1932

Abstract

Since the nucleoid was isolated from bacteria in the 1970s, two fundamental questions emerged and are still in the spotlight: how bacteria organize their chromosomes to fit inside the cell and how nucleoid organization enables essential biological processes. During the last decades, knowledge of bacterial chromosome organization has advanced considerably, and today, such chromosomes are considered to be highly organized and dynamic structures that are shaped by multiple factors in a multiscale manner. Here we review not only the classical well-known factors involved in chromosome organization but also novel components that have recently been shown to dynamically shape the 3D structuring of the bacterial genome. We focus on the different functional elements that control short-range organization and describe how they collaborate in the establishment of the higher-order folding and disposition of the chromosome. Recent advances have opened new avenues for a deeper understanding of the principles and mechanisms of chromosome organization in bacteria.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-033021-113232
2021-10-08
2024-06-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/75/1/annurev-micro-033021-113232.html?itemId=/content/journals/10.1146/annurev-micro-033021-113232&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Ali Azam T, 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]
  2. 2. 
    Arias-Cartin R, Dobihal GS, Campos M, Surovtsev IV, Parry B, Jacobs-Wagner C. 2017. Replication fork passage drives asymmetric dynamics of a critical nucleoid-associated protein in Caulobacter. EMBO J 36:3301–18
    [Google Scholar]
  3. 3. 
    Arold ST, Leonard PG, Parkinson GN, Ladbury JE. 2010. H-NS forms a superhelical protein scaffold for DNA condensation. PNAS 107:3615728–32
    [Google Scholar]
  4. 4. 
    Badrinarayanan A, Le TB, Laub MT. 2015. Bacterial chromosome organization and segregation. Annu. Rev. Cell Dev. Biol. 31:171–99
    [Google Scholar]
  5. 5. 
    Badrinarayanan A, Reyes-Lamothe R, Uphoff S, Leake MC, Sherratt DJ. 2012. In vivo architecture and action of bacterial structural maintenance of chromosome proteins. Science 338:6106528–31
    [Google Scholar]
  6. 6. 
    Ball CA, Osuna R, Ferguson KC, Johnson RC. 1992. Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. J. Bacteriol. 174:248043–56
    [Google Scholar]
  7. 7. 
    Barre F-X, Søballe B, Michel B, Aroyo M, Robertson M, Sherratt D. 2001. Circles: the replication-recombination-chromosome segregation connection. PNAS 98:158189–95
    [Google Scholar]
  8. 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. 9. 
    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]
  10. 10. 
    Bettridge K, Verma S, Weng X, Adhya S, Xiao J 2020. Single-molecule tracking reveals that the nucleoid-associated protein HU plays a dual role in maintaining proper nucleoid volume through differential interactions with chromosomal DNA. Mol. Microbiol. 115:12–27
    [Google Scholar]
  11. 11. 
    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]
  12. 12. 
    Bliska JB, Cozzarelli NR. 1987. Use of site-specific recombination as a probe of DNA structure and metabolism in vivo. J Mol. Biol. 194:2205–18
    [Google Scholar]
  13. 13. 
    Böhm K, Giacomelli G, Schmidt A, Imhof A, Koszul R et al. 2020. Chromosome organization by a conserved condensin-ParB system in the actinobacterium Corynebacterium glutamicum. Nat. Commun. 11:11485
    [Google Scholar]
  14. 14. 
    Boudreau BA, Hron DR, Qin L, van der Valk RA, Kotlajich MV et al. 2018. StpA and Hha stimulate pausing by RNA polymerase by promoting DNA-DNA bridging of H-NS filaments. Nucleic Acids Res 46:115525–46
    [Google Scholar]
  15. 15. 
    Bouffartigues E, Buckle M, Badaut C, Travers A, Rimsky S 2007. H-NS cooperative binding to high-affinity sites in a regulatory element results in transcriptional silencing. Nat. Struct. Mol. Biol. 14:5441–48
    [Google Scholar]
  16. 16. 
    Brézellec P, Hoebeke M, Hiet MS, Pasek S, Ferat JL. 2006. DomainSieve: a protein domain–based screen that led to the identification of dam-associated genes with potential link to DNA maintenance. Bioinformatics 22:161935–41
    [Google Scholar]
  17. 17. 
    Buss J, Coltharp C, Shtengel G, Yang X, Hess H, Xiao J 2015. A multi-layered protein network stabilizes the Escherichia coli FtsZ-ring and modulates constriction dynamics. PLOS Genet 11:4e1005128
    [Google Scholar]
  18. 18. 
    Carabetta VJ. 2021. Addressing the possibility of a histone-like code in bacteria. J. Proteome Res. 20:27–37
    [Google Scholar]
  19. 19. 
    Cournac A, Marbouty M, Mozziconacci J, Koszul R. 2016. Generation and analysis of chromosomal contact maps of yeast species. Methods Mol. Biol. 1361:227–45
    [Google Scholar]
  20. 20. 
    Cournac A, Marie-Nelly H, Marbouty M, Koszul R, Mozziconacci J. 2012. Normalization of a chromosomal contact map. BMC Genom 13:436
    [Google Scholar]
  21. 21. 
    Dame RT, Rashid F-ZM, Grainger DC. 2020. Chromosome organization in bacteria: mechanistic insights into genome structure and function. Nat. Rev. Genet. 21:4227–42
    [Google Scholar]
  22. 22. 
    Dewachter L, Verstraeten N, Fauvart M, Michiels J. 2018. An integrative view of cell cycle control in Escherichia coli. FEMS Microbiol. Rev. 42:2116–36
    [Google Scholar]
  23. 23. 
    Dillon SC, Dorman CJ. 2010. Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat. Rev. Microbiol. 8:3185–95
    [Google Scholar]
  24. 24. 
    Dorman CJ. 2014. H-NS-like nucleoid-associated proteins, mobile genetic elements and horizontal gene transfer in bacteria. Plasmid 75:1–11
    [Google Scholar]
  25. 25. 
    Duigou S, Boccard F. 2017. Long range chromosome organization in Escherichia coli: The position of the replication origin defines the non-structured regions and the Right and Left macrodomains. PLOS Genet 13:5e1006758
    [Google Scholar]
  26. 26. 
    Dupaigne P, Tonthat NK, Espeli 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]
  27. 27. 
    El Karoui M, Biaudet V, Schbath S, Gruss A. 1999. Characteristics of Chi distribution on different bacterial genomes. Res. Microbiol. 150:9–10579–87
    [Google Scholar]
  28. 28. 
    Espeli O, Borne R, Dupaigne P, Thiel A, Gigant E et al. 2012. A MatP-divisome interaction coordinates chromosome segregation with cell division in E. coli. EMBO J 31:143198–211
    [Google Scholar]
  29. 29. 
    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]
  30. 30. 
    Espinosa E, Paly E, Barre F-X. 2020. High-resolution whole-genome analysis of sister-chromatid contacts. Mol. Cell 79:5857–69.e3
    [Google Scholar]
  31. 31. 
    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]
  32. 32. 
    Fitzgerald S, Kary SC, Alshabib EY, MacKenzie KD, Stoebel DM et al. 2020. Redefining the H-NS protein family: A diversity of specialized core and accessory forms exhibit hierarchical transcriptional network integration. Nucleic Acids Res 48:1810184–98
    [Google Scholar]
  33. 33. 
    Gao F. 2015. Bacteria may have multiple replication origins. Front. Microbiol. 6:324
    [Google Scholar]
  34. 34. 
    Gray WT, Govers SK, Xiang Y, Parry BR, Campos M et al. 2019. Nucleoid size scaling and intracellular organization of translation across bacteria. Cell 177:61632–48.e20
    [Google Scholar]
  35. 35. 
    Gruber S. 2018. SMC complexes sweeping through the chromosome: going with the flow and against the tide. Curr. Opin. Microbiol. 42:96–103
    [Google Scholar]
  36. 36. 
    Gruber S, Veening JW, 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]
  37. 37. 
    Guilhas B, Walter J-C, Rech J, David G, Walliser NO et al. 2020. ATP-driven separation of liquid phase condensates in bacteria. Mol. Cell 79:2293–303.e4
    [Google Scholar]
  38. 38. 
    Guo MS, Haakonsen DL, Zeng W, Schumacher MA, Laub MT. 2018. A bacterial chromosome structuring protein binds overtwisted DNA to stimulate type II topoisomerases and enable DNA replication. Cell 175:2583–97.e23
    [Google Scholar]
  39. 39. 
    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]
  40. 40. 
    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]
  41. 41. 
    Hassler M, Shaltiel IA, Haering CH. 2018. Towards a unified model of SMC complex function. Curr. Biol. 28:21R1266–81
    [Google Scholar]
  42. 42. 
    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]
  43. 43. 
    Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ et al. 2016. A new view of the tree of life. Nat. Microbiol. 1:16048
    [Google Scholar]
  44. 44. 
    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]
  45. 45. 
    Hyman AA, Weber CA, Jülicher F. 2014. Liquid-liquid phase separation in biology. Annu. Rev. Cell Dev. Biol. 30:39–58
    [Google Scholar]
  46. 46. 
    Imakaev M, Fudenberg G, McCord RP, Naumova N, Goloborodko A et al. 2012. Iterative correction of Hi-C data reveals hallmarks of chromosome organization. Nat. Methods 9:10999–1003
    [Google Scholar]
  47. 47. 
    Johnson RC, Bruist MF, Simon MI. 1986. Host protein requirements for in vitro site-specific DNA inversion. Cell 46:4531–39
    [Google Scholar]
  48. 48. 
    Joyeux M. 2015. Compaction of bacterial genomic DNA: clarifying the concepts. J. Phys. Condens. Matter. 27:38383001
    [Google Scholar]
  49. 49. 
    Jun S, Mulder B. 2006. Entropy-driven spatial organization of highly confined polymers: lessons for the bacterial chromosome. PNAS 103:3312388–93
    [Google Scholar]
  50. 50. 
    Junier I, Boccard F, Espeli 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]
  51. 51. 
    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]
  52. 52. 
    Kamar RI, Banigan EJ, Erbas A, Giuntoli RD, de la Cruz MO et al. 2017. Facilitated dissociation of transcription factors from single DNA binding sites. PNAS 114:16E3251–57
    [Google Scholar]
  53. 53. 
    Kavenoff R, Bowen BC. 1976. Electron microscopy of membrane-free folded chromosomes from Escherichia coli. Chromosoma 59:289–101
    [Google Scholar]
  54. 54. 
    Koch C, Kahmann R. 1986. Purification and properties of the Escherichia coli host factor required for inversion of the G segment in bacteriophage Mu. J. Biol. Chem. 261:3315673–78
    [Google Scholar]
  55. 55. 
    Kono N, Arakawa K, Tomita M. 2011. Comprehensive prediction of chromosome dimer resolution sites in bacterial genomes. BMC Genomics 12:19
    [Google Scholar]
  56. 56. 
    Köppen A, Krobitsch S, Thoms B, Wackernagel W. 1995. Interaction with the recombination hot spot chi in vivo converts the RecBCD enzyme of Escherichia coli into a chi-independent recombinase by inactivation of the RecD subunit. PNAS 92:146249–53
    [Google Scholar]
  57. 57. 
    Krasilnikov AS, Podtelezhnikov A, Vologodskii A, Mirkin SM. 1999. Large-scale effects of transcriptional DNA supercoiling in vivo. J. Mol. Biol. 292:51149–60
    [Google Scholar]
  58. 58. 
    Krylov AS, Zasedateleva OA, Prokopenko DV, Rouviere-Yaniv J, Mirzabekov AD. 2001. Massive parallel analysis of the binding specificity of histone-like protein HU to single- and double-stranded DNA with generic oligodeoxyribonucleotide microchips. Nucleic Acids Res 29:122654–60
    [Google Scholar]
  59. 59. 
    Lal A, Dhar A, Trostel A, Kouzine F, Seshasayee ASN, Adhya S. 2016. Genome scale patterns of supercoiling in a bacterial chromosome. Nat. Commun. 7:11055
    [Google Scholar]
  60. 60. 
    Le TB, Laub MT. 2016. Transcription rate and transcript length drive formation of chromosomal interaction domain boundaries. EMBO J 35:141582–95
    [Google Scholar]
  61. 61. 
    Le TBK, Imakaev MV, Mirny LA, Laub MT. 2013. High-resolution mapping of the spatial organization of a bacterial chromosome. Science 342:6159731–34
    [Google Scholar]
  62. 62. 
    Lee CM, Wang G, Pertsinidis A, Marians KJ. 2019. Topoisomerase III acts at the replication fork to remove precatenanes. J. Bacteriol. 201:7e00563-18
    [Google Scholar]
  63. 63. 
    Levy O, Ptacin JL, Pease PJ, Gore J, Eisen MB et al. 2005. Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase. PNAS 102:4917618–23
    [Google Scholar]
  64. 64. 
    Lioy VS, Cournac A, Marbouty M, Duigou S, Mozziconacci J et al. 2018. Multiscale structuring of the E. coli chromosome by nucleoid-associated and condensin proteins. Cell 172:4771–83.e18
    [Google Scholar]
  65. 65. 
    Lioy VS, Junier I, Lagage V, Vallet I, Boccard F. 2020. Distinct activities of bacterial condensins for chromosome management in Pseudomonas aeruginosa. Cell Rep 33:108344
    [Google Scholar]
  66. 66. 
    Liu LF, Wang JC. 1987. Supercoiling of the DNA template during transcription. PNAS 84:207024–27
    [Google Scholar]
  67. 67. 
    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]
  68. 68. 
    Luo H, Gao F. 2019. DoriC 10.0: an updated database of replication origins in prokaryotic genomes including chromosomes and plasmids. Nucleic Acids Res 47:D1D74–77
    [Google Scholar]
  69. 69. 
    Mäkelä J, Sherratt DJ. 2020. Organization of the Escherichia coli chromosome by a MukBEF axial core. Mol. Cell 78:2250–60.e5
    [Google Scholar]
  70. 70. 
    Marbouty M, Baudry L, Cournac A, Koszul R. 2017. Scaffolding bacterial genomes and probing host-virus interactions in gut microbiome by proximity ligation (chromosome capture) assay. Sci. Adv. 3:2e1602105
    [Google Scholar]
  71. 71. 
    Marbouty M, Le Gall A, Cattoni DI, Cournac A, Koh A et al. 2015. Condensin- and replication-mediated bacterial chromosome folding and origin condensation revealed by Hi-C and super-resolution imaging. Mol. Cell 59:4588–602
    [Google Scholar]
  72. 72. 
    Martínez-Antonio A, Janga SC, Thieffry D. 2008. Functional organisation of Escherichia coli transcriptional regulatory network. J. Mol. Biol. 381:1238–47
    [Google Scholar]
  73. 73. 
    Mercier R, Petit MA, 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]
  74. 74. 
    Moulin L, Rahmouni AR, Boccard F. 2005. Topological insulators inhibit diffusion of transcription-induced positive supercoils in the chromosome of Escherichia coli. Mol. Microbiol. 55:2601–10
    [Google Scholar]
  75. 75. 
    Mukherjee S, Seshadri R, Varghese NJ, Eloe-Fadrosh EA, Meier-Kolthoff JP et al. 2017. 1,003 reference genomes of bacterial and archaeal isolates expand coverage of the tree of life. Nat. Biotechnol. 35:7676–83
    [Google Scholar]
  76. 76. 
    Murtin C, Engelhorn M, Geiselmann J, Boccard F. 1998. A quantitative UV laser footprinting analysis of the interaction of IHF with specific binding sites: re-evaluation of the effective concentration of IHF in the cell. J. Mol. Biol. 284:4949–61
    [Google Scholar]
  77. 77. 
    Nielsen HJ, Ottesen JR, Youngren B, Austin SJ, Hansen FG. 2006. The Escherichia coli chromosome is organized with the left and right chromosome arms in separate cell halves. Mol. Microbiol. 62:2331–38
    [Google Scholar]
  78. 78. 
    Niki H, Jaffe 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]
  79. 79. 
    Niki H, Yamaichi Y, Hiraga S. 2000. Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev 14:2212–23
    [Google Scholar]
  80. 80. 
    Nolivos S, Upton AL, Badrinarayanan A, Muller J, Zawadzka K et al. 2016. MatP regulates the coordinated action of topoisomerase IV and MukBEF in chromosome segregation. Nat. Commun. 7:10466
    [Google Scholar]
  81. 81. 
    Ozaki S, Jenal U, Katayama T. 2020. Novel divisome-associated protein spatially coupling the Z-ring with the chromosomal replication terminus in Caulobacter crescentus. mBio 11:2e00487-20
    [Google Scholar]
  82. 82. 
    Petrushenko ZM, She W, Rybenkov VV. 2011. A new family of bacterial condensins. Mol. Microbiol. 81:4881–96
    [Google Scholar]
  83. 83. 
    Pinson V, Takahashi M, Rouviere-Yaniv J. 1999. Differential binding of the Escherichia coli HU, homodimeric forms and heterodimeric form to linear, gapped and cruciform DNA. J. Mol. Biol. 287:3485–97
    [Google Scholar]
  84. 84. 
    Planchenault C, Pons MC, Schiavon C, Siguier P, Rech J et al. 2020. Intracellular positioning systems limit the entropic eviction of secondary replicons toward the nucleoid edges in bacterial cells. J. Mol. Biol. 432:3745–61
    [Google Scholar]
  85. 85. 
    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]
  86. 86. 
    Qin L, Erkelens AM, Ben Bdira F, Dame RT 2019. The architects of bacterial DNA bridges: a structurally and functionally conserved family of proteins. Open Biol 9:12190223
    [Google Scholar]
  87. 87. 
    Rahmouni AR, Wells RD. 1992. Direct evidence for the effect of transcription on local DNA supercoiling in vivo. J. Mol. Biol. 223:1131–44
    [Google Scholar]
  88. 88. 
    Rajasekar KV, Baker R, Fisher GLM, Bolla JR, Mäkelä J et al. 2019. Dynamic architecture of the Escherichia coli structural maintenance of chromosomes (SMC) complex, MukBEF. Nucleic Acids Res 47:189696–707
    [Google Scholar]
  89. 89. 
    Reyes-Lamothe R, Sherratt DJ 2019. The bacterial cell cycle, chromosome inheritance and cell growth. Nat. Rev. Microbiol. 17:8467–78
    [Google Scholar]
  90. 90. 
    Ricci DP, Melfi MD, Lasker K, Dill DL, McAdams HH, Shapiro L. 2016. Cell cycle progression in Caulobacter requires a nucleoid-associated protein with high AT sequence recognition. PNAS 113:40E5952–61
    [Google Scholar]
  91. 91. 
    Rovinskiy N, Agbleke AA, Chesnokova O, Pang Z, Higgins NP. 2012. Rates of gyrase supercoiling and transcription elongation control supercoil density in a bacterial chromosome. PLOS Genet 8:8e1002845
    [Google Scholar]
  92. 92. 
    Sánchez-Romero MA, Casadesús J. 2020. The bacterial epigenome. Nat. Rev. Microbiol. 18:17–20
    [Google Scholar]
  93. 93. 
    Sayyed HE, Chat LL, Lebailly E, Vickridge E, Pages C et al. 2016. Mapping topoisomerase IV binding and activity sites on the E. coli genome. PLOS Genet 12:5e1006025
    [Google Scholar]
  94. 94. 
    Scheirer KE, Higgins NP. 2001. Transcription induces a supercoil domain barrier in bacteriophage Mu. Biochimie 83:2155–59
    [Google Scholar]
  95. 95. 
    Schmidt A, Kochanowski K, Vedelaar S, Ahrné E, Volkmer B et al. 2016. The quantitative and condition-dependent Escherichia coli proteome. Nat. Biotechnol. 34:1104–10
    [Google Scholar]
  96. 96. 
    Schneider R, Lurz R, Lüder G, Tolksdorf C, Travers A, Muskhelishvili G 2001. An architectural role of the Escherichia coli chromatin protein FIS in organising DNA. Nucleic Acids Res 29:245107–14
    [Google Scholar]
  97. 97. 
    Schneider R, Travers A, Muskhelishvili G. 1997. FIS modulates growth phase–dependent topological transitions of DNA in Escherichia coli. Mol. Microbiol. 26:3519–30
    [Google Scholar]
  98. 98. 
    Shen BA, Landick R. 2019. Transcription of bacterial chromatin. J. Mol. Biol. 431:204040–66
    [Google Scholar]
  99. 99. 
    Shendruk TN, Bertrand M, de Haan HW, Harden JL, Slater GW. 2015. Simulating the entropic collapse of coarse-grained chromosomes. Biophys J 108:4810–20
    [Google Scholar]
  100. 100. 
    Sinden RR, Pettijohn DE. 1981. Chromosomes in living Escherichia coli cells are segregated into domains of supercoiling. PNAS 78:1224–28
    [Google Scholar]
  101. 101. 
    Skoko D, Yoo D, Bai H, Schnurr B, Yan J et al. 2006. Mechanism of chromosome compaction and looping by the Escherichia coli nucleoid protein Fis. J. Mol. Biol. 364:4777–98
    [Google Scholar]
  102. 102. 
    Staczek P, Higgins NP. 1998. Gyrase and Topo IV modulate chromosome domain size in vivo. Mol. Microbiol. 29:61435–48
    [Google Scholar]
  103. 103. 
    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]
  104. 104. 
    Strom AR, Brangwynne CP. 2019. The liquid nucleome—phase transitions in the nucleus at a glance. J. Cell Sci. 132:22jcs235093
    [Google Scholar]
  105. 105. 
    Sutormin D, Rubanova N, Logacheva M, Ghilarov D, Severinov K. 2019. Single-nucleotide-resolution mapping of DNA gyrase cleavage sites across the Escherichia coli genome. Nucleic Acids Res 47:31373–88
    [Google Scholar]
  106. 106. 
    Taylor JA, Panis G, Viollier PH, Marczynski GT. 2017. A novel nucleoid-associated protein coordinates chromosome replication and chromosome partition. Nucleic Acids Res 45:158916–29
    [Google Scholar]
  107. 107. 
    Thiel A, Valens M, Vallet-Gely I, Espeli 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]
  108. 108. 
    Tonthat NK, Arold ST, Pickering BF, Van Dyke MW, Liang S et al. 2011. Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J 30:1154–64
    [Google Scholar]
  109. 109. 
    Touchon M, Rocha EPC. 2016. Coevolution of the organization and structure of prokaryotic genomes. Cold Spring Harb. Perspect. Biol. 8:1a018168
    [Google Scholar]
  110. 110. 
    Touzain F, Petit M-A, Schbath S, Karoui ME. 2011. DNA motifs that sculpt the bacterial chromosome. Nat. Rev. Microbiol. 9:115–26
    [Google Scholar]
  111. 111. 
    Tran NT, Laub MT, Le TBK 2017. SMC progressively aligns chromosomal arms in Caulobacter crescentus but is antagonized by convergent transcription. Cell Rep 20:92057–71
    [Google Scholar]
  112. 112. 
    Trussart M, Yus E, Martinez S, Baù D, Tahara YO et al. 2017. Defined chromosome structure in the genome-reduced bacterium Mycoplasma pneumoniae. Nat. Commun. 8:114665
    [Google Scholar]
  113. 113. 
    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]
  114. 114. 
    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]
  115. 115. 
    Valens M, Thiel A, Boccard F. 2016. The MaoP/maoS site-specific system organizes the Ori region of the E. coli chromosome into a macrodomain. PLOS Genet 12:9e1006309
    [Google Scholar]
  116. 116. 
    Vallet-Gely I, Boccard F. 2013. Chromosomal organization and segregation in Pseudomonas aeruginosa. PLOS Genet 9:5e1003492
    [Google Scholar]
  117. 117. 
    Vazquez Nunez R, Ruiz Avila LB, Gruber S 2019. Transient DNA occupancy of the SMC interarm space in prokaryotic condensin. Mol. Cell 75:2209–23.e6
    [Google Scholar]
  118. 118. 
    Verma SC, Qian Z, Adhya SL. 2019. Architecture of the Escherichia coli nucleoid. PLOS Genet 15:12e1008456
    [Google Scholar]
  119. 119. 
    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]
  120. 120. 
    Vora T, Hottes AK, Tavazoie S. 2009. Protein occupancy landscape of a bacterial genome. Mol. Cell 35:2247–53
    [Google Scholar]
  121. 121. 
    Wang S, Cosstick R, Gardner JF, Gumport RI. 1995. The specific binding of Escherichia coli integration host factor involves both major and minor grooves of DNA. Biochemistry 34:4013082–90
    [Google Scholar]
  122. 122. 
    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]
  123. 123. 
    Wang X, Brandão HB, Le TBK, Laub MT, Rudner DZ. 2017. Bacillus subtilis SMC complexes juxtapose chromosome arms as they travel from origin to terminus. Science 355:6324524–27
    [Google Scholar]
  124. 124. 
    Wang X, Le TBK, Lajoie BR, Dekker J, Laub MT, Rudner DZ. 2015. Condensin promotes the juxtaposition of DNA flanking its loading site in Bacillus subtilis. Genes Dev 29:151661–75
    [Google Scholar]
  125. 125. 
    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]
  126. 126. 
    Wang X, Montero Llopis P, Rudner DZ. 2014. Bacillus subtilis chromosome organization oscillates between two distinct patterns. PNAS 111:3512877–82
    [Google Scholar]
  127. 127. 
    Wang X, Tang OW, Riley EP, Rudner DZ. 2014. The SMC condensin complex is required for origin segregation in Bacillus subtilis. Curr. Biol. 24:3287–92
    [Google Scholar]
  128. 128. 
    Weber PM, Moessel F, Paredes GF, Viehboeck T, Vischer NOE, Bulgheresi S. 2019. A bidimensional segregation mode maintains symbiont chromosome orientation toward its host. Curr. Biol. 29:183018–28.e4
    [Google Scholar]
  129. 129. 
    Wilhelm L, Bürmann F, Minnen A, Shin H-C, Toseland CP et al. 2015. SMC condensin entraps chromosomal DNA by an ATP hydrolysis dependent loading mechanism in Bacillus subtilis. eLife 4:e06659
    [Google Scholar]
  130. 130. 
    Worcel A, Burgi E. 1972. On the structure of the folded chromosome of Escherichia coli. J. Mol. Biol. 71:2127–47
    [Google Scholar]
  131. 131. 
    Wu F, Japaridze A, Zheng X, Wiktor J, Kerssemakers JWJ, Dekker C. 2019. Direct imaging of the circular chromosome in a live bacterium. Nat. Commun. 10:12194
    [Google Scholar]
  132. 132. 
    Wu F, Swain P, Kuijpers L, Zheng X, Felter K et al. 2019. Cell boundary confinement sets the size and position of the E. coli chromosome. Curr. Biol. 29:132131–44.e4
    [Google Scholar]
  133. 133. 
    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]
  134. 134. 
    Yatskevich S, Rhodes J, Nasmyth K. 2019. Organization of chromosomal DNA by SMC complexes. Annu. Rev. Genet. 53:445–82
    [Google Scholar]
  135. 135. 
    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]
  136. 136. 
    Zawadzki P, Stracy M, Ginda K, Zawadzka K, Lesterlin C et al. 2015. The localization and action of topoisomerase IV in Escherichia coli chromosome segregation is coordinated by the SMC complex, MukBEF. Cell Rep. 13:112587–96
    [Google Scholar]
  137. 137. 
    Zechiedrich EL, Khodursky AB, Cozzarelli NR. 1997. Topoisomerase IV, not gyrase, decatenates products of site-specific recombination in Escherichia coli. Genes Dev 11:192580–92
    [Google Scholar]
/content/journals/10.1146/annurev-micro-033021-113232
Loading
/content/journals/10.1146/annurev-micro-033021-113232
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error