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The Chromosome Segregation Machinery in Bacteria

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Abstract

Two different mechanisms for chromosome segregation can be envisioned in bacteria based on current knowledge. In some bacteria that have a single chromosome, the separation of sister chromosomes is achieved by an active machinery that can move individual regions on the chromosomes over a distance of several microns within a few minutes. This process is independent of cell elongation. Several key factors have been identified for this active machinery and will be discussed. However, the driving “motor” has not yet been discovered, although suspicious candidates like filament-forming proteins and RNA polymerase are under intensive investigation. Alternatively, chromosomes can be randomly separated if several copies are present within the cell, which seems to occur in the bacterial phylum of Cyanobacteria, and possibly in many other species.

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References

  • Angert ER, Clements KD (2004) Initiation of intracellular offspring in Epulopiscium. Mol Microbiol 51:827-835

    Article  CAS  PubMed  Google Scholar 

  • Aussel L, Barre FX, Aroyo M, Stasiak A, Stasiak AZ, Sherratt D (2002) FtsK is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell 108:195-205

    Article  CAS  PubMed  Google Scholar 

  • Azam TA, Hiraga S, Ishihama A (2000) Two types of localization of the DNA-binding proteins within the Escherichia coli nucleoid. Genes Cells 5:613-626

    Article  CAS  PubMed  Google Scholar 

  • Barilla D, Rosenberg MF, Nobbmann U, Hayes F (2005) Bacterial DNA segregation dynamics mediated by the polymerizing protein ParF. EMBO J 24:1453-1464

    Article  CAS  PubMed  Google Scholar 

  • Bates D, Kleckner N (2005) Chromosome and replisome dynamics in E coli: loss of sister cohesion triggers global chromosome movement and mediates chromosome segregation. Cell 121:899-911

    Article  CAS  PubMed  Google Scholar 

  • Ben-Yehuda S, Losick R (2002) Asymmetric cell division in B. subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ. Cell 109:257-266

    Article  CAS  PubMed  Google Scholar 

  • Blakely G, May G, McCulloch R, Arciszewska LK, Burke M, Lovett ST, Sherratt DJ (1993) Two related recombinases are required for site-specific recombination at dif and cer in E coli K12. Cell 75:351-361

    Article  CAS  PubMed  Google Scholar 

  • Breuert S, Allers T, Spohn G, Soppa J (2006) Regulated polyploidy in halophilic archaea. PLoS ONE 1:e92

    Article  PubMed  Google Scholar 

  • Britton RA, Lin DC-H, Grossman AD (1998a) Characterization of a prokaryotic SMC protein involved in chromosome partitioning. Genes Dev 12:1254-1259

    Article  CAS  PubMed  Google Scholar 

  • Britton RA, Powell BS, Dasgupta S, Sun Q, Margolin W, Lupski JR, Court DL (1998b) Cell cycle arrest in Era GTPase mutants: a potential growth rate-regulated checkpoint in Escherichia coli. Mol Microbiol 27:739-750

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Erickson HP (2005) Rapid in vitro assembly dynamics and subunit turnover of FtsZ demonstrated by fluorescence resonance energy transfer. J Biol Chem 280:22549-22554

    Article  CAS  PubMed  Google Scholar 

  • Cui Y, Petrushenko ZM, Rybenkov VV (2008) MukB acts as a macromolecular clamp in DNA condensation. Nat Struct Mol Biol 15:411-418

    Article  CAS  PubMed  Google Scholar 

  • Defeu Soufo HJ, Graumann PL (2003) Actin-like proteins MreB and Mbl from Bacillus subtilis are required for bipolar positioning of replication origins. Curr Biol 13:1916-1920

    Article  CAS  Google Scholar 

  • Defeu Soufo HJ, Graumann PL (2004) Dynamic movement of actin-like proteins within bacterial cells. EMBO Rep 5:789-794

    Article  CAS  PubMed  Google Scholar 

  • Defeu Soufo HJ, Graumann PL (2005) 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. BMC Cell Biol 6:10

    Article  PubMed  Google Scholar 

  • Doi M, Wachi M, Ishino F, Tomioka S, Ito M, Sakagami Y, Suzuki A, Matsuhashi M (1988) 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. J Bacteriol 170:4619-4624

    CAS  PubMed  Google Scholar 

  • Dworkin J, Losick R (2002) Does RNA polymerase help drive chromosome segregation in bacteria? Proc Natl Acad Sci USA 99:14089-14094

    Article  CAS  PubMed  Google Scholar 

  • Ebersbach G, Gerdes K (2004) Bacterial mitosis: partitioning protein ParA oscillates in spiral-shaped structures and positions plasmids at mid-cell. Mol Microbiol 52:385-398

    Article  CAS  PubMed  Google Scholar 

  • Ebersbach G, Ringgaard S, Moller-Jensen J, Wang Q, Sherratt DJ, Gerdes K (2006) Regular cellular distribution of plasmids by oscillating and filament-forming ParA ATPase of plasmid pB171. Mol Microbiol 61:1428-1442

    Article  CAS  PubMed  Google Scholar 

  • Espeli O, Nurse P, Levine C, Lee C, Marians KJ (2003) SetB: an integral membrane protein that affects chromosome segregation in Escherichia coli. Mol Microbiol 50:495-509

    Article  CAS  PubMed  Google Scholar 

  • Fogel MA, Waldor MK (2005) Distinct segregation dynamics of the two Vibrio cholerae chromosomes. Mol Microbiol 55:125-136

    Article  CAS  PubMed  Google Scholar 

  • Fogel MA, Waldor MK (2006) A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes Dev 20:3269-3282

    Article  CAS  PubMed  Google Scholar 

  • Fossum S, Crooke E, Skarstad K (2007) Organization of sister origins and replisomes during multifork DNA replication in Escherichia coli. EMBO J 26:4514-4522

    Article  CAS  PubMed  Google Scholar 

  • Gerdes K, Moller-Jensen J, Ebersbach G, Kruse T, Nordstrom K (2004) Bacterial mitotic machineries. Cell 116:359-366

    Article  CAS  PubMed  Google Scholar 

  • Gitai Z, Dye NA, Reisenauer A, Wachi M, Shapiro L (2005) MreB actin-mediated segregation of a specific region of a bacterial chromosome. Cell 120:329-341

    Article  CAS  PubMed  Google Scholar 

  • Gordon S, Sitnikov D, Webb CD, Teleman A, Losick R, Murray AW, Wright A (1997) Chromosome and low copy plasmid segregation in E. coli: visual evidence for distinct mechanisms. Cell 90:1113-1121

    Article  CAS  PubMed  Google Scholar 

  • Graumann PL (2000) Bacillus subtilis SMC is required for proper arrangement of the chromosome and for efficient segregation of replication termini but not for bipolar movement of newly duplicated origin regions. J Bacteriol 182:6463-6471

    Article  CAS  PubMed  Google Scholar 

  • Hirano T (2005) SMC proteins and chromosome mechanics: from bacteria to humans. Philos Trans R Soc Lond B Biol Sci 360:507-514

    Article  CAS  PubMed  Google Scholar 

  • Hu B, Yang G, Zhao W, Zhang Y, Zhao J (2007) MreB is important for cell shape but not for chromosome segregation of the filamentous cyanobacterium Anabaena sP PCC 7120. Mol Microbiol 63:1640-1652

    Article  CAS  PubMed  Google Scholar 

  • Jacob F, Brenner S, Cuzin F (1963) On the regulation of DNA replication in bacteria. Cold Spring Harbor Symp Quant Biol 28:329-348

    CAS  Google Scholar 

  • Jakimowicz D, Gust B, Zakrzewska-Czerwinska J, Chater KF (2005) Developmental-stage-specific assembly of ParB complexes in Streptomyces coelicolor hyphae. J Bacteriol 187:3572-3580

    Article  CAS  PubMed  Google Scholar 

  • Jensen SO, Thompson LS, Harry EJ (2005) Cell division in Bacillus subtilis: FtsZ and FtsA association is Z-ring independent, and FtsA is required for efficient midcell Z-Ring assembly. J Bacteriol 187:6536-6544

    Article  CAS  PubMed  Google Scholar 

  • Jones LJ, Carballido-Lopez R, Errington J (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104:913-922

    Article  CAS  PubMed  Google Scholar 

  • Kato J, Nishimura Y, Imamura R, Niki H, Hiraga S, Suzuki H (1990) New topoisomerase essential for chromosome segregation in E coli. Cell 63:393-404

    Article  CAS  PubMed  Google Scholar 

  • Kim HJ, Calcutt MJ, Schmidt FJ, Chater KF (2000) Partitioning of the linear chromosome during sporulation of Streptomyces coelicolor A3(2) involves an oriC-linked parAB locus. J Bacteriol 182:1313-1320

    Article  CAS  PubMed  Google Scholar 

  • Kireeva N, Lakonishok M, Kireev I, Hirano T, Belmont AS (2004) Visualization of early chromosome condensation: a hierarchical folding, axial glue model of chromosome structure. J Cell Biol 166:775-785

    Google Scholar 

  • Köhler P, Marahiel MA (1997) Association of the histone-like protein HBsu with the nucleoid of Bacillus subtilis. J Bacteriol 179:2060-2064

    PubMed  Google Scholar 

  • Kruse T, Moller-Jensen J, Lobner-Olesen A, Gerdes K (2003) Dysfunctional MreB inhibits chromosome segregation in Escherichia coli. EMBO J 22:5283-5292

    Article  CAS  PubMed  Google Scholar 

  • Kruse T, Blagoev B, Lobner-Olesen A, Wachi M, Sasaki K, Iwai N, Mann M, Gerdes K (2006) Actin homolog MreB and RNA polymerase interact and are both required for chromosome segregation in Escherichia coli. Genes Dev 20:113-124

    Article  CAS  PubMed  Google Scholar 

  • Kuempel PL, Henson JM, Dircks L, Tecklenburg M, Lim DF (1991) dif, a recA-independent recombination site in the terminus region of the chromosome of Escherichia coli. New Biol 3:799-811

    CAS  PubMed  Google Scholar 

  • Lemon KP, Grossman AD (1998) Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science 282:1516-1519

    Article  CAS  PubMed  Google Scholar 

  • Lindow JC, Britton RA, Grossman AD (2002a) Structural maintenance of chromosomes protein of Bacillus subtilis affects supercoiling in vivo. J Bacteriol 184:5317-5322

    Article  CAS  PubMed  Google Scholar 

  • Lindow JC, Kuwano M, Moriya S, Grossman AD (2002b) Subcellular localization of the Bacillus subtilis structural maintenance of chromosomes (SMC) protein. Mol Microbiol 46:997-1009

    Article  CAS  PubMed  Google Scholar 

  • Margolin W (2005) FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol 6:862-871

    Article  CAS  PubMed  Google Scholar 

  • Mascarenhas J, Soppa J, Strunnikov A, Graumann PL (2002a) Cell cycle dependent localization of two novel prokaryotic chromosome segregation and condensation proteins in Bacillus subtilis that interact with SMC protein. EMBO J 21:3108-3118

    Article  CAS  PubMed  Google Scholar 

  • Mascarenhas J, Soppa J, Strunnikov AV, Graumann PL (2002b) Cell cycle-dependent localization of two novel prokaryotic chromosome segregation and condensation proteins in Bacillus subtilis that interact with SMC protein. EMBO J 21:3108-3118

    Article  CAS  PubMed  Google Scholar 

  • Mascarenhas J, Volkov AV, Rinn C, Schiener J, Guckenberger R, Graumann PL (2005) Dynamic assembly, localization and proteolysis of the Bacillus subtilis SMC complex. BMC Cell Biol 6:28

    Article  PubMed  Google Scholar 

  • Mendell JE, Clements KD, Choat JH, Angert ER (2008) Extreme polyploidy in a large bacterium. Proc Natl Acad Sci USA 105:6730-6734

    Article  CAS  PubMed  Google Scholar 

  • Niki H, Imamura R, Kitaoka M, Yamanaka K, Ogura T, Hiraga S (1992) E coli MukB protein involved in chromosome partition forms a homodimer with a rod-and-hinge structure having DNA binding and ATP/GTP binding activities. EMBO J 11:5101-5109

    CAS  PubMed  Google Scholar 

  • Niki H, Yamaichi Y, Hiraga S (2000) Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev 14:212-223

    CAS  PubMed  Google Scholar 

  • Ohsumi K, Yamazoe M, Hiraga S (2001) Different localization of SeqA-bound nascent DNA clusters and MukF-MukE- MukB complex in Escherichia coli cells. Mol Microbiol 40:835-845

    Article  CAS  PubMed  Google Scholar 

  • Peters PC, Migocki MD, Thoni C, Harry EJ (2007) A new assembly pathway for the cytokinetic Z ring from a dynamic helical structure in vegetatively growing cells of Bacillus subtilis. Mol Microbiol 64:487-499

    Article  CAS  PubMed  Google Scholar 

  • Petrushenko ZM, Lai CH, Rybenkov VV (2006) Antagonistic interactions of kleisins and DNA with bacterial Condensin MukB. J Biol Chem 281:34208-34217

    Article  CAS  PubMed  Google Scholar 

  • Postow L, Hardy CD, Arsuaga J, Cozzarelli NR (2004) Topological domain structure of the Escherichia coli chromosome. Genes Dev 18:1766-1779

    Article  CAS  PubMed  Google Scholar 

  • Reyes-Lamothe R, Possoz C, Danilova O, Sherratt DJ (2008) Independent positioning and action of Escherichia coli replisomes in live cells. Cell 133:90-102

    Article  CAS  PubMed  Google Scholar 

  • Sawitzke J, Austin S (2001) An analysis of the factory model for chromosome replication and segregation in bacteria. Mol Microbiol 40:786-794

    Article  CAS  PubMed  Google Scholar 

  • Schneider D, Fuhrmann E, Scholz I, Hess WR, Graumann PL (2007) Fluorescence staining of live cyanobacterial cells suggest non-stringent chromosome segregation and absence of a connection between cytoplasmic and thylakoid membranes. BMC Cell Biol 8:39

    Article  PubMed  Google Scholar 

  • Srivastava P, Demarre G, Karpova TS, McNally J, Chattoraj DK (2007) Changes in nucleoid morphology and origin localization upon inhibition or alteration of the actin homolog, MreB, of Vibrio cholerae. J Bacteriol 189:7450-7463

    Article  CAS  PubMed  Google Scholar 

  • Staczek P, Higgins NP (1998) Gyrase and Topo IV modulate chromosome domain size in vivo. Mol Microbiol 29:1435-1448

    Article  CAS  PubMed  Google Scholar 

  • Stone MD, Bryant Z, Crisona NJ, Smith SB, Vologodskii A, Bustamante C, Cozzarelli NR (2003) Chirality sensing by Escherichia coli topoisomerase IV and the mechanism of type II topoisomerases. Proc Natl Acad Sci USA 100:8654-8659

    Article  CAS  PubMed  Google Scholar 

  • Sunako Y, Onogi T, Hiraga S (2001) Sister chromosome cohesion of Escherichia coli. Mol Microbiol 42:1233-1242

    Article  CAS  PubMed  Google Scholar 

  • Tadesse S, Graumann PL (2006) Differential and dynamic localization of topoisomerases in Bacillus subtilis. J Bacteriol 188:3002-3011

    Article  CAS  PubMed  Google Scholar 

  • Tadesse S, Mascarenhas J, Kosters B, Hasilik A, Graumann PL (2005) Genetic interaction of the SMC complex with topoisomerase IV in Bacillus subtilis. Microbiology 151:3729-3737

    Article  CAS  PubMed  Google Scholar 

  • Teleman AA, Graumann PL, Lin DCH, Grossman AD, Losick R (1998) Chromosome arrangement within a bacterium. Curr Biol 8:1102-1109

    Article  CAS  PubMed  Google Scholar 

  • Viollier PH, Thanbichler M, McGrath PT, West L, Meewan M, McAdams HH, Shapiro L (2004) Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proc Natl Acad Sci USA 101:9257-9262

    Article  CAS  PubMed  Google Scholar 

  • Volkov AV, Mascarenhas J, Andrei-Selmer C, Ulrich HD, Grauman PL (2003) A prokaryotic condensin/cohesin-like complex can actively compact chromosomes from a single position on the nucleoid. Mol Cell Biol 23:5638-5650

    Google Scholar 

  • Wang JC, (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 3:430-440

    Google Scholar 

  • Webb CD, Teleman A, Gordon S, Straight A, Belmont A, Lin DC-H, Grossman AD, Wright A, Losick R (1997) Bipolar localization of the replication origin regions of chromosomes in vegetative and sporulating cells of B. subtilis. Cell 88:667-674

    Article  CAS  PubMed  Google Scholar 

  • Webb CD, Graumann PL, Kahana J, Teleman AA, Silver P, Losick R (1998) Use of time-lapse microscopy to visualize rapid movement of the replication origin region of the chromosome during the cell cycle in Bacillus subtilis. Mol Microbiol 28:883-892

    Article  CAS  PubMed  Google Scholar 

  • Weitao T, Dasgupta S, Nordstrom K (2000) Role of the mukB gene in chromosome and plasmid partition in Escherichia coli. Mol Microbiol 38:392-400

    Article  CAS  PubMed  Google Scholar 

  • Woldringh CL, Nanninga N (2006) Structural and physical aspects of bacterial chromosome segregation. J Struct Biol 156:273-283

    Article  CAS  PubMed  Google Scholar 

  • Wu LJ, Errington J (2004) Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117:915-925

    Article  CAS  PubMed  Google Scholar 

  • Yamazoe M, Onogi T, Sunako Y, Niki H, Yamanaka K, Ichimura T, Hiraga S (1999) Complex formation of MukB, MukE and MukF proteins involved in chromosome partitioning in Escherichia coli. EMBO J 18:5873-5884

    Article  CAS  PubMed  Google Scholar 

  • Yang MC, Losick R (2001) Cytological evidence for association of the ends of the linear chromosome in Streptomyces coelicolor. J Bacteriol 183:5180-5186

    Article  CAS  PubMed  Google Scholar 

  • Zechiedrich EL, Khodursky AB, Cozzarelli NR (1997) Topoisomerase IV, not gyrase, decatenates products of site-specific recombination in Escherichia coli. Genes Dev 11:2580-2592

    Article  CAS  PubMed  Google Scholar 

  • Zechiedrich EL, Khodursky AB, Bachellier S, Schneider R, Chen D, Lilley DM, Cozzarelli NR (2000) Roles of topoisomerases in maintaining steady-state DNA supercoiling in Escherichia coli. J Biol Chem 275:8103-8113

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Work in my laboratory is supported by the University of Freiburg and the Deutsche Forschungsgemeinschaft.

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Correspondence to Peter L. Graumann .

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Graumann, P.L. (2010). The Chromosome Segregation Machinery in Bacteria. In: Dame, R.T., Dorman, C.J. (eds) Bacterial Chromatin. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3473-1_3

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