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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Angert ER, Clements KD (2004) Initiation of intracellular offspring in Epulopiscium. Mol Microbiol 51:827-835
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
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
Barilla D, Rosenberg MF, Nobbmann U, Hayes F (2005) Bacterial DNA segregation dynamics mediated by the polymerizing protein ParF. EMBO J 24:1453-1464
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
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
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
Breuert S, Allers T, Spohn G, Soppa J (2006) Regulated polyploidy in halophilic archaea. PLoS ONE 1:e92
Britton RA, Lin DC-H, Grossman AD (1998a) Characterization of a prokaryotic SMC protein involved in chromosome partitioning. Genes Dev 12:1254-1259
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
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
Cui Y, Petrushenko ZM, Rybenkov VV (2008) MukB acts as a macromolecular clamp in DNA condensation. Nat Struct Mol Biol 15:411-418
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
Defeu Soufo HJ, Graumann PL (2004) Dynamic movement of actin-like proteins within bacterial cells. EMBO Rep 5:789-794
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
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
Dworkin J, Losick R (2002) Does RNA polymerase help drive chromosome segregation in bacteria? Proc Natl Acad Sci USA 99:14089-14094
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
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
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
Fogel MA, Waldor MK (2005) Distinct segregation dynamics of the two Vibrio cholerae chromosomes. Mol Microbiol 55:125-136
Fogel MA, Waldor MK (2006) A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes Dev 20:3269-3282
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
Gerdes K, Moller-Jensen J, Ebersbach G, Kruse T, Nordstrom K (2004) Bacterial mitotic machineries. Cell 116:359-366
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
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
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
Hirano T (2005) SMC proteins and chromosome mechanics: from bacteria to humans. Philos Trans R Soc Lond B Biol Sci 360:507-514
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
Jacob F, Brenner S, Cuzin F (1963) On the regulation of DNA replication in bacteria. Cold Spring Harbor Symp Quant Biol 28:329-348
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
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
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
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
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
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
Köhler P, Marahiel MA (1997) Association of the histone-like protein HBsu with the nucleoid of Bacillus subtilis. J Bacteriol 179:2060-2064
Kruse T, Moller-Jensen J, Lobner-Olesen A, Gerdes K (2003) Dysfunctional MreB inhibits chromosome segregation in Escherichia coli. EMBO J 22:5283-5292
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
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
Lemon KP, Grossman AD (1998) Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science 282:1516-1519
Lindow JC, Britton RA, Grossman AD (2002a) Structural maintenance of chromosomes protein of Bacillus subtilis affects supercoiling in vivo. J Bacteriol 184:5317-5322
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
Margolin W (2005) FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol 6:862-871
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
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
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
Mendell JE, Clements KD, Choat JH, Angert ER (2008) Extreme polyploidy in a large bacterium. Proc Natl Acad Sci USA 105:6730-6734
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
Niki H, Yamaichi Y, Hiraga S (2000) Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev 14:212-223
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
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
Petrushenko ZM, Lai CH, Rybenkov VV (2006) Antagonistic interactions of kleisins and DNA with bacterial Condensin MukB. J Biol Chem 281:34208-34217
Postow L, Hardy CD, Arsuaga J, Cozzarelli NR (2004) Topological domain structure of the Escherichia coli chromosome. Genes Dev 18:1766-1779
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
Sawitzke J, Austin S (2001) An analysis of the factory model for chromosome replication and segregation in bacteria. Mol Microbiol 40:786-794
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
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
Staczek P, Higgins NP (1998) Gyrase and Topo IV modulate chromosome domain size in vivo. Mol Microbiol 29:1435-1448
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
Sunako Y, Onogi T, Hiraga S (2001) Sister chromosome cohesion of Escherichia coli. Mol Microbiol 42:1233-1242
Tadesse S, Graumann PL (2006) Differential and dynamic localization of topoisomerases in Bacillus subtilis. J Bacteriol 188:3002-3011
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
Teleman AA, Graumann PL, Lin DCH, Grossman AD, Losick R (1998) Chromosome arrangement within a bacterium. Curr Biol 8:1102-1109
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
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
Wang JC, (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 3:430-440
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
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
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
Woldringh CL, Nanninga N (2006) Structural and physical aspects of bacterial chromosome segregation. J Struct Biol 156:273-283
Wu LJ, Errington J (2004) Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117:915-925
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
Yang MC, Losick R (2001) Cytological evidence for association of the ends of the linear chromosome in Streptomyces coelicolor. J Bacteriol 183:5180-5186
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
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
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Work in my laboratory is supported by the University of Freiburg and the Deutsche Forschungsgemeinschaft.
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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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DOI: https://doi.org/10.1007/978-90-481-3473-1_3
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