1932

Abstract

If fully stretched out, a typical bacterial chromosome would be nearly 1 mm long, approximately 1,000 times the length of a cell. Not only must cells massively compact their genetic material, but they must also organize their DNA in a manner that is compatible with a range of cellular processes, including DNA replication, DNA repair, homologous recombination, and horizontal gene transfer. Recent work, driven in part by technological advances, has begun to reveal the general principles of chromosome organization in bacteria. Here, drawing on studies of many different organisms, we review the emerging picture of how bacterial chromosomes are structured at multiple length scales, highlighting the functions of various DNA-binding proteins and the impact of physical forces. Additionally, we discuss the spatial dynamics of chromosomes, particularly during their segregation to daughter cells. Although there has been tremendous progress, we also highlight gaps that remain in understanding chromosome organization and segregation.

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2015-11-13
2024-04-15
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Literature Cited

  1. Adams D, Shekhtman E, Zechiedrich E, Schmid M, Cozzarelli N. 1992. The role of topoisomerase-IV in partitioning bacterial replicons and the structure of catenated intermediates in DNA replication. Cell 71:2277–88 [Google Scholar]
  2. Adams DW, Wu LJ, Errington J. 2015. Nucleoid occlusion protein Noc recruits DNA to the bacterial cell membrane. EMBO J. 34:4491–501 [Google Scholar]
  3. Auner H, Buckle M, Deufel A, Kutateladze T, Lazarus L. et al. 2003. Mechanism of transcriptional activation by FIS: role of core promoter structure and DNA topology. J. Mol. Biol. 331:2331–44 [Google Scholar]
  4. Austin SJ, Mural RJ, Chattoraj DK, Abeles AL. 1985. Trans- and cis-acting elements for the replication of P1 miniplasmids. J. Mol. Biol. 183:2195–202 [Google Scholar]
  5. Azam TA, Hiraga S, Ishihama A. 2000. Two types of localization of the DNA-binding proteins within the Escherichia coli nucleoid. Genes Cells 5:8613–26 [Google Scholar]
  6. Azam TA, Iwata A, Nishimura A, Ueda S, Ishihama A. 1999. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol. 181:206361–70 [Google Scholar]
  7. Bakshi S, Siryaporn A, Goulian M, Weisshaar JC. 2012. Superresolution imaging of ribosomes and RNA polymerase in live Escherichia coli cells. Mol. Microbiol. 85:121–38 [Google Scholar]
  8. 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 121:6899–911 [Google Scholar]
  9. Bensaid A, Almeida A, Drlica K, Rouviere-Yaniv J. 1996. Cross-talk between topoisomerase I and HU in Escherichia coli. J. Mol. Biol. 256:2292–300 [Google Scholar]
  10. Ben-Yehuda S, Fujita M, Liu XS, Gorbatyuk B, Skoko D. et al. 2005. Defining a centromere-like element in Bacillus subtilis by identifying the binding sites for the chromosome-anchoring protein RacA. Mol. Cell 17:6773–82 [Google Scholar]
  11. Ben-Yehuda S, Rudner DZ, Losick R. 2003. RacA, a bacterial protein that anchors chromosomes to the cell poles. Science 299:5606532–36 [Google Scholar]
  12. Berlatzky IA, Rouvinski A, Ben-Yehuda S. 2008. Spatial organization of a replicating bacterial chromosome. PNAS 105:3714136–40 [Google Scholar]
  13. Bernhardt TG, de Boer PAJ. 2005. SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol. Cell 18:5555–64 [Google Scholar]
  14. Bigot S, Saleh OA, Lesterlin C, Pages C, El Karoui M. et al. 2005. KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J. 24:213770–80 [Google Scholar]
  15. Bigot S, Sivanathan V, Possoz C, Barre F-X, Cornet F. 2007. FtsK, a literate chromosome segregation machine. Mol. Microbiol. 64:61434–41 [Google Scholar]
  16. Bowman GR, Comolli LR, Zhu J, Eckart M, Koenig M. et al. 2008. A polymeric protein anchors the chromosomal origin/ParB complex at a bacterial cell pole. Cell 134:6945–55 [Google Scholar]
  17. Britton RA, Lin DC, Grossman AD. 1998. Characterization of a prokaryotic SMC protein involved in chromosome partitioning. Genes Dev. 12:91254–59 [Google Scholar]
  18. Butan C, Hartnell LM, Fenton AK, Bliss D, Sockett RE. et al. 2011. Spiral architecture of the nucleoid in Bdellovibrio bacteriovorus. J. Bacteriol. 193:61341–50 [Google Scholar]
  19. Chaconas G, Kobryn K. 2010. Structure, function, and evolution of linear replicons in Borrelia. Annu. Rev. Microbiol. 64:1185–202 [Google Scholar]
  20. Chen S, Calvo JM. 2002. Leucine-induced dissociation of Escherichia coli Lrp hexadecamers to octamers. J. Mol. Biol. 318:41031–42 [Google Scholar]
  21. Claret L, Rouviere-Yaniv J. 1997. Variation in HU composition during growth of Escherichia coli: the heterodimer is required for long term survival. J. Mol. Biol. 273:193–104 [Google Scholar]
  22. Dame RT, Noom MC, Wuite GJL. 2006. Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature 444:7117387–90 [Google Scholar]
  23. Dame RT, Wyman C, Goosen N. 2000. H-NS mediated compaction of DNA visualised by atomic force microscopy. Nucleic Acids Res. 28:183504–10 [Google Scholar]
  24. Danilova O, Reyes-Lamothe R, Pinskaya M, Sherratt D, Possoz C. 2007. MukB colocalizes with the oriC region and is required for organization of the two Escherichia coli chromosome arms into separate cell halves. Mol. Microbiol. 65:61485–92 [Google Scholar]
  25. De Vries R. 2010. DNA condensation in bacteria: Interplay between macromolecular crowding and nucleoid proteins. Biochimie 92:121715–21 [Google Scholar]
  26. Dillon SC, Dorman CJ. 2010. Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat. Rev. Microbiol. 8:3185–95 [Google Scholar]
  27. Di Ventura B, Knecht B, Andreas H, Godinez WJ, Fritsche M. et al. 2013. Chromosome segregation by the Escherichia coli Min system. Mol. Syst. Biol. 9:686 [Google Scholar]
  28. Dupaigne P, Tonthat NK, Espéli O, Whitfill T, Boccard F, Schumacher MA. 2012. Molecular basis for a protein-mediated DNA-bridging mechanism that functions in condensation of the E. coli chromosome. Mol. Cell 48:4560–71 [Google Scholar]
  29. Dyson P. 2011. Streptomyces: Molecular Biology and Biotechnology Poole, UK: Horiz. Sci. Press
  30. Easter J, Gober JW. 2002. ParB-stimulated nucleotide exchange regulates a switch in functionally distinct ParA activities. Mol. Cell 10:2427–34 [Google Scholar]
  31. Ebersbach G, Briegel A, Jensen GJ, Jacobs-Wagner C. 2008. A self-associating protein critical for chromosome attachment, division, and polar organization in Caulobacter. Cell 134:6956–68 [Google Scholar]
  32. Ebersbach G, Ringgaard S, Møller-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. 61:61428–42 [Google Scholar]
  33. Espeli O, Levine C, Hassing H, Marians KJ. 2003. Temporal regulation of topoisomerase IV activity in E. coli. Mol. Cell 11:1189–201 [Google Scholar]
  34. Espeli O, Mercier R, Boccard F. 2008. DNA dynamics vary according to macrodomain topography in the E. coli chromosome. Mol. Microbiol. 68:61418–27 [Google Scholar]
  35. Fekete RA, Chattoraj DK. 2005. A cis-acting sequence involved in chromosome segregation in Escherichia coli. Mol. Microbiol. 55:1175–83 [Google Scholar]
  36. Fiebig A, Keren K, Theriot JA. 2006. Fine-scale time-lapse analysis of the biphasic, dynamic behaviour of the two Vibrio cholerae chromosomes. Mol. Microbiol. 60:51164–78 [Google Scholar]
  37. Fisher JK, Bourniquel A, Witz G, Weiner B, Prentiss M, Kleckner N. 2013. Four-dimensional imaging of E. coli nucleoid organization and dynamics in living cells. Cell 153:4882–95 [Google Scholar]
  38. Flärdh K, Buttner MJ. 2009. Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat. Rev. Microbiol. 7:136–49 [Google Scholar]
  39. Fogel MA, Waldor MK. 2006. A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes Dev. 20:233269–82 [Google Scholar]
  40. Frenkiel-Krispin D, Minsky A. 2006. Nucleoid organization and the maintenance of DNA integrity in E. coli, B. subtilis and D. radiodurans. J. Struct. Biol. 156:2311–19 [Google Scholar]
  41. Frenkiel-Krispin D, Sack R, Englander J, Shimoni E, Eisenstein M. et al. 2004. Structure of the DNA-SspC complex: implications for DNA packaging, protection, and repair in bacterial spores. J. Bacteriol. 186:113525–30 [Google Scholar]
  42. Gerdes K, Howard M, Szardenings F. 2010. Pushing and pulling in prokaryotic DNA segregation. Cell 141:6927–42 [Google Scholar]
  43. Graham TGW, Wang X, Song D, Etson CM, van Oijen AM. et al. 2014. ParB spreading requires DNA bridging. Genes Dev. 28:111228–38 [Google Scholar]
  44. Grainge I, Bregu M, Vazquez M, Sivanathan V, Ip SC, Sherratt DJ. 2007. Unlinking chromosome catenanes in vivo by site-specific recombination. EMBO J. 26:194228–38 [Google Scholar]
  45. Grainger DC, Hurd D, Goldberg MD, Busby SJW. 2006. Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res. 34:164642–52 [Google Scholar]
  46. Grainger DC, Hurd D, Harrison M, Holdstock J, Busby SJW. 2005. Studies of the distribution of Escherichia coli cAMP-receptor protein and RNA polymerase along the E. coli chromosome. PNAS 102:4917693–98 [Google Scholar]
  47. Gruber S, Errington J. 2009. Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 137:4685–96 [Google Scholar]
  48. Gruber S, Veening J-W, Bach J, Blettinger M, Bramkamp M, Errington J. 2014. Interlinked sister chromosomes arise in the absence of condensin during fast replication in B. subtilis. Curr. Biol. 24:3293–98 [Google Scholar]
  49. Guo F, Adhya S. 2007. Spiral structure of Escherichia coli HUαβ provides foundation for DNA supercoiling. PNAS 104:114309–14 [Google Scholar]
  50. Gupta M, Sajid A, Sharma K, Ghosh S, Arora G. et al. 2014. HupB, a nucleoid-associated protein of Mycobacterium tuberculosis, is modified by serine/threonine protein kinases in vivo. J. Bacteriol. 196:142646–57 [Google Scholar]
  51. Hadizadeh Yazdi N, Guet CC, Johnson RC, Marko JF. 2012. Variation of the folding and dynamics of the Escherichia coli chromosome with growth conditions. Mol. Microbiol. 86:61318–33 [Google Scholar]
  52. Hardy CD, Cozzarelli NR. 2005. A genetic selection for supercoiling mutants of Escherichia coli reveals proteins implicated in chromosome structure. Mol. Microbiol. 57:61636–52 [Google Scholar]
  53. Harms A, Treuner-Lange A, Schumacher D, Sogaard-Andersen L. 2013. Tracking of chromosome and replisome dynamics in Myxococcus xanthus reveals a novel chromosome arrangement. PLOS Genet. 9:9e1003802 [Google Scholar]
  54. Hayama R, Marians KJ. 2010. Physical and functional interaction between the condensin MukB and the decatenase topoisomerase IV in Escherichia coli. PNAS 107:4418826–31 [Google Scholar]
  55. Higgins CF, Dorman CJ, Stirling DA, Waddell L, Booth IR. et al. 1988. A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell 52:4569–84 [Google Scholar]
  56. Higgins NP, Yang X, Fu Q, Roth JR. 1996. Surveying a supercoil domain by using the gamma delta resolution system in Salmonella typhimurium. J. Bacteriol. 178:102825–35 [Google Scholar]
  57. Hong SH, McAdams HH. 2011. Compaction and transport properties of newly replicated Caulobacter crescentus DNA. Mol. Microbiol. 82:61349–58 [Google Scholar]
  58. Huisman O, Faelen M, Girard D, Jaffé A, Toussaint A, Rouvière-Yaniv J. 1989. Multiple defects in Escherichia coli mutants lacking HU protein. J. Bacteriol. 171:73704–12 [Google Scholar]
  59. Hwang LC, Vecchiarelli AG, Han Y-W, Mizuuchi M, Harada Y. et al. 2013. ParA-mediated plasmid partition driven by protein pattern self-organization. EMBO J. 32:91238–49 [Google Scholar]
  60. Ireton K, Gunther NW, Grossman AD. 1994. spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis. J. Bacteriol. 176:175320–29 [Google Scholar]
  61. Jacob F, Brenner S, Cuzin F. 1963. On the regulation of DNA replication in bacteria. Cold Spring Harb. Symp. Quant. Biol. 28:329–48 [Google Scholar]
  62. Jain IH, Vijayan V, O'Shea EK. 2012. Spatial ordering of chromosomes enhances the fidelity of chromosome partitioning in cyanobacteria. PNAS 109:3413638–43 [Google Scholar]
  63. Jakimowicz D, Żydek P, Kois A, Zakrzewska-Czerwińska J, Chater KF. 2007. Alignment of multiple chromosomes along helical ParA scaffolding in sporulating Streptomyces hyphae. Mol. Microbiol. 65:3625–41 [Google Scholar]
  64. Javer A, Kuwada NJ, Long Z, Benza VG, Dorfman KD. et al. 2014. Persistent super-diffusive motion of Escherichia coli chromosomal loci. Nat. Commun. 5:3854 [Google Scholar]
  65. Jensen RB, Shapiro L. 1999. The Caulobacter crescentus smc gene is required for cell cycle progression and chromosome segregation. PNAS 96:1910661–66 [Google Scholar]
  66. Jensen RB, Wang SC, Shapiro L. 2001. A moving DNA replication factory in Caulobacter crescentus. EMBO J. 20:174952–63 [Google Scholar]
  67. Joshi MC, Bourniquel A, Fisher J, Ho BT, Magnan D. et al. 2011. Escherichia coli sister chromosome separation includes an abrupt global transition with concomitant release of late-splitting intersister snaps. PNAS 108:72765–70 [Google Scholar]
  68. Joshi MC, Magnan D, Montminy TP, Lies M, Stepankiw N, Bates D. 2013. Regulation of sister chromosome cohesion by the replication fork tracking protein SeqA. PLOS Genet. 9:8e1003673 [Google Scholar]
  69. Junier I, Boccard F, Espéli O. 2014. Polymer modeling of the E. coli genome reveals the involvement of locus positioning and macrodomain structuring for the control of chromosome conformation and segregation. Nucleic Acids Res. 42:31461–73 [Google Scholar]
  70. Jun S, Mulder B. 2006. Entropy-driven spatial organization of highly confined polymers: lessons for the bacterial chromosome. PNAS 103:3312388–93 [Google Scholar]
  71. Jun S, Wright A. 2010. Entropy as the driver of chromosome segregation. Nat. Rev. Microbiol. 8:8600–7 [Google Scholar]
  72. Kahramanoglou C, Seshasayee ASN, Prieto AI, Ibberson D, Schmidt S. et al. 2011. Direct and indirect effects of H-NS and Fis on global gene expression control in Escherichia coli. Nucleic Acids Res. 39:62073–91 [Google Scholar]
  73. Kaidow A, Wachi M, Nakamura J, Magae J, Nagai K. 1995. Anucleate cell production by Escherichia coli Δhns mutant lacking a histone-like protein, H-NS. J. Bacteriol. 177:123589–92 [Google Scholar]
  74. Kar S, Edgar R, Adhya S. 2005. Nucleoid remodeling by an altered HU protein: reorganization of the transcription program. PNAS 102:4516397–402 [Google Scholar]
  75. Kavenoff R, Ryder OA. 1976. Electron microscopy of membrane-associated folded chromosomes of Escherichia coli. Chromosoma 55:113–25 [Google Scholar]
  76. Kleckner N, Fisher JK, Stouf M, White MA, Bates D, Witz G. 2014. The bacterial nucleoid: nature, dynamics and sister segregation. Curr. Opin. Microbiol. 22:127–37 [Google Scholar]
  77. Laloux G, Jacobs-Wagner C. 2013. Spatiotemporal control of PopZ localization through cell cycle-coupled multimerization. J. Cell Biol. 201:6827–41 [Google Scholar]
  78. Le TB, Imakaev MV, Mirny LA, Laub MT. 2013. High-resolution mapping of the spatial organization of a bacterial chromosome. Science 342:6159731–34 [Google Scholar]
  79. Le TB, Laub MT. 2014. New approaches to understanding the spatial organization of bacterial genomes. Curr. Opin. Microbiol. 22:15–21 [Google Scholar]
  80. Lemon KP, Grossman AD. 1998. Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science 282:53931516–19 [Google Scholar]
  81. Lenarcic R, Halbedel S, Visser L, Shaw M, Wu LJ. et al. 2009. Localisation of DivIVA by targeting to negatively curved membranes. EMBO J. 28:152272–82 [Google Scholar]
  82. Leonard AC, Grimwade JE. 2005. Building a bacterial orisome: emergence of new regulatory features for replication origin unwinding. Mol. Microbiol. 55:4978–85 [Google Scholar]
  83. Leonard TA, Butler PJ, Löwe J. 2005. Bacterial chromosome segregation: structure and DNA binding of the Soj dimer—a conserved biological switch. EMBO J. 24:2270–82 [Google Scholar]
  84. Lesterlin C, Ball G, Schermelleh L, Sherratt DJ. 2014. RecA bundles mediate homology pairing between distant sisters during DNA break repair. Nature 506:7487249–53 [Google Scholar]
  85. Lesterlin C, Barre F-X, Cornet F. 2004. Genetic recombination and the cell cycle: what we have learned from chromosome dimers. Mol. Microbiol. 54:51151–60 [Google Scholar]
  86. Lesterlin C, Pages C, Dubarry N, Dasgupta S, Cornet F. 2008. Asymmetry of chromosome Replichores renders the DNA translocase activity of FtsK essential for cell division and cell shape maintenance in Escherichia coli. PLOS Genet. 4:12e1000288 [Google Scholar]
  87. Lewis PJ, Thaker SD, Errington J. 2000. Compartmentalization of transcription and translation in Bacillus subtilis. EMBO J. 19:4710–18 [Google Scholar]
  88. Li Y, Stewart NK, Berger AJ, Vos S, Schoeffler AJ. et al. 2010. Escherichia coli condensin MukB stimulates topoisomerase IV activity by a direct physical interaction. PNAS 107:4418832–37 [Google Scholar]
  89. Libby EA, Roggiani M, Goulian M. 2012. Membrane protein expression triggers chromosomal locus repositioning in bacteria. PNAS 109:197445–50 [Google Scholar]
  90. Lim HC, Surovtsev IV, Beltran BG, Huang F, Bewersdorf J, Jacobs-Wagner C. 2014. Evidence for a DNA-relay mechanism in ParABS-mediated chromosome segregation. eLife 3:e02758 [Google Scholar]
  91. Lin DC, Grossman AD. 1998. Identification and characterization of a bacterial chromosome partitioning site. Cell 92:5675–85 [Google Scholar]
  92. Livny J, Yamaichi Y, Waldor MK. 2007. Distribution of centromere-like parS sites in bacteria: insights from comparative genomics. J. Bacteriol. 189:238693–703 [Google Scholar]
  93. Löwe J, Ellonen A, Allen MD, Atkinson C, Sherratt DJ, Grainge I. 2008. Molecular mechanism of sequence-directed DNA loading and translocation by FtsK. Mol. Cell 31:4498–509 [Google Scholar]
  94. Lucchini S, Rowley G, Goldberg MD, Hurd D, Harrison M, Hinton JCD. 2006. H-NS mediates the silencing of laterally acquired genes in bacteria. PLOS Pathog. 2:8e81 [Google Scholar]
  95. Malik M, Bensaid A, Rouviere-Yaniv J, Drlica K. 1996. Histone-like protein HU and bacterial DNA topology: suppression of an HU deficiency by gyrase mutations. J. Mol. Biol. 256:166–76 [Google Scholar]
  96. Mera PE, Kalogeraki VS, Shapiro L. 2014. Replication initiator DnaA binds at the Caulobacter centromere and enables chromosome segregation. PNAS 111:4516100–5 [Google Scholar]
  97. Mercier R, Petit M-A, Schbath S, Robin S, El Karoui M. et al. 2008. The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 135:3475–85 [Google Scholar]
  98. Mohl DA, Easter J, Gober JW. 2001. The chromosome partitioning protein, ParB, is required for cytokinesis in Caulobacter crescentus. Mol. Microbiol. 42:3741–55 [Google Scholar]
  99. Mukherjee A, DiMario PJ, Grove A. 2009. Mycobacterium smegmatis histone-like protein Hlp is nucleoid associated. FEMS Microbiol. Lett. 291:2232–40 [Google Scholar]
  100. Mumm JP, Landy A, Gelles J. 2006. Viewing single lambda site-specific recombination events from start to finish. EMBO J. 25:194586–95 [Google Scholar]
  101. Murray H, Errington J. 2008. Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell 135:174–84 [Google Scholar]
  102. Murray H, Ferreira H, Errington J. 2006. The bacterial chromosome segregation protein Spo0J spreads along DNA from parS nucleation sites. Mol. Microbiol. 61:51352–61 [Google Scholar]
  103. Navarre WW, Porwollik S, Wang Y, McClelland M, Rosen H. et al. 2006. Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313:5784236–38 [Google Scholar]
  104. Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P. 2000. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64:3548–72 [Google Scholar]
  105. Nicolas E, Upton AL, Uphoff S, Henry O, Badrinarayanan A, Sherratt D. 2014. The SMC complex MukBEF recruits topoisomerase IV to the origin of replication region in live Escherichia coli. Mbio 5:1e01001–13 [Google Scholar]
  106. Nielsen HJ, Li Y, Youngren B, Hansen FG, Austin S. 2006a. Progressive segregation of the Escherichia coli chromosome. Mol. Microbiol. 61:2383–93 [Google Scholar]
  107. Nielsen HJ, Ottesen JR, Youngren B, Austin SJ, Hansen FG. 2006b. The Escherichia coli chromosome is organized with the left and right chromosome arms in separate cell halves. Mol. Microbiol. 62:2331–38 [Google Scholar]
  108. Niki H, Jaffé A, Imamura R, Ogura T, Hiraga S. 1991. The new gene mukB codes for a 177 kd protein with coiled-coil domains involved in chromosome partitioning of E. coli. EMBO J. 10:1183–93 [Google Scholar]
  109. Niki H, Yamaichi Y, Hiraga S. 2000. Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev. 14:2212–23 [Google Scholar]
  110. Nolivos S, Sherratt D. 2014. The bacterial chromosome: architecture and action of bacterial SMC and SMC-like complexes. FEMS Microbiol. Rev. 38:3380–92 [Google Scholar]
  111. Oliva MA, Halbedel S, Freund SM, Dutow P, Leonard TA. et al. 2010. Features critical for membrane binding revealed by DivIVA crystal structure. EMBO J. 29:121988–2001 [Google Scholar]
  112. Peter BJ, Ullsperger C, Hiasa H, Marians KJ, Cozzarelli NR. 1998. The structure of supercoiled intermediates in DNA replication. Cell 94:6819–27 [Google Scholar]
  113. Postow L, Hardy CD, Arsuaga J, Cozzarelli NR. 2004. Topological domain structure of the Escherichia coli chromosome. Genes Dev. 18:141766–79 [Google Scholar]
  114. Prieto AI, Kahramanoglou C, Ali RM, Fraser GM, Seshasayee ASN, Luscombe NM. 2012. Genomic analysis of DNA binding and gene regulation by homologous nucleoid-associated proteins IHF and HU in Escherichia coli K12. Nucleic Acids Res. 40:83524–37 [Google Scholar]
  115. Ptacin JL, Gahlmann A, Bowman GR, Perez AM, von Diezmann ARS. et al. 2014. Bacterial scaffold directs pole-specific centromere segregation. PNAS 111:19E2046–55 [Google Scholar]
  116. Ptacin JL, Lee SF, Garner EC, Toro E, Eckart M. et al. 2010. A spindle-like apparatus guides bacterial chromosome segregation. Nat. Cell Biol. 12:8791–98 [Google Scholar]
  117. Ramamurthi KS, Losick R. 2009. Negative membrane curvature as a cue for subcellular localization of a bacterial protein. PNAS 106:3213541–45 [Google Scholar]
  118. Reyes-Lamothe R, Possoz C, Danilova O, Sherratt DJ. 2008. Independent positioning and action of Escherichia coli replisomes in live cells. Cell 133:190–102 [Google Scholar]
  119. Rice PA, Yang S, Mizuuchi K, Nash HA. 1996. Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn. Cell 87:71295–306 [Google Scholar]
  120. Ringgaard S, van Zon J, Howard M, Gerdes K. 2009. Movement and equipositioning of plasmids by ParA filament disassembly. PNAS 106:4619369–74 [Google Scholar]
  121. Robinow C, Kellenberger E. 1994. The bacterial nucleoid revisited. Microbiol. Rev. 58:2211–32 [Google Scholar]
  122. Salerno P, Larsson J, Bucca G, Laing E, Smith CP, Flärdh K. 2009. One of the two genes encoding nucleoid-associated HU proteins in Streptomyces coelicolor is developmentally regulated and specifically involved in spore maturation. J. Bacteriol. 191:216489–500 [Google Scholar]
  123. Sánchez-Romero MA, Busby SJW, Dyer NP, Ott S, Millard AD, Grainger DC. 2010. Dynamic distribution of SeqA protein across the chromosome of Escherichia coli K-12. mBio 1:1e00012–10 [Google Scholar]
  124. Sawitzke JA, Austin S. 2000. Suppression of chromosome segregation defects of Escherichia coli muk mutants by mutations in topoisomerase I. PNAS 97:41671–76 [Google Scholar]
  125. Schneider R, Travers A, Kutateladze T, Muskhelishvili G. 1999. A DNA architectural protein couples cellular physiology and DNA topology in Escherichia coli. Mol. Microbiol. 34:5953–64 [Google Scholar]
  126. Schofield WB, Lim HC, Jacobs-Wagner C. 2010. Cell cycle coordination and regulation of bacterial chromosome segregation dynamics by polarly localized proteins. EMBO J. 29:183068–81 [Google Scholar]
  127. Scholefield G, Whiting R, Errington J, Murray H. 2011. Spo0J regulates the oligomeric state of Soj to trigger its switch from an activator to an inhibitor of DNA replication initiation. Mol. Microbiol. 79:41089–100 [Google Scholar]
  128. Schwartz MA, Shapiro L. 2011. An SMC ATPase mutant disrupts chromosome segregation in Caulobacter. Mol. Microbiol. 82:61359–74 [Google Scholar]
  129. Shebelut CW, Guberman JM, van Teeffelen S, Yakhnina AA, Gitai Z. 2010. Caulobacter chromosome segregation is an ordered multistep process. PNAS 107:3214194–98 [Google Scholar]
  130. Sinden RR, Pettijohn DE. 1981. Chromosomes in living Escherichia coli cells are segregated into domains of supercoiling. PNAS 78:1224–28 [Google Scholar]
  131. Singh SS, Singh N, Bonocora RP, Fitzgerald DM, Wade JT, Grainger DC. 2014. Widespread suppression of intragenic transcription initiation by H-NS. Genes Dev. 28:3214–19 [Google Scholar]
  132. Sivanathan V, Allen MD, de Bekker C, Baker R, Arciszewska LK. et al. 2006. The FtsK gamma domain directs oriented DNA translocation by interacting with KOPS. Nat. Struct. Mol. Biol. 13:11965–72 [Google Scholar]
  133. Smits WK, Grossman AD. 2010. The transcriptional regulator Rok binds A+T-rich DNA and is involved in repression of a mobile genetic element in Bacillus subtilis. PLOS Genet. 6:11e1001207 [Google Scholar]
  134. Steiner W, Liu G, Donachie WD, Kuempel P. 1999. The cytoplasmic domain of FtsK protein is required for resolution of chromosome dimers. Mol. Microbiol. 31:2579–83 [Google Scholar]
  135. Steiner WW, Kuempel PL. 1998. Sister chromatid exchange frequencies in Escherichia coli analyzed by recombination at the dif resolvase site. J. Bacteriol. 180:236269–75 [Google Scholar]
  136. Stein RA, Deng S, Higgins NP. 2005. Measuring chromosome dynamics on different time scales using resolvases with varying half-lives. Mol. Microbiol. 56:41049–61 [Google Scholar]
  137. Stella S, Cascio D, Johnson RC. 2010. The shape of the DNA minor groove directs binding by the DNA-bending protein Fis. Genes Dev. 24:8814–26 [Google Scholar]
  138. Sullivan NL, Marquis KA, Rudner DZ. 2009. Recruitment of SMC by ParB-parS organizes the origin region and promotes efficient chromosome segregation. Cell 137:4697–707 [Google Scholar]
  139. Swiercz JP, Nanji T, Gloyd M, Guarné A, Elliot MA. 2013. A novel nucleoid-associated protein specific to the actinobacteria. Nucleic Acids Res. 41:74171–84 [Google Scholar]
  140. Swinger KK, Lemberg KM, Zhang Y, Rice PA. 2003. Flexible DNA bending in HU-DNA cocrystal structures. EMBO J. 22:143749–60 [Google Scholar]
  141. Tadesse S, Mascarenhas J, Kösters B, Hasilik A, Graumann PL. 2005. Genetic interaction of the SMC complex with topoisomerase IV in Bacillus subtilis. Microbiology 151:113729–37 [Google Scholar]
  142. Thanbichler M, Shapiro L. 2006. MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126:1147–62 [Google Scholar]
  143. Thiel A, Valens M, Vallet-Gely I, Espéli O, Boccard F. 2012. Long-range chromosome organization in E. coli: a site-specific system isolates the Ter macrodomain. PLOS Genet. 8:4e1002672 [Google Scholar]
  144. Toro E, Hong S-H, McAdams HH, Shapiro L. 2008. Caulobacter requires a dedicated mechanism to initiate chromosome segregation. PNAS 105:4015435–40 [Google Scholar]
  145. Tsai HH, Huang CH, Tessmer I, Erie DA, Chen CW. 2011. Linear Streptomyces plasmids form superhelical circles through interactions between their terminal proteins. Nucleic Acids Res. 39:62165–74 [Google Scholar]
  146. Umbarger MA, Toro E, Wright MA, Porreca GJ, Bau D. et al. 2011. The three-dimensional architecture of a bacterial genome and its alteration by genetic perturbation. Mol. Cell 44:2252–64 [Google Scholar]
  147. Valens M, Penaud S, Rossignol M, Cornet F, Boccard F. 2004. Macrodomain organization of the Escherichia coli chromosome. EMBO J. 23:214330–41 [Google Scholar]
  148. Vallet-Gely I, Boccard F. 2013. Chromosomal organization and segregation in Pseudomonas aeruginosa. PLOS Genet. 9:5e1003492 [Google Scholar]
  149. Vecchiarelli AG, Han Y-W, Tan X, Mizuuchi M, Ghirlando R. et al. 2010. ATP control of dynamic P1 ParA-DNA interactions: a key role for the nucleoid in plasmid partition. Mol. Microbiol. 78:178–91 [Google Scholar]
  150. Vecchiarelli AG, Mizuuchi K, Funnell BE. 2012. Surfing biological surfaces: exploiting the nucleoid for partition and transport in bacteria. Mol. Microbiol. 86:3513–23 [Google Scholar]
  151. Vecchiarelli AG, Neuman KC, Mizuuchi K. 2014. A propagating ATPase gradient drives transport of surface-confined cellular cargo. PNAS 111:134880–85 [Google Scholar]
  152. Viollier PH, Thanbichler M, McGrath PT, West L, Meewan M. et al. 2004. Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. PNAS 101:259257–62 [Google Scholar]
  153. Vos SM, Tretter EM, Schmidt BH, Berger JM. 2011. All tangled up: how cells direct, manage and exploit topoisomerase function. Nat. Rev. Mol. Cell Biol. 12:12827–41 [Google Scholar]
  154. Wang W, Li GW, Chen C, Xie XS, Zhuang X. 2011. Chromosome organization by a nucleoid-associated protein in live bacteria. Science 333:60481445–49 [Google Scholar]
  155. Wang X, Liu X, Possoz C, Sherratt DJ. 2006. The two Escherichia coli chromosome arms locate to separate cell halves. Genes Dev. 20:131727–31 [Google Scholar]
  156. Wang X, Montero Llopis P, Rudner DZ. 2014a. Bacillus subtilis chromosome organization oscillates between two distinct patterns. PNAS 111:3512877–82 [Google Scholar]
  157. Wang X, Reyes-Lamothe R, Sherratt DJ. 2008. Modulation of Escherichia coli sister chromosome cohesion by topoisomerase IV. Genes Dev. 22:172426–33 [Google Scholar]
  158. Wang X, Rudner DZ. 2014. Spatial organization of bacterial chromosomes. Curr. Opin. Microbiol. 22:66–72 [Google Scholar]
  159. Wang X, Sherratt DJ. 2010. Independent segregation of the two arms of the Escherichia coli ori region requires neither RNA synthesis nor MreB dynamics. J. Bacteriol. 192:236143–53 [Google Scholar]
  160. Wang X, Tang OW, Riley EP, Rudner DZ. 2014b. The SMC condensin complex is required for origin segregation in Bacillus subtilis. Curr. Biol. 24:3287–92 [Google Scholar]
  161. Weber SC, Spakowitz AJ, Theriot JA. 2012. Nonthermal ATP-dependent fluctuations contribute to the in vivo motion of chromosomal loci. PNAS 109:197338–43 [Google Scholar]
  162. Weitao T, Nordström K, Dasgupta S. 1999. Mutual suppression of mukB and seqA phenotypes might arise from their opposing influences on the Escherichia coli nucleoid structure. Mol. Microbiol. 34:1157–68 [Google Scholar]
  163. Wiggins PA, Cheveralls KC, Martin JS, Lintner R, Kondev J. 2010. Strong intranucleoid interactions organize the Escherichia coli chromosome into a nucleoid filament. PNAS 107:114991–95 [Google Scholar]
  164. Wolf SG, Frenkiel D, Arad T, Finkel SE, Kolter R, Minsky A. 1999. DNA protection by stress-induced biocrystallization. Nature 400:673983–85 [Google Scholar]
  165. Wright MA, Kharchenko P, Church GM, Segrè D. 2007. Chromosomal periodicity of evolutionarily conserved gene pairs. PNAS 104:2510559–64 [Google Scholar]
  166. Wu LJ, Errington J. 1994. Bacillus subtilis SpoIIIE protein required for DNA segregation during asymmetric cell division. Science 264:5158572–75 [Google Scholar]
  167. Wu LJ, Errington J. 1998. Use of asymmetric cell division and spoIIIE mutants to probe chromosome orientation and organization in Bacillus subtilis. Mol. Microbiol. 27:4777–86 [Google Scholar]
  168. Wu LJ, Errington J. 2003. RacA and the Soj-Spo0J system combine to effect polar chromosome segregation in sporulating Bacillus subtilis. Mol. Microbiol. 49:61463–75 [Google Scholar]
  169. Wu LJ, Errington J. 2004. Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117:7915–25 [Google Scholar]
  170. Wu LJ, Ishikawa S, Kawai Y, Oshima T, Ogasawara N, Errington J. 2009. Noc protein binds to specific DNA sequences to coordinate cell division with chromosome segregation. EMBO J. 28:131940–52 [Google Scholar]
  171. Yamaichi Y, Bruckner R, Ringgaard S, Möll A, Cameron DE. et al. 2012. A multidomain hub anchors the chromosome segregation and chemotactic machinery to the bacterial pole. Genes Dev. 26:202348–60 [Google Scholar]
  172. Yamaichi Y, Niki H. 2004. migS, a cis-acting site that affects bipolar positioning of oriC on the Escherichia coli chromosome. EMBO J. 23:1221–33 [Google Scholar]
  173. Yang MC, Losick R. 2001. Cytological evidence for association of the ends of the linear chromosome in Streptomyces coelicolor. J. Bacteriol. 183:175180–86 [Google Scholar]
  174. Youngren B, Nielsen HJ, Jun S, Austin S. 2014. The multifork Escherichia coli chromosome is a self-duplicating and self-segregating thermodynamic ring polymer. Genes Dev. 28:171–84 [Google Scholar]
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