterial Protein That Anchors Chromosomes to the Cell Poles , 2002, Science.

[47]  D. Sherratt,et al.  Independent Positioning and Action of Escherichia coli Replisomes in Live Cells , 2008, Cell.

[48]  S. Jun Can entropy save bacteria , 2008, 0808.2646.

[49]  Christian Lesterlin,et al.  Asymmetry of Chromosome Replichores Renders the DNA Translocase Activity of FtsK Essential for Cell Division and Cell Shape Maintenance in Escherichia coli , 2008, PLoS genetics.

[50]  D. Sherratt,et al.  The two Escherichia coli chromosome arms locate to separate cell halves. , 2006, Genes & development.

[51]  F. Cornet,et al.  FtsK, a literate chromosome segregation machine , 2007, Molecular microbiology.

[52]  Paul A. Wiggins,et al.  Strong intranucleoid interactions organize the Escherichia coli chromosome into a nucleoid filament , 2010, Proceedings of the National Academy of Sciences.

[53]  O. Espéli,et al.  Chromosome Structuring Limits Genome Plasticity in Escherichia coli , 2007, PLoS genetics.

[54]  T. Odijk,et al.  Osmotic compaction of supercoiled DNA into a bacterial nucleoid. , 1998, Biophysical chemistry.

[55]  L. Shapiro,et al.  MipZ, a Spatial Regulator Coordinating Chromosome Segregation with Cell Division in Caulobacter , 2006, Cell.

[56]  J. Tomizawa,et al.  Replication of the escherichia coli K12 chromosome. , 1967, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Michelle D. Wang,et al.  Force and velocity measured for single molecules of RNA polymerase. , 1998, Science.

[58]  S. Kennedy,et al.  FtsK-Dependent Dimer Resolution on Multiple Chromosomes in the Pathogen Vibrio cholerae , 2008, PLoS genetics.

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

[60]  L. Shapiro,et al.  A Polymeric Protein Anchors the Chromosomal Origin/ParB Complex at a Bacterial Cell Pole , 2008, Cell.

[61]  N R Cozzarelli,et al.  Topoisomerase IV, not gyrase, decatenates products of site-specific recombination in Escherichia coli. , 1997, Genes & development.

[62]  W. Margolin,et al.  Role of the C terminus of FtsK in Escherichia coli chromosome segregation. , 1998, Journal of bacteriology.

[63]  D. Rudner,et al.  Recruitment of SMC by ParB-parS Organizes the Origin Region and Promotes Efficient Chromosome Segregation , 2009, Cell.

[64]  M. Vázquez,et al.  Unlinking chromosome catenanes in vivo by site‐specific recombination , 2007, The EMBO journal.

[65]  P. Srivastava,et al.  Segregation of the Replication Terminus of the Two Vibrio cholerae Chromosomes , 2006, Journal of bacteriology.

[66]  L. Finzi,et al.  Single-molecule kinetic studies on DNA transcription and transcriptional regulation. , 1995, Biophysical journal.

[67]  K. Marians,et al.  Physical and functional interaction between the condensin MukB and the decatenase topoisomerase IV in Escherichia coli , 2010, Proceedings of the National Academy of Sciences.

[68]  O. Espéli,et al.  DNA dynamics vary according to macrodomain topography in the E. coli chromosome , 2008, Molecular microbiology.

[69]  N. Kleckner,et al.  Chromosome and Replisome Dynamics in E. coli: Loss of Sister Cohesion Triggers Global Chromosome Movement and Mediates Chromosome Segregation , 2005, Cell.

[70]  Kim Nasmyth,et al.  Segregating Sister Genomes: The Molecular Biology of Chromosome Separation , 2002, Science.

[71]  O. Espéli,et al.  Temporal regulation of topoisomerase IV activity in E. coli. , 2003, Molecular cell.

[72]  L. Shapiro,et al.  The Bifunctional FtsK Protein Mediates Chromosome Partitioning and Cell Division in Caulobacter , 2006, Journal of bacteriology.

[73]  N. Kleckner,et al.  Escherichia coli sister chromosome separation includes an abrupt global transition with concomitant release of late-splitting intersister snaps , 2011, Proceedings of the National Academy of Sciences.

[74]  Davide Marenduzzo,et al.  Entropic organization of interphase chromosomes , 2009, The Journal of cell biology.

[75]  V. Norris,et al.  Hypothesis: membrane domains and hyperstructures control bacterial division. , 2001, Biochimie.

[76]  D. Chattoraj,et al.  A cis‐acting sequence involved in chromosome segregation in Escherichia coli , 2004, Molecular microbiology.

[77]  M. Waldor,et al.  Distinct segregation dynamics of the two Vibrio cholerae chromosomes , 2004, Molecular microbiology.

[78]  K. Chater,et al.  Alignment of multiple chromosomes along helical ParA scaffolding in sporulating Streptomyces hyphae , 2007, Molecular microbiology.

[79]  仁木 宏典 The new gene mukB codes for a 177 kd protein with coiled-coil domains involved in chromosome partitioning of E. coli , 1991 .

[80]  Melanie B. Berkmen,et al.  Spatial and temporal organization of the Bacillus subtilis replication cycle , 2006, Molecular microbiology.

[81]  Y. Hirota,et al.  Gene organization in the region containing a new gene involved in chromosome partition in Escherichia coli , 1988, Journal of bacteriology.

[82]  H. E. Kubitschek,et al.  Chromosome Replication and the Division Cycle of Escherichia coli B/r , 1971, Journal of bacteriology.

[83]  J. Theriot,et al.  Fine-scale time-lapse analysis of the biphasic, dynamic behaviour of the two Vibrio cholerae chromosomes , 2006, Molecular microbiology.

[84]  Jan Löwe,et al.  Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. , 2006, Molecular cell.

[85]  J. E. Cabrera,et al.  Active Transcription of rRNA Operons Condenses the Nucleoid in Escherichia coli: Examining the Effect of Transcription on Nucleoid Structure in the Absence of Transertion , 2009, Journal of bacteriology.

[86]  D. Lane,et al.  ParABS Systems of the Four Replicons of Burkholderia cenocepacia: New Chromosome Centromeres Confer Partition Specificity , 2006, Journal of bacteriology.

[87]  D. Sherratt,et al.  Dancing around the divisome: asymmetric chromosome segregation in Escherichia coli. , 2005, Genes & development.

[88]  Naotake Ogasawara,et al.  Escherichia coli with a linear genome , 2007, EMBO reports.

[89]  Zemer Gitai,et al.  Caulobacter chromosome segregation is an ordered multistep process , 2010, Proceedings of the National Academy of Sciences.

[90]  D. Bates The bacterial replisome: back on track? , 2008, Molecular microbiology.

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

[92]  I. Fishov,et al.  Membrane-catalyzed Nucleotide Exchange on DnaA , 2006, Journal of Biological Chemistry.

[93]  C. M. Berg,et al.  Chromosome replication in some strains of Escherichia coli K12. , 1968, Cold Spring Harbor symposia on quantitative biology.

[94]  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.

[95]  S. Austin,et al.  Segregation of the Escherichia coli chromosome terminus , 2003, Molecular microbiology.

[96]  S. Ben-Yehuda,et al.  Spatial organization of a replicating bacterial chromosome , 2008, Proceedings of the National Academy of Sciences.

[97]  O. Espéli,et al.  A Physical and Functional Interaction between Escherichia coli FtsK and Topoisomerase IV* , 2003, Journal of Biological Chemistry.