Architecture of the Escherichia coli nucleoid

English version

Autoři: Subhash C. Verma ^aff001; Zhong Qian ^aff001; Sankar L. Adhya ^aff001
Působiště autorů: Laboratory of Molecular Biology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, United States of America ^aff001
Vyšlo v časopise: Architecture of the Escherichia coli nucleoid. PLoS Genet 15(12): e1008456. doi:10.1371/journal.pgen.1008456
Kategorie: Topic Page
doi: https://doi.org/10.1371/journal.pgen.1008456

Souhrn

How genomes are organized within cells and how the 3D architecture of a genome influences cellular functions are significant questions in biology. A bacterial genomic DNA resides inside cells in a highly condensed and functionally organized form called nucleoid (nucleus-like structure without a nuclear membrane). The Escherichia coli chromosome or nucleoid is composed of the genomic DNA, RNA, and protein. The nucleoid forms by condensation and functional arrangement of a single chromosomal DNA with the help of chromosomal architectural proteins and RNA molecules as well as DNA supercoiling. Although a high-resolution structure of a bacterial nucleoid is yet to come, five decades of research has established the following salient features of the E. coli nucleoid elaborated below: 1) The chromosomal DNA is on the average a negatively supercoiled molecule that is folded as plectonemic loops, which are confined into many independent topological domains due to supercoiling diffusion barriers; 2) The loops spatially organize into megabase size regions called macrodomains, which are defined by more frequent physical interactions among DNA sites within the same macrodomain than between different macrodomains; 3) The condensed and spatially organized DNA takes the form of a helical ellipsoid radially confined in the cell; and 4) The DNA in the chromosome appears to have a condition-dependent 3-D structure that is linked to gene expression so that the nucleoid architecture and gene transcription are tightly interdependent, influencing each other reciprocally. Current advents of high-resolution microscopy, single-molecule analysis and molecular structure determination of the components are expected to reveal the total structure and function of the bacterial nucleoid.

Klíčová slova:

Bacterial genomics – Condensation – DNA – DNA structure – DNA transcription – DNA-binding proteins – Sequence motif analysis – Chromosomal DNA

Zdroje

1. Stonington OG, Pettijohn DE. The folded genome of Escherichia coli isolated in a protein-DNA-RNA complex. Proc Natl Acad Sci U S A. 1971;68(1):6–9. Epub 1971/01/01. doi: 10.1073/pnas.68.1.6 4924971; PubMed Central PMCID: PMC391088.

2. Worcel A, Burgi E. On the structure of the folded chromosome of Escherichia coli. J Mol Biol. 1972;71(2):127–47. doi: 10.1016/0022-2836(72)90342-7 4564477.

3. Dame RT, Tark-Dame M. Bacterial chromatin: converging views at different scales. Curr Opin Cell Biol. 2016;40:60–5. doi: 10.1016/j.ceb.2016.02.015 26942688.

4. Kleckner N, Fisher JK, Stouf M, White MA, Bates D, Witz G. The bacterial nucleoid: nature, dynamics and sister segregation. Curr Opin Microbiol. 2014;22:127–37. Epub 2014/12/03. doi: 10.1016/j.mib.2014.10.001 25460806; PubMed Central PMCID: PMC4359759.

5. Bloomfield VA. DNA condensation by multivalent cations. Biopolymers. 1997;44(3):269–82. doi: 10.1002/(SICI)1097-0282(1997)44:3<269::AID-BIP6>3.0.CO;2-T PubMed PMID: WOS:000073424300006. 9591479

6. Trun N, Marko J. Architecture of a bacterial chromosome. Am Soc Microbiol News. 1998;64(5):276–83.

7. Valens M, Penaud S, Rossignol M, Cornet F, Boccard F. Macrodomain organization of the Escherichia coli chromosome. EMBO J. 2004;23(21):4330–41. doi: 10.1038/sj.emboj.7600434 15470498; PubMed Central PMCID: PMC524398.

8. Fisher JK, Bourniquel A, Witz G, Weiner B, Prentiss M, Kleckner N. Four-dimensional imaging of E. coli nucleoid organization and dynamics in living cells. Cell. 2013;153(4):882–95. doi: 10.1016/j.cell.2013.04.006 23623305; PubMed Central PMCID: PMC3670778.

9. Le Gall A, Cattoni DI, Guilhas B, Mathieu-Demaziere C, Oudjedi L, Fiche JB, et al. Bacterial partition complexes segregate within the volume of the nucleoid. Nat Commun. 2016;7:12107. doi: 10.1038/ncomms12107 27377966; PubMed Central PMCID: PMC4935973.

10. Hadizadeh Yazdi N, Guet CC, Johnson RC, Marko JF. Variation of the folding and dynamics of the Escherichia coli chromosome with growth conditions. Mol Microbiol. 2012;86(6):1318–33. doi: 10.1111/mmi.12071 23078205; PubMed Central PMCID: PMC3524407.

11. Olins AL, Olins DE. Spheroid chromatin units (v bodies). Science. 1974;183(4122):330–2. Epub 1974/01/25. doi: 10.1126/science.183.4122.330 4128918.

12. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997;389(6648):251–60. Epub 1997/09/26. doi: 10.1038/38444 9305837.

13. Khorasanizadeh S. The nucleosome: from genomic organization to genomic regulation. Cell. 2004;116(2):259–72. Epub 2004/01/28. doi: 10.1016/s0092-8674(04)00044-3 14744436.

14. Talukder A, Ishihama A. Growth phase dependent changes in the structure and protein composition of nucleoid in Escherichia coli. Science China Life sciences. 2015;58(9):902–11. Epub 2015/07/26. doi: 10.1007/s11427-015-4898-0 26208826.

15. Azam TA, Ishihama A. Twelve species of the nucleoid-associated protein from Escherichia coli. Sequence recognition specificity and DNA binding affinity. J Biol Chem. 1999;274(46):33105–13. Epub 1999/11/07. doi: 10.1074/jbc.274.46.33105 10551881.

16. Ali Azam T, Iwata A, Nishimura A, Ueda S, Ishihama A. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol. 1999;181(20):6361–70. Epub 1999/10/09. 10515926; PubMed Central PMCID: PMC103771.

17. Swinger KK, Lemberg KM, Zhang Y, Rice PA. Flexible DNA bending in HU-DNA cocrystal structures. EMBO J. 2003;22(14):3749–60. doi: 10.1093/emboj/cdg351 12853489; PubMed Central PMCID: PMC165621.

18. Guo F, Adhya S. Spiral structure of Escherichia coli HUalphabeta provides foundation for DNA supercoiling. Proc Natl Acad Sci U S A. 2007;104(11):4309–14. Epub 2007/03/16. doi: 10.1073/pnas.0611686104 17360520; PubMed Central PMCID: PMC1838598.

19. Pinson V, Takahashi M, Rouviere-Yaniv J. Differential binding of the Escherichia coli HU, homodimeric forms and heterodimeric form to linear, gapped and cruciform DNA. J Mol Biol. 1999;287(3):485–97. Epub 1999/03/27. doi: 10.1006/jmbi.1999.2631 10092454.

20. Lang B, Blot N, Bouffartigues E, Buckle M, Geertz M, Gualerzi CO, et al. High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Research. 2007;35(18):6330–7. doi: 10.1093/nar/gkm712 PubMed PMID: WOS:000250683600041. 17881364

21. Gulvady R, Gao Y, Kenney LJ, Yan J. A single molecule analysis of H-NS uncouples DNA binding affinity from DNA specificity. Nucleic Acids Res. 2018;46(19):10216–24. Epub 2018/09/22. doi: 10.1093/nar/gky826 30239908; PubMed Central PMCID: PMC6212787.

22. Craig NL, Nash HA. E. coli integration host factor binds to specific sites in DNA. Cell. 1984;39(3 Pt 2):707–16. doi: 10.1016/0092-8674(84)90478-1 6096022.

23. Wang S, Cosstick R, Gardner JF, Gumport RI. The specific binding of Escherichia coli integration host factor involves both major and minor grooves of DNA. Biochemistry-Us. 1995;34(40):13082–90. Epub 1995/10/10. doi: 10.1021/bi00040a020 7548068.

24. Shao Y, Feldman-Cohen LS, Osuna R. Functional characterization of the Escherichia coli Fis-DNA binding sequence. J Mol Biol. 2008;376(3):771–85. doi: 10.1016/j.jmb.2007.11.101 18178221; PubMed Central PMCID: PMC2292415.

25. Stella S, Cascio D, Johnson RC. The shape of the DNA minor groove directs binding by the DNA-bending protein Fis. Genes Dev. 2010;24(8):814–26. doi: 10.1101/gad.1900610 20395367; PubMed Central PMCID: PMC2854395.

26. Karas VO, Westerlaken I, Meyer AS. The DNA-Binding Protein from Starved Cells (Dps) Utilizes Dual Functions To Defend Cells against Multiple Stresses. J Bacteriol. 2015;197(19):3206–15. Epub 2015/07/29. doi: 10.1128/JB.00475-15 26216848; PubMed Central PMCID: PMC4560292.

27. Mercier R, Petit MA, Schbath S, Robin S, El Karoui M, Boccard F, et al. The MatP/matS Site-Specific System Organizes the Terminus Region of the E-coli Chromosome into a Macrodomain. Cell. 2008;135(3):475–85. doi: 10.1016/j.cell.2008.08.031 PubMed PMID: WOS:000260536300018. 18984159

28. Rouviere-Yaniv J, Gros F. Characterization of a novel, low-molecular-weight DNA-binding protein from Escherichia coli. Proc Natl Acad Sci U S A. 1975;72(9):3428–32. Epub 1975/09/01. doi: 10.1073/pnas.72.9.3428 1103148; PubMed Central PMCID: PMC433007.

29. Suryanarayana T, Subramanian AR. Specific association of two homologous DNA-binding proteins to the native 30-S ribosomal subunits of Escherichia coli. Biochimica et biophysica acta. 1978;520(2):342–57. Epub 1978/09/27. doi: 10.1016/0005-2787(78)90232-0 213117.

30. Mende L, Timm B, Subramanian R. Primary structures of two homologous ribosome-associated DNA-binding proteins of Escherichia coli. FEBS Lett. 1978;96(2):395–8. doi: 10.1016/0014-5793(78)80446-3 215461.

31. Megraw TL, Chae CB. Functional complementarity between the HMG1-like yeast mitochondrial histone HM and the bacterial histone-like protein HU. J Biol Chem. 1993;268(17):12758–63. Epub 1993/06/15. 8509411.

32. Paull TT, Johnson RC. DNA looping by Saccharomyces cerevisiae high mobility group proteins NHP6A/B. Consequences for nucleoprotein complex assembly and chromatin condensation. J Biol Chem. 1995;270(15):8744–54. Epub 1995/04/14. doi: 10.1074/jbc.270.15.8744 7721780.

33. Kamashev D, Rouviere-Yaniv J. The histone-like protein HU binds specifically to DNA recombination and repair intermediates. EMBO J. 2000;19(23):6527–35. Epub 2000/12/02. doi: 10.1093/emboj/19.23.6527 11101525; PubMed Central PMCID: PMC305869.

34. Shindo H, Furubayashi A, Shimizu M, Miyake M, Imamoto F. Preferential binding of E.coli histone-like protein HU alpha to negatively supercoiled DNA. Nucleic Acids Res. 1992;20(7):1553–8. doi: 10.1093/nar/20.7.1553 1579448; PubMed Central PMCID: PMC312237.

35. Pontiggia A, Negri A, Beltrame M, Bianchi ME. Protein HU binds specifically to kinked DNA. Mol Microbiol. 1993;7(3):343–50. doi: 10.1111/j.1365-2958.1993.tb01126.x 8459763.

36. Bonnefoy E, Takahashi M, Yaniv JR. DNA-binding parameters of the HU protein of Escherichia coli to cruciform DNA. J Mol Biol. 1994;242(2):116–29. doi: 10.1006/jmbi.1994.1563 8089835.

37. Castaing B, Zelwer C, Laval J, Boiteux S. HU protein of Escherichia coli binds specifically to DNA that contains single-strand breaks or gaps. J Biol Chem. 1995;270(17):10291–6. doi: 10.1074/jbc.270.17.10291 7730334.

38. Lyubchenko YL, Shlyakhtenko LS, Aki T, Adhya S. Atomic force microscopic demonstration of DNA looping by GalR and HU. Nucleic Acids Res. 1997;25(4):873–6. doi: 10.1093/nar/25.4.873 9016640; PubMed Central PMCID: PMC146491.

39. Swinger KK, Rice PA. Structure-based analysis of HU-DNA binding. J Mol Biol. 2007;365(4):1005–16. Epub 2006/11/14. doi: 10.1016/j.jmb.2006.10.024 17097674; PubMed Central PMCID: PMC1945228.

40. Hammel M, Amlanjyoti D, Reyes FE, Chen JH, Parpana R, Tang HY, et al. HU multimerization shift controls nucleoid compaction. Sci Adv. 2016;2(7):e1600650. doi: 10.1126/sciadv.1600650 27482541; PubMed Central PMCID: PMC4966879.

41. Kano Y, Goshima N, Wada M, Imamoto F. Participation of hup gene product in replicative transposition of Mu phage in Escherichia coli. Gene. 1989;76(2):353–8. doi: 10.1016/0378-1119(89)90175-3 2666261.

42. Ogura T, Niki H, Kano Y, Imamoto F, Hiraga S. Maintenance of plasmids in HU and IHF mutants of Escherichia coli. Mol Gen Genet. 1990;220(2):197–203. doi: 10.1007/bf00260482 2183003.

43. Hwang DS, Kornberg A. Opening of the replication origin of Escherichia coli by DnaA protein with protein HU or IHF. J Biol Chem. 1992;267(32):23083–6. Epub 1992/11/15. 1429655.

44. Macvanin M, Edgar R, Cui F, Trostel A, Zhurkin V, Adhya S. Noncoding RNAs binding to the nucleoid protein HU in Escherichia coli. J Bacteriol. 2012;194(22):6046–55. Epub 2012/09/04. doi: 10.1128/JB.00961-12 22942248; PubMed Central PMCID: PMC3486375.

45. van Noort J, Verbrugge S, Goosen N, Dekker C, Dame RT. Dual architectural roles of HU: formation of flexible hinges and rigid filaments. Proc Natl Acad Sci U S A. 2004;101(18):6969–74. Epub 2004/05/01. doi: 10.1073/pnas.0308230101 15118104; PubMed Central PMCID: PMC406450.

46. Kahramanoglou C, Seshasayee AS, Prieto AI, Ibberson D, Schmidt S, Zimmermann J, et al. Direct and indirect effects of H-NS and Fis on global gene expression control in Escherichia coli. Nucleic Acids Res. 2011;39(6):2073–91. doi: 10.1093/nar/gkq934 21097887; PubMed Central PMCID: PMC3064808.

47. Prieto AI, Kahramanoglou C, Ali RM, Fraser GM, Seshasayee AS, Luscombe NM. Genomic analysis of DNA binding and gene regulation by homologous nucleoid-associated proteins IHF and HU in Escherichia coli K12. Nucleic Acids Res. 2012;40(8):3524–37. Epub 2011/12/20. doi: 10.1093/nar/gkr1236 22180530; PubMed Central PMCID: PMC3333857.

48. Sarkar R, Rybenkov VV. A Guide to Magnetic Tweezers and Their Applications. Front Phys. 2016;4. doi: ARTN 48. PubMed PMID: WOS:000389259500002. doi: 10.3389/fphy.2016.00048

49. Rice PA, Yang S, Mizuuchi K, Nash HA. Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn. Cell. 1996;87(7):1295–306. doi: 10.1016/s0092-8674(00)81824-3 8980235.

50. Murtin C, Engelhorn M, Geiselmann J, Boccard F. 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. 1998;284(4):949–61. Epub 1998/12/05. doi: 10.1006/jmbi.1998.2256 9837718.

51. Ditto MD, Roberts D, Weisberg RA. Growth phase variation of integration host factor level in Escherichia coli. J Bacteriol. 1994;176(12):3738–48. Epub 1994/06/01. doi: 10.1128/jb.176.12.3738-3748.1994 8206852; PubMed Central PMCID: PMC205563.

52. Lin J, Chen H, Droge P, Yan J. Physical organization of DNA by multiple non-specific DNA-binding modes of integration host factor (IHF). PLoS One. 2012;7(11):e49885. doi: 10.1371/journal.pone.0049885 23166787; PubMed Central PMCID: PMC3498176.

53. Jacquet M, Cukier-Kahn R, Pla J, Gros F. A thermostable protein factor acting on in vitro DNA transcription. Biochem Biophys Res Commun. 1971;45(6):1597–607. doi: 10.1016/0006-291x(71)90204-x 4942735.

54. Cukier-Kahn R, Jacquet M, Gros F. Two heat-resistant, low molecular weight proteins from Escherichia coli that stimulate DNA-directed RNA synthesis. Proc Natl Acad Sci U S A. 1972;69(12):3643–7. doi: 10.1073/pnas.69.12.3643 4566454; PubMed Central PMCID: PMC389839.

55. Spassky A, Buc HC. Physico-chemical properties of a DNA binding protein: Escherichia coli factor H1. Eur J Biochem. 1977;81(1):79–90. doi: 10.1111/j.1432-1033.1977.tb11929.x 338303.

56. Varshavsky AJ, Nedospasov SA, Bakayev VV, Bakayeva TG, Georgiev GP. Histone-like proteins in the purified Escherichia coli deoxyribonucleoprotein. Nucleic Acids Res. 1977;4(8):2725–45. doi: 10.1093/nar/4.8.2725 333393; PubMed Central PMCID: PMC342604.

57. Falconi M, Gualtieri MT, La Teana A, Losso MA, Pon CL. Proteins from the prokaryotic nucleoid: primary and quaternary structure of the 15-kD Escherichia coli DNA binding protein H-NS. Mol Microbiol. 1988;2(3):323–9. doi: 10.1111/j.1365-2958.1988.tb00035.x 3135462.

58. Ueguchi C, Suzuki T, Yoshida T, Tanaka K, Mizuno T. Systematic mutational analysis revealing the functional domain organization of Escherichia coli nucleoid protein H-NS. J Mol Biol. 1996;263(2):149–62. doi: 10.1006/jmbi.1996.0566 8913298.

59. Rimsky S, Zuber F, Buckle M, Buc H. A molecular mechanism for the repression of transcription by the H-NS protein. Mol Microbiol. 2001;42(5):1311–23. doi: 10.1046/j.1365-2958.2001.02706.x 11886561.

60. Bouffartigues E, Buckle M, Badaut C, Travers A, Rimsky S. H-NS cooperative binding to high-affinity sites in a regulatory element results in transcriptional silencing. Nat Struct Mol Biol. 2007;14(5):441–8. Epub 2007/04/17. doi: 10.1038/nsmb1233 17435766.

61. Amit R, Oppenheim AB, Stavans J. Increased bending rigidity of single DNA molecules by H-NS, a temperature and osmolarity sensor. Biophys J. 2003;84(4):2467–73. doi: 10.1016/S0006-3495(03)75051-6 12668454; PubMed Central PMCID: PMC1302812.

62. Dame RT, Noom MC, Wuite GJ. Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature. 2006;444(7117):387–90. doi: 10.1038/nature05283 17108966.

63. Dame RT, Wyman C, Goosen N. H-NS mediated compaction of DNA visualised by atomic force microscopy. Nucleic Acids Res. 2000;28(18):3504–10. doi: 10.1093/nar/28.18.3504 10982869; PubMed Central PMCID: PMC110753.

64. Liu Y, Chen H, Kenney LJ, Yan J. A divalent switch drives H-NS/DNA-binding conformations between stiffening and bridging modes. Genes Dev. 2010;24(4):339–44. doi: 10.1101/gad.1883510 20159954; PubMed Central PMCID: PMC2816733.

65. van der Valk RA, Vreede J, Qin L, Moolenaar GF, Hofmann A, Goosen N, et al. Mechanism of environmentally driven conformational changes that modulate H-NS DNA-bridging activity. Elife. 2017;6. doi: e27369 doi: 10.7554/eLife.27369 PubMed PMID: WOS:000413181000001.

66. Yamada H, Muramatsu S, Mizuno T. An Escherichia-Coli Protein That Preferentially Binds to Sharply Curved DNA. J Biochem-Tokyo. 1990;108(3):420–5. PubMed PMID: WOS:A1990DX38200014. doi: 10.1093/oxfordjournals.jbchem.a123216 2126011

67. Martin-Orozco N, Touret N, Zaharik ML, Park E, Kopelman R, Miller S, et al. Visualization of vacuolar acidification-induced transcription of genes of pathogens inside macrophages. Molecular biology of the cell. 2006;17(1):498–510. Epub 2005/10/28. doi: 10.1091/mbc.E04-12-1096 16251362; PubMed Central PMCID: PMC1345685.

68. Winardhi RS, Yan J, Kenney LJ. H-NS Regulates Gene Expression and Compacts the Nucleoid: Insights from Single-Molecule Experiments. Biophys J. 2015;109(7):1321–9. doi: 10.1016/j.bpj.2015.08.016 26445432; PubMed Central PMCID: PMC4601063.

69. Walthers D, Li Y, Liu Y, Anand G, Yan J, Kenney LJ. Salmonella enterica response regulator SsrB relieves H-NS silencing by displacing H-NS bound in polymerization mode and directly activates transcription. J Biol Chem. 2011;286(3):1895–902. Epub 2010/11/10. doi: 10.1074/jbc.M110.164962 21059643; PubMed Central PMCID: PMC3023485.

70. Gao Y, Foo YH, Winardhi RS, Tang Q, Yan J, Kenney LJ. Charged residues in the H-NS linker drive DNA binding and gene silencing in single cells. Proc Natl Acad Sci U S A. 2017;114(47):12560–5. Epub 2017/11/08. doi: 10.1073/pnas.1716721114 29109287; PubMed Central PMCID: PMC5703333.

71. Hancock SP, Stella S, Cascio D, Johnson RC. DNA Sequence Determinants Controlling Affinity, Stability and Shape of DNA Complexes Bound by the Nucleoid Protein Fis. PLoS One. 2016;11(3):e0150189. doi: 10.1371/journal.pone.0150189 26959646; PubMed Central PMCID: PMC4784862.

72. Kostrewa D, Granzin J, Koch C, Choe HW, Raghunathan S, Wolf W, et al. Three-dimensional structure of the E. coli DNA-binding protein FIS. Nature. 1991;349(6305):178–80. doi: 10.1038/349178a0 1986310.

73. Kostrewa D, Granzin J, Stock D, Choe HW, Labahn J, Saenger W. Crystal structure of the factor for inversion stimulation FIS at 2.0 A resolution. J Mol Biol. 1992;226(1):209–26. doi: 10.1016/0022-2836(92)90134-6 1619650.

74. Cho BK, Knight EM, Barrett CL, Palsson BO. Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts. Genome Res. 2008;18(6):900–10. doi: 10.1101/gr.070276.107 18340041; PubMed Central PMCID: PMC2413157.

75. Travers A, Muskhelishvili G. DNA microloops and microdomains: a general mechanism for transcription activation by torsional transmission. J Mol Biol. 1998;279(5):1027–43. doi: 10.1006/jmbi.1998.1834 9642081.

76. Skoko D, Yan J, Johnson RC, Marko JF. Low-force DNA condensation and discontinuous high-force decondensation reveal a loop-stabilizing function of the protein Fis. Physical review letters. 2005;95(20):208101. doi: 10.1103/PhysRevLett.95.208101 16384101.

77. Skoko D, Yoo D, Bai H, Schnurr B, Yan J, McLeod SM, et al. Mechanism of chromosome compaction and looping by the Escherichia coli nucleoid protein Fis. J Mol Biol. 2006;364(4):777–98. doi: 10.1016/j.jmb.2006.09.043 17045294; PubMed Central PMCID: PMC1988847.

78. Johnson RC, Simon MI. Hin-mediated site-specific recombination requires two 26 bp recombination sites and a 60 bp recombinational enhancer. Cell. 1985;41(3):781–91. doi: 10.1016/s0092-8674(85)80059-3 2988787.

79. Kahmann R, Rudt F, Koch C, Mertens G. G-Inversion in Bacteriophage-Mu-DNA Is Stimulated by a Site within the Invertase Gene and a Host Factor. Cell. 1985;41(3):771–80. doi: 10.1016/s0092-8674(85)80058-1 PubMed PMID: WOS:A1985AMS1500016. 3159478

80. Pettijohn DE, Hecht R. RNA molecules bound to the folded bacterial genome stabilize DNA folds and segregate domains of supercoiling. Cold Spring Harbor symposia on quantitative biology. 1974;38:31–41. Epub 1974/01/01. doi: 10.1101/sqb.1974.038.01.006 4598638.

81. Ohniwa RL, Morikawa K, Takeshita SL, Kim J, Ohta T, Wada C, et al. Transcription-coupled nucleoid architecture in bacteria. Genes Cells. 2007;12(10):1141–52. doi: 10.1111/j.1365-2443.2007.01125.x 17903174.

82. Balandina A, Kamashev D, Rouviere-Yaniv J. The bacterial histone-like protein HU specifically recognizes similar structures in all nucleic acids. DNA, RNA, and their hybrids. J Biol Chem. 2002;277(31):27622–8. Epub 2002/05/15. doi: 10.1074/jbc.M201978200 12006568.

83. Balandina A, Claret L, Hengge-Aronis R, Rouviere-Yaniv J. The Escherichia coli histone-like protein HU regulates rpoS translation. Mol Microbiol. 2001;39(4):1069–79. Epub 2001/03/17. doi: 10.1046/j.1365-2958.2001.02305.x 11251825.

84. Qian Z, Macvanin M, Dimitriadis EK, He X, Zhurkin V, Adhya S. A New Noncoding RNA Arranges Bacterial Chromosome Organization. MBio. 2015;6(4). Epub 2015/08/27. doi: 10.1128/mBio.00998-15 26307168; PubMed Central PMCID: PMC4550694.

85. Qian Z, Zhurkin VB, Adhya S. DNA-RNA interactions are critical for chromosome condensation in Escherichia coli. Proc Natl Acad Sci U S A. 2017;114(46):12225–30. Epub 2017/11/01. doi: 10.1073/pnas.1711285114 29087325; PubMed Central PMCID: PMC5699063.

86. Bauer WR, Crick FH, White JH. Supercoiled DNA. Sci Am. 1980;243(1):100–13. Epub 1980/07/01. 6256851.

87. Sinden R. DNA Structure and Function. San Diego: Academic Press; 1994.

88. Bates AD, Maxwell A. DNA Topology. Oxford: Oxford University Press; 2005.

89. Sinden RR, Carlson JO, Pettijohn DE. Torsional tension in the DNA double helix measured with trimethylpsoralen in living E. coli cells: analogous measurements in insect and human cells. Cell. 1980;21(3):773–83. doi: 10.1016/0092-8674(80)90440-7 6254668.

90. Griffith JD. Visualization of prokaryotic DNA in a regularly condensed chromatin-like fiber. Proc Natl Acad Sci U S A. 1976;73(2):563–7. doi: 10.1073/pnas.73.2.563 1108025; PubMed Central PMCID: PMC335950.

91. Postow L, Hardy CD, Arsuaga J, Cozzarelli NR. Topological domain structure of the Escherichia coli chromosome. Genes Dev. 2004;18(14):1766–79. doi: 10.1101/gad.1207504 15256503; PubMed Central PMCID: PMC478196.

92. Bliska JB, Cozzarelli NR. Use of site-specific recombination as a probe of DNA structure and metabolism in vivo. J Mol Biol. 1987;194(2):205–18. doi: 10.1016/0022-2836(87)90369-x 3039150.

93. Holmes VF, Cozzarelli NR. Closing the ring: Links between SMC proteins and chromosome partitioning, condensation, and supercoiling. P Natl Acad Sci USA. 2000;97(4):1322–4. doi: 10.1073/pnas.040576797 PubMed PMID: WOS:000085409600003. 10677457

94. Champoux JJ. DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem. 2001;70:369–413. doi: 10.1146/annurev.biochem.70.1.369 11395412.

95. Gellert M, Mizuuchi K, Odea MH, Nash HA. DNA Gyrase—Enzyme That Introduces Superhelical Turns into DNA. P Natl Acad Sci USA. 1976;73(11):3872–6. doi: 10.1073/pnas.73.11.3872 PubMed PMID: WOS:A1976CN11500019. 186775

96. Depew RE, Liu LF, Wang JC. Interaction between DNA and Escherichia-Coli Protein-Omega—Formation of a Complex between Single-Stranded-DNA and Omega-Protein. Journal of Biological Chemistry. 1978;253(2):511–8. PubMed PMID: WOS:A1978EK02600037. 338610

97. Kirkegaard K, Wang JC. Escherichia coli DNA topoisomerase I catalyzed linking of single-stranded rings of complementary base sequences. Nucleic Acids Res. 1978;5(10):3811–20. Epub 1978/10/01. doi: 10.1093/nar/5.10.3811 214763; PubMed Central PMCID: PMC342711.

98. Raji A, Zabel DJ, Laufer CS, Depew RE. Genetic-Analysis of Mutations That Compensate for Loss of Escherichia-Coli DNA Topoisomerase-I. Journal of Bacteriology. 1985;162(3):1173–9. PubMed PMID: WOS:A1985AJL5700047. 2987184

99. Dean F, Krasnow MA, Otter R, Matzuk MM, Spengler SJ, Cozzarelli NR. Escherichia coli type-1 topoisomerases: identification, mechanism, and role in recombination. Cold Spring Harbor symposia on quantitative biology. 1983;47 Pt 2:769–77. doi: 10.1101/sqb.1983.047.01.088 6305585.

100. Zechiedrich EL, Khodursky AB, Bachellier S, Schneider R, Chen D, Lilley DM, et al. Roles of topoisomerases in maintaining steady-state DNA supercoiling in Escherichia coli. J Biol Chem. 2000;275(11):8103–13. doi: 10.1074/jbc.275.11.8103 10713132.

101. Kato J, Nishimura Y, Imamura R, Niki H, Hiraga S, Suzuki H. New topoisomerase essential for chromosome segregation in E. coli. Cell. 1990;63(2):393–404. doi: 10.1016/0092-8674(90)90172-b 2170028.

102. Liu LF, Wang JC. Supercoiling of the DNA template during transcription. Proc Natl Acad Sci U S A. 1987;84(20):7024–7. doi: 10.1073/pnas.84.20.7024 2823250; PubMed Central PMCID: PMC299221.

103. Kouzine F, Liu J, Sanford S, Chung HJ, Levens D. The dynamic response of upstream DNA to transcription-generated torsional stress. Nat Struct Mol Biol. 2004;11(11):1092–100. Epub 2004/10/27. doi: 10.1038/nsmb848 15502847.

104. Rouviere-Yaniv J, Yaniv M, Germond JE. E. coli DNA binding protein HU forms nucleosomelike structure with circular double-stranded DNA. Cell. 1979;17(2):265–74. Epub 1979/06/01. doi: 10.1016/0092-8674(79)90152-1 222478.

105. Broyles SS, Pettijohn DE. Interaction of the Escherichia coli HU protein with DNA. Evidence for formation of nucleosome-like structures with altered DNA helical pitch. J Mol Biol. 1986;187(1):47–60. Epub 1986/01/05. doi: 10.1016/0022-2836(86)90405-5 3514923.

106. Kundukad B, Cong P, van der Maarel JR, Doyle PS. Time-dependent bending rigidity and helical twist of DNA by rearrangement of bound HU protein. Nucleic Acids Res. 2013;41(17):8280–8. doi: 10.1093/nar/gkt593 23828037; PubMed Central PMCID: PMC3783175.

107. Tupper AE, Owen-Hughes TA, Ussery DW, Santos DS, Ferguson DJ, Sidebotham JM, et al. The chromatin-associated protein H-NS alters DNA topology in vitro. EMBO J. 1994;13(1):258–68. 8306968; PubMed Central PMCID: PMC394800.

108. Schneider R, Lurz R, Luder G, Tolksdorf C, Travers A, Muskhelishvili G. An architectural role of the Escherichia coli chromatin protein FIS in organising DNA. Nucleic Acids Res. 2001;29(24):5107–14. doi: 10.1093/nar/29.24.5107 11812843; PubMed Central PMCID: PMC97572.

109. Schneider R, Travers A, Kutateladze T, Muskhelishvili G. A DNA architectural protein couples cellular physiology and DNA topology in Escherichia coli. Mol Microbiol. 1999;34(5):953–64. doi: 10.1046/j.1365-2958.1999.01656.x 10594821.

110. Bensaid A, Almeida A, Drlica K, Rouviere-Yaniv J. Cross-talk between topoisomerase I and HU in Escherichia coli. J Mol Biol. 1996;256(2):292–300. Epub 1996/02/23. doi: 10.1006/jmbi.1996.0086 8594197.

111. Malik M, Bensaid A, Rouviere-Yaniv J, Drlica K. Histone-like protein HU and bacterial DNA topology: suppression of an HU deficiency by gyrase mutations. J Mol Biol. 1996;256(1):66–76. Epub 1996/02/16. doi: 10.1006/jmbi.1996.0068 8609614.

112. Marians KJ. DNA gyrase-catalyzed decatenation of multiply linked DNA dimers. J Biol Chem. 1987;262(21):10362–8. Epub 1987/07/25. 3038875.

113. Sinden RR, Pettijohn DE. Chromosomes in living Escherichia coli cells are segregated into domains of supercoiling. Proc Natl Acad Sci U S A. 1981;78(1):224–8. Epub 1981/01/01. doi: 10.1073/pnas.78.1.224 6165987; PubMed Central PMCID: PMC319024.

114. Higgins NP, Yang XL, Fu QQ, Roth JR. Surveying a supercoil domain by using the gamma delta resolution system in Salmonella typhimurium. Journal of Bacteriology. 1996;178(10):2825–35. doi: 10.1128/jb.178.10.2825-2835.1996 PubMed PMID: WOS:A1996UL27500013. 8631670

115. Yan Y, Ding Y, Leng F, Dunlap D, Finzi L. Protein-mediated loops in supercoiled DNA create large topological domains. Nucleic Acids Res. 2018;46(9):4417–24. Epub 2018/03/15. doi: 10.1093/nar/gky153 29538766; PubMed Central PMCID: PMC5961096.

116. Leng F, Chen B, Dunlap DD. Dividing a supercoiled DNA molecule into two independent topological domains. Proc Natl Acad Sci U S A. 2011;108(50):19973–8. doi: 10.1073/pnas.1109854108 22123985; PubMed Central PMCID: PMC3250177.

117. Moulin L, Rahmouni AR, Boccard F. Topological insulators inhibit diffusion of transcription-induced positive supercoils in the chromosome of Escherichia coli. Mol Microbiol. 2005;55(2):601–10. Epub 2005/01/22. doi: 10.1111/j.1365-2958.2004.04411.x 15659173.

118. Dimri GP, Rudd KE, Morgan MK, Bayat H, Ames GFL. Physical Mapping of Repetitive Extragenic Palindromic Sequences in Escherichia-Coli and Phylogenetic Distribution among Escherichia-Coli Strains and Other Enteric Bacteria. Journal of Bacteriology. 1992;174(14):4583–93. doi: 10.1128/jb.174.14.4583-4593.1992 1624447:A1992JE39900007.

119. Booker BM, Deng S, Higgins NP. DNA topology of highly transcribed operons in Salmonella enterica serovar Typhimurium. Mol Microbiol. 2010;78(6):1348–64. Epub 2010/12/15. doi: 10.1111/j.1365-2958.2010.07394.x 21143310.

120. Deng S, Stein RA, Higgins NP. Organization of supercoil domains and their reorganization by transcription. Molecular Microbiology. 2005;57(6):1511–21. doi: 10.1111/j.1365-2958.2005.04796.x PubMed PMID: WOS:000231610600001. 16135220

121. Deng S, Stein RA, Higgins NP. Transcription-induced barriers to supercoil diffusion in the Salmonella typhimurium chromosome. Proc Natl Acad Sci U S A. 2004;101(10):3398–403. Epub 2004/03/03. doi: 10.1073/pnas.0307550101 14993611; PubMed Central PMCID: PMC373473.

122. Dekker J, Rippe K, Dekker M, Kleckner N. Capturing chromosome conformation. Science. 2002;295(5558):1306–11. doi: 10.1126/science.1067799 PubMed PMID: WOS:000173926000047. 11847345

123. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009;326(5950):289–93. Epub 2009/10/10. doi: 10.1126/science.1181369 19815776; PubMed Central PMCID: PMC2858594.

124. Lioy VS, Cournac A, Marbouty M, Duigou S, Mozziconacci J, Espeli O, et al. Multiscale Structuring of the E. coli Chromosome by Nucleoid-Associated and Condensin Proteins. Cell. 2018;172(4):771–83 e18. Epub 2018/01/24. doi: 10.1016/j.cell.2017.12.027 29358050.

125. Le TB, Imakaev MV, Mirny LA, Laub MT. High-resolution mapping of the spatial organization of a bacterial chromosome. Science. 2013;342(6159):731–4. Epub 2013/10/26. doi: 10.1126/science.1242059 24158908; PubMed Central PMCID: PMC3927313.

126. Wang X, Le TB, Lajoie BR, Dekker J, Laub MT, Rudner DZ. Condensin promotes the juxtaposition of DNA flanking its loading site in Bacillus subtilis. Genes Dev. 2015;29(15):1661–75. Epub 2015/08/09. doi: 10.1101/gad.265876.115 26253537; PubMed Central PMCID: PMC4536313.

127. Dekker J, Heard E. Structural and functional diversity of Topologically Associating Domains. FEBS Lett. 2015;589(20 Pt A):2877–84. Epub 2015/09/09. doi: 10.1016/j.febslet.2015.08.044 26348399; PubMed Central PMCID: PMC4598308.

128. Niki H, Hiraga S. Polar localization of the replication origin and terminus in Escherichia coli nucleoids during chromosome partitioning. Genes Dev. 1998;12(7):1036–45. Epub 1998/05/09. doi: 10.1101/gad.12.7.1036 9531540; PubMed Central PMCID: PMC316681.

129. Niki H, Yamaichi Y, Hiraga S. Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev. 2000;14(2):212–23. Epub 2000/02/01. 10652275; PubMed Central PMCID: PMC316355.

130. Boccard F, Esnault E, Valens M. Spatial arrangement and macrodomain organization of bacterial chromosomes. Mol Microbiol. 2005;57(1):9–16. Epub 2005/06/14. doi: 10.1111/j.1365-2958.2005.04651.x 15948945.

131. Duigou S, Boccard F. 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. 2017;13(5):e1006758. doi: 10.1371/journal.pgen.1006758 28486476; PubMed Central PMCID: PMC5441646.

132. Nolivos S, Upton AL, Badrinarayanan A, Muller J, Zawadzka K, Wiktor J, et al. MatP regulates the coordinated action of topoisomerase IV and MukBEF in chromosome segregation. Nat Commun. 2016;7:10466. Epub 2016/01/29. doi: 10.1038/ncomms10466 26818444; PubMed Central PMCID: PMC4738335.

133. Dupaigne P, Tonthat NK, Espeli O, Whitfill T, Boccard F, Schumacher MA. Molecular Basis for a Protein-Mediated DNA-Bridging Mechanism that Functions in Condensation of the E. coli Chromosome. Molecular Cell. 2012;48(4):560–71. doi: 10.1016/j.molcel.2012.09.009 PubMed PMID: WOS:000311919500009. 23084832

134. Woo JS, Lim JH, Shin HC, Suh MK, Ku B, Lee KH, et al. Structural studies of a bacterial condensin complex reveal ATP-dependent disruption of intersubunit interactions. Cell. 2009;136(1):85–96. doi: 10.1016/j.cell.2008.10.050 19135891.

135. Fennell-Fezzie R, Gradia SD, Akey D, Berger JM. The MukF subunit of Escherichia coli condensin: architecture and functional relationship to kleisins. EMBO J. 2005;24(11):1921–30. doi: 10.1038/sj.emboj.7600680 15902272; PubMed Central PMCID: PMC1142612.

136. Petrushenko ZM, Lai CH, Rybenkov VV. Antagonistic interactions of kleisins and DNA with bacterial Condensin MukB. J Biol Chem. 2006;281(45):34208–17. doi: 10.1074/jbc.M606723200 16982609; PubMed Central PMCID: PMC1634889.

137. Badrinarayanan A, Reyes-Lamothe R, Uphoff S, Leake MC, Sherratt DJ. In vivo architecture and action of bacterial structural maintenance of chromosome proteins. Science. 2012;338(6106):528–31. doi: 10.1126/science.1227126 23112333; PubMed Central PMCID: PMC3807729.

138. Kumar R, Grosbart M, Nurse P, Bahng S, Wyman CL, Marians KJ. The bacterial condensin MukB compacts DNA by sequestering supercoils and stabilizing topologically isolated loops. J Biol Chem. 2017;292(41):16904–20. doi: 10.1074/jbc.M117.803312 28842486; PubMed Central PMCID: PMC5641887.

139. Uhlmann F. SMC complexes: from DNA to chromosomes. Nat Rev Mol Cell Biol. 2016;17(7):399–412. doi: 10.1038/nrm.2016.30 27075410.

140. Melby TE, Ciampaglio CN, Briscoe G, Erickson HP. The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: Long, antiparallel coiled coils, folded at a flexible hinge. Journal of Cell Biology. 1998;142(6):1595–604. doi: 10.1083/jcb.142.6.1595 PubMed PMID: WOS:000076116400016. 9744887

141. Niki H, Imamura R, Kitaoka M, Yamanaka K, Ogura T, Hiraga S. 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. 1992;11(13):5101–9. 1464330; PubMed Central PMCID: PMC556988.

142. Yamazoe M, Onogi T, Sunako Y, Niki H, Yamanaka K, Ichimura T, et al. Complex formation of MukB, MukE and MukF proteins involved in chromosome partitioning in Escherichia coli. EMBO J. 1999;18(21):5873–84. Epub 1999/11/02. doi: 10.1093/emboj/18.21.5873 10545099; PubMed Central PMCID: PMC1171653.

143. Li YY, Stewart NK, Berger AJ, Vos S, Schoeffler AJ, Berger JM, et al. Escherichia coli condensin MukB stimulates topoisomerase IV activity by a direct physical interaction. P Natl Acad Sci USA. 2010;107(44):18832–7. doi: 10.1073/pnas.1008678107 PubMed PMID: WOS:000283749000021. 20921377

144. Nicolas E, Upton AL, Uphoff S, Henry O, Badrinarayanan A, Sherratt D. The SMC complex MukBEF recruits topoisomerase IV to the origin of replication region in live Escherichia coli. MBio. 2014;5(1):e01001–13. doi: 10.1128/mBio.01001-13 24520061; PubMed Central PMCID: PMC3950513.

145. Vos SM, Stewart NK, Oakley MG, Berger JM. Structural basis for the MukB-topoisomerase IV interaction and its functional implications in vivo. EMBO J. 2013;32(22):2950–62. doi: 10.1038/emboj.2013.218 24097060; PubMed Central PMCID: PMC3832749.

146. Zawadzki P, Stracy M, Ginda K, Zawadzka K, Lesterlin C, Kapanidis AN, et al. The Localization and Action of Topoisomerase IV in Escherichia coli Chromosome Segregation Is Coordinated by the SMC Complex, MukBEF. Cell reports. 2015;13(11):2587–96. Epub 2015/12/22. doi: 10.1016/j.celrep.2015.11.034 26686641; PubMed Central PMCID: PMC5061553.

147. Badrinarayanan A, Lesterlin C, Reyes-Lamothe R, Sherratt D. The Escherichia coli SMC complex, MukBEF, shapes nucleoid organization independently of DNA replication. J Bacteriol. 2012;194(17):4669–76. doi: 10.1128/JB.00957-12 22753058; PubMed Central PMCID: PMC3415497.

148. Baxter J, Oliver AW, Schalbetter SA. Are SMC Complexes Loop Extruding Factors? Linking Theory With Fact. Bioessays. 2019;41(1):e1800182. Epub 2018/12/07. doi: 10.1002/bies.201800182 30506702.

149. Zawadzka K, Zawadzki P, Baker R, Rajasekar KV, Wagner F, Sherratt DJ, et al. MukB ATPases are regulated independently by the N- and C-terminal domains of MukF kleisin. Elife. 2018;7. Epub 2018/01/13. doi: 10.7554/eLife.31522 29323635; PubMed Central PMCID: PMC5812716.

150. Sawitzke JA, Austin S. Suppression of chromosome segregation defects of Escherichia coli muk mutants by mutations in topoisomerase I. Proc Natl Acad Sci U S A. 2000;97(4):1671–6. doi: 10.1073/pnas.030528397 10660686; PubMed Central PMCID: PMC26494.

151. Adachi S, Hiraga S. Mutants suppressing novobiocin hypersensitivity of a mukB null mutation. J Bacteriol. 2003;185(13):3690–5. doi: 10.1128/JB.185.13.3690-3695.2003 12813060; PubMed Central PMCID: PMC161581.

152. Petrushenko ZM, Lai CH, Rai R, Rybenkov VV. DNA reshaping by MukB. Right-handed knotting, left-handed supercoiling. J Biol Chem. 2006;281(8):4606–15. doi: 10.1074/jbc.M504754200 16368697; PubMed Central PMCID: PMC1633270.

153. Gaal T, Bratton BP, Sanchez-Vazquez P, Sliwicki A, Sliwicki K, Vegel A, et al. Colocalization of distant chromosomal loci in space in E. coli: a bacterial nucleolus. Genes Dev. 2016;30(20):2272–85. Epub 2016/11/30. doi: 10.1101/gad.290312.116 27898392; PubMed Central PMCID: PMC5110994.

154. Jin DJ, Cabrera JE. Coupling the distribution of RNA polymerase to global gene regulation and the dynamic structure of the bacterial nucleoid in Escherichia coli. J Struct Biol. 2006;156(2):284–91. Epub 2006/08/29. doi: 10.1016/j.jsb.2006.07.005 16934488.

155. Qian Z, Dimitriadis EK, Edgar R, Eswaramoorthy P, Adhya S. Galactose repressor mediated intersegmental chromosomal connections in Escherichia coli. Proc Natl Acad Sci U S A. 2012;109(28):11336–41. doi: 10.1073/pnas.1208595109 22733746; PubMed Central PMCID: PMC3396475.

156. Weickert MJ, Adhya S. The galactose regulon of Escherichia coli. Mol Microbiol. 1993;10(2):245–51. Epub 1993/10/01. doi: 10.1111/j.1365-2958.1993.tb01950.x 7934815.

157. Agerschou ED, Christiansen G, Schafer NP, Madsen DJ, Brodersen DE, Semsey S, et al. The transcriptional regulator GalR self-assembles to form highly regular tubular structures. Sci Rep. 2016;6:27672. Epub 2016/06/10. doi: 10.1038/srep27672 27279285; PubMed Central PMCID: PMC4899725.

158. Bates D, Epstein J, Boye E, Fahrner K, Berg H, Kleckner N. The Escherichia coli baby cell column: a novel cell synchronization method provides new insight into the bacterial cell cycle. Mol Microbiol. 2005;57(2):380–91. doi: 10.1111/j.1365-2958.2005.04693.x 15978072; PubMed Central PMCID: PMC2973562.

159. Kavenoff R, Ryder OA. Electron microscopy of membrane-associated folded chromosomes of Escherichia coli. Chromosoma. 1976;55(1):13–25. doi: 10.1007/bf00288323 767075.

160. Worcel A, Burgi E. Properties of a membrane-attached form of the folded chromosome of Escherichia coli. J Mol Biol. 1974;82(1):91–105. Epub 1974/01/05. doi: 10.1016/0022-2836(74)90576-2 4594427.

161. Roggiani M, Goulian M. Chromosome-Membrane Interactions in Bacteria. Annu Rev Genet. 2015;49:115–29. doi: 10.1146/annurev-genet-112414-054958 26436460.

162. Libby EA, Roggiani M, Goulian M. Membrane protein expression triggers chromosomal locus repositioning in bacteria. Proc Natl Acad Sci U S A. 2012;109(19):7445–50. Epub 2012/04/25. doi: 10.1073/pnas.1109479109 22529375; PubMed Central PMCID: PMC3358875.

163. Brameyer S, Rosch TC, El Andari J, Hoyer E, Schwarz J, Graumann PL, et al. DNA-binding directs the localization of a membrane-integrated receptor of the ToxR family. Commun Biol. 2019;2:4. Epub 2019/02/12. doi: 10.1038/s42003-018-0248-7 30740540; PubMed Central PMCID: PMC6320335.

164. Espeli O, Borne R, Dupaigne P, Thiel A, Gigant E, Mercier R, et al. A MatP-divisome interaction coordinates chromosome segregation with cell division in E. coli. EMBO J. 2012;31(14):3198–211. Epub 2012/05/15. doi: 10.1038/emboj.2012.128 22580828; PubMed Central PMCID: PMC3400007.

165. Bernhardt TG, de Boer PA. SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over Chromosomes in E. coli. Mol Cell. 2005;18(5):555–64. Epub 2005/05/27. doi: 10.1016/j.molcel.2005.04.012 15916962; PubMed Central PMCID: PMC4428309.

166. Almiron M, Link AJ, Furlong D, Kolter R. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 1992;6(12B):2646–54. doi: 10.1101/gad.6.12b.2646 1340475.

167. Frenkiel-Krispin D, Ben-Avraham I, Englander J, Shimoni E, Wolf SG, Minsky A. Nucleoid restructuring in stationary-state bacteria. Mol Microbiol. 2004;51(2):395–405. doi: 10.1046/j.1365-2958.2003.03855.x 14756781.

168. Ball CA, Osuna R, Ferguson KC, Johnson RC. Dramatic Changes in Fis Levels Upon Nutrient Upshift in Escherichia-Coli. Journal of Bacteriology. 1992;174(24):8043–56. PubMed PMID: WOS:A1992KC71900023. doi: 10.1128/jb.174.24.8043-8056.1992 1459953

169. Claret L, Rouviere-Yaniv J. Variation in HU composition during growth of Escherichia coli: the heterodimer is required for long term survival. J Mol Biol. 1997;273(1):93–104. Epub 1997/11/21. doi: 10.1006/jmbi.1997.1310 9367749.

170. Lal A, Dhar A, Trostel A, Kouzine F, Seshasayee AS, Adhya S. Genome scale patterns of supercoiling in a bacterial chromosome. Nat Commun. 2016;7:11055. doi: 10.1038/ncomms11055 27025941; PubMed Central PMCID: PMC4820846.

171. Kar S, Edgar R, Adhya S. Nucleoid remodeling by an altered HU protein: reorganization of the transcription program. Proc Natl Acad Sci U S A. 2005;102(45):16397–402. Epub 2005/11/01. doi: 10.1073/pnas.0508032102 16258062; PubMed Central PMCID: PMC1283455.

172. Lim CJ, Lee SY, Kenney LJ, Yan J. Nucleoprotein filament formation is the structural basis for bacterial protein H-NS gene silencing. Sci Rep. 2012;2:509. doi: 10.1038/srep00509 22798986; PubMed Central PMCID: PMC3396134.

173. Aki T, Choy HE, Adhya S. Histone-like protein HU as a specific transcriptional regulator: co-factor role in repression of gal transcription by GAL repressor. Genes Cells. 1996;1(2):179–88. doi: 10.1046/j.1365-2443.1996.d01-236.x 9140062.

174. Pagel JM, Winkelman JW, Adams CW, Hatfield GW. DNA topology-mediated regulation of transcription initiation from the tandem promoters of the ilvGMEDA operon of Escherichia coli. J Mol Biol. 1992;224(4):919–35. Epub 1992/04/20. doi: 10.1016/0022-2836(92)90460-2 1569580.

175. Parekh BS, Hatfield GW. Transcriptional activation by protein-induced DNA bending: evidence for a DNA structural transmission model. Proc Natl Acad Sci U S A. 1996;93(3):1173–7. Epub 1996/02/06. doi: 10.1073/pnas.93.3.1173 8577735; PubMed Central PMCID: PMC40051.

176. Dorman CJ, Dorman MJ. DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression. Biophysical reviews. 2016;8(3):209–20. Epub 2017/05/17. doi: 10.1007/s12551-016-0205-y 28510224; PubMed Central PMCID: PMC5425793.

177. Chong S, Chen C, Ge H, Xie XS. Mechanism of transcriptional bursting in bacteria. Cell. 2014;158(2):314–26. Epub 2014/07/19. doi: 10.1016/j.cell.2014.05.038 25036631; PubMed Central PMCID: PMC4105854.

178. Peter BJ, Arsuaga J, Breier AM, Khodursky AB, Brown PO, Cozzarelli NR. Genomic transcriptional response to loss of chromosomal supercoiling in Escherichia coli. Genome Biol. 2004;5(11):R87. Epub 2004/11/13. doi: 10.1186/gb-2004-5-11-r87 15535863; PubMed Central PMCID: PMC545778.

179. Berger M, Farcas A, Geertz M, Zhelyazkova P, Brix K, Travers A, et al. Coordination of genomic structure and transcription by the main bacterial nucleoid-associated protein HU. EMBO reports. 2010;11(1):59–64. Epub 2009/12/17. doi: 10.1038/embor.2009.232 20010798; PubMed Central PMCID: PMC2816637.

180. Berger M, Gerganova V, Berger P, Rapiteanu R, Lisicovas V, Dobrindt U. Genes on a Wire: The Nucleoid-Associated Protein HU Insulates Transcription Units in Escherichia coli. Sci Rep. 2016;6:31512. doi: 10.1038/srep31512 27545593; PubMed Central PMCID: PMC4992867.

181. Koli P, Sudan S, Fitzgerald D, Adhya S, Kar S. Conversion of commensal Escherichia coli K-12 to an invasive form via expression of a mutant histone-like protein. MBio. 2011;2(5). Epub 2011/09/08. doi: 10.1128/mBio.00182-11 21896677; PubMed Central PMCID: PMC3172693.

182. Kar S, Choi EJ, Guo F, Dimitriadis EK, Kotova SL, Adhya S. Right-handed DNA supercoiling by an octameric form of histone-like protein HU: modulation of cellular transcription. J Biol Chem. 2006;281(52):40144–53. Epub 2006/10/26. doi: 10.1074/jbc.M605576200 17062578.

183. Vanhecke D, Graber W, Studer D. Close-to-native ultrastructural preservation by high pressure freezing. Method Cell Biol. 2008;88:151–64. doi: 10.1016/S0091-679x(08)00409-3 PubMed PMID: WOS:000257693100009.

184. Ou HD, Phan S, Deerinck TJ, Thor A, Ellisman MH, O'Shea CC. ChromEMT: Visualizing 3D chromatin structure and compaction in interphase and mitotic cells. Science. 2017;357(6349). doi: 10.1126/science.aag0025 28751582.

185. Narayan K, Subramaniam S. Focused ion beams in biology. Nat Methods. 2015;12(11):1021–31. Epub 2015/10/30. doi: 10.1038/nmeth.3623 26513553.