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Biophysical Reviews

, Volume 8, Supplement 1, pp 89–100 | Cite as

DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression

  • Charles J. Dorman
  • Matthew J. Dorman
Review

Abstract

Although it has become routine to consider DNA in terms of its role as a carrier of genetic information, it is also an important contributor to the control of gene expression. This regulatory principle arises from its structural properties. DNA is maintained in an underwound state in most bacterial cells and this has important implications both for DNA storage in the nucleoid and for the expression of genetic information. Underwinding of the DNA through reduction in its linking number potentially imparts energy to the duplex that is available to drive DNA transactions, such as transcription, replication and recombination. The topological state of DNA also influences its affinity for some DNA binding proteins, especially in DNA sequences that have a high A + T base content. The underwinding of DNA by the ATP-dependent topoisomerase DNA gyrase creates a continuum between metabolic flux, DNA topology and gene expression that underpins the global response of the genome to changes in the intracellular and external environments. These connections describe a fundamental and generalised mechanism affecting global gene expression that underlies the specific control of transcription operating through conventional transcription factors. This mechanism also provides a basal level of control for genes acquired by horizontal DNA transfer, assisting microbial evolution, including the evolution of pathogenic bacteria.

Keywords

DNA supercoiling DNA topoisomerases Transcription Gene regulation 

Notes

Acknowledgements

This work was supported by Science Foundation Ireland Principal Investigator Award 13/IA/1875.

Compliance with ethical standards

Conflict of interest

Charles J. Dorman declares that he has no conflict of interest.

Matthew J. Dorman declares that he has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Ahmed W, Menon S, Karthik PVDNB, Nagaraja V (2016) Autoregulation of topoisomerase I expression by supercoiling sensitive transcription. Nucleic Acids Res 44:1541–1552PubMedCrossRefGoogle Scholar
  2. Alanazi AM, Neidle EL, Momany C (2013) The DNA-binding domain of BenM reveals the structural basis for the recognition of a T-N11-A sequence motif by LysR-type transcriptional regulators. Acta Crystallogr D Biol Crystallogr 69:1995–2007PubMedCrossRefGoogle Scholar
  3. Alice AF, Sanchez-Rivas C (1997) DNA supercoiling and osmoresistance in Bacillus subtilis 168. Curr Microbiol 35:309–315PubMedCrossRefGoogle Scholar
  4. Aubry A, Pan XS, Fisher LM, Jarlier V, Cambau E (2004) Mycobacterium tuberculosis DNA gyrase: interaction with quinolones and correlation with antimycobacterial drug activity. Antimicrob Agents Chemother 48:1281–1288PubMedPubMedCentralCrossRefGoogle Scholar
  5. Balke VL, Gralla JD (1987) Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli. J Bacteriol 169:4499–4506PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bang IS, Audia JP, Park YK, Foster JW (2002) Autoinduction of the ompR response regulator by acid shock and control of the Salmonella enterica acid tolerance response. Mol Microbiol 44:1235–1250PubMedCrossRefGoogle Scholar
  7. Bates AD, Maxwell A (2007) Energy coupling in type II topoisomerases: why do they hydrolyze ATP? Biochemistry 46:7929–7941PubMedCrossRefGoogle Scholar
  8. Bauer WR, Crick FHC, White JH (1980) Supercoiled DNA. Sci Am 243:100–113PubMedGoogle Scholar
  9. Bebbington KJ, Williams HD (2001) A role for DNA supercoiling in the regulation of the cytochrome bd oxidase of Escherichia coli. Microbiology 147:591–598PubMedCrossRefGoogle Scholar
  10. Beltrametti F, Kresse AU, Guzmán CA (1999) Transcriptional regulation of the esp genes of enterohemorrhagic Escherichia coli. J Bacteriol 181:3409–3418PubMedPubMedCentralGoogle Scholar
  11. Bliska JB, Cozzarelli NR (1987) Use of site-specific recombination as a probe of DNA structure and metabolism in vivo. J Mol Biol 194:238–218CrossRefGoogle Scholar
  12. Bohrer CH, Roberts E (2016) A biophysical model of supercoiling dependent transcription predicts a structural aspect to gene regulation. BMC Biophys 9:2PubMedPubMedCentralCrossRefGoogle Scholar
  13. Boles TC, White JH, Cozzarelli NR (1990) Structure of plectonemically supercoiled DNA. J Mol Biol 213:931–951PubMedCrossRefGoogle Scholar
  14. Booker BM, Deng S, Higgins NP (2010) DNA topology of highly transcribed operons in Salmonella enterica serovar Typhimurium. Mol Microbiol 78:1348–1364PubMedCrossRefGoogle Scholar
  15. Bordes P, Conter A, Morales V, Bouvier J, Kolb A, Gutierrez C (2003) DNA supercoiling contributes to disconnect sigmaS accumulation from sigmaS-dependent transcription in Escherichia coli. Mol Microbiol 48:561–571PubMedCrossRefGoogle Scholar
  16. 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 14:441–448PubMedCrossRefGoogle Scholar
  17. Brambilla E, Sclavi B (2015) Gene regulation by H-NS as a function of growth conditions depends on chromosomal position in Escherichia coli. G3 (Bethesda) 5:605–614CrossRefGoogle Scholar
  18. Brennan RG (1993) The winged-helix DNA-binding motif: another helix-turn-helix takeoff. Cell 74:773–776PubMedCrossRefGoogle Scholar
  19. Bryant JA, Sellars LE, Busby SJ, Lee DJ (2014) Chromosome position effects on gene expression in Escherichia coli K-12. Nucleic Acids Res 42:11383–11392PubMedPubMedCentralCrossRefGoogle Scholar
  20. Cameron AD, Dorman CJ (2012) A fundamental regulatory mechanism operating through OmpR and DNA topology controls expression of Salmonella pathogenicity islands SPI-1 and SPI-2. PLoS Genet 8, e1002615PubMedPubMedCentralCrossRefGoogle Scholar
  21. Cameron AD, Stoebel DM, Dorman CJ (2011) DNA supercoiling is differentially regulated by environmental factors and FIS in Escherichia coli and Salmonella enterica. Mol Microbiol 80:85–101PubMedCrossRefGoogle Scholar
  22. Cameron AD, Kröger C, Quinn HJ, Scally IK, Daly AJ, Kary SC, Dorman CJ (2013) Transmission of an oxygen availability signal at the Salmonella enterica serovar Typhimurium fis promoter. PLoS One 8, e84382PubMedPubMedCentralCrossRefGoogle Scholar
  23. Caramel A, Schnetz K (1998) Lac and Lambda repressors relieve silencing of the Escherichia coli bgl promoter. Activation by alteration of a repressing nucleoprotein complex. J Mol Biol 284:875–883PubMedCrossRefGoogle Scholar
  24. Champion K, Higgins NP (2007) Growth rate toxicity phenotypes and homeostatic supercoil control differentiate Escherichia coli from Salmonella enterica serovar Typhimurium. J Bacteriol 189:5839–5849PubMedPubMedCentralCrossRefGoogle Scholar
  25. Chen CC, Wu HY (2005) LeuO protein delimits the transcriptionally active and repressive domains on the bacterial chromosome. J Biol Chem 280:15111–15121PubMedCrossRefGoogle Scholar
  26. Chen D, Bowater R, Dorman CJ, Lilley DM (1992) Activity of a plasmid-borne leu-500 promoter depends on the transcription and translation of an adjacent gene. Proc Natl Acad Sci U S A 89:8784–8788PubMedPubMedCentralCrossRefGoogle Scholar
  27. Chen CC, Ghole M, Majumder A, Wang Z, Chandana S, Wu HY (2003) LeuO-mediated transcriptional derepression. J Biol Chem 278:38094–38103PubMedCrossRefGoogle Scholar
  28. Chen CC, Chou MY, Huang CH, Majumder A, Wu HY (2005) A cis-spreading nucleoprotein filament is responsible for the gene silencing activity found in the promoter relay mechanism. J Biol Chem 280:5101–5112PubMedCrossRefGoogle Scholar
  29. Cheung KJ, Badarinarayana V, Selinger DW, Janse D, Church GM (2003) A microarray-based antibiotic screen identifies a regulatory role for supercoiling in the osmotic stress response of Escherichia coli. Genome Res 13:206–215PubMedPubMedCentralCrossRefGoogle Scholar
  30. Chiu TP, Yang L, Zhou T, Main BJ, Parker SC, Nuzhdin SV, Tullius TD, Rohs R (2015) GBshape: a genome browser database for DNA shape annotations. Nucleic Acids Res 43:D103–D109PubMedCrossRefGoogle Scholar
  31. Chong S, Chen C, Ge H, Xie XS (2014) Mechanism of transcriptional bursting in bacteria. Cell 158:314–326PubMedPubMedCentralCrossRefGoogle Scholar
  32. Conter A, Menchon C, Gutierrez C (1997) Role of DNA supercoiling and rpoS sigma factor in the osmotic and growth phase-dependent induction of the gene osmE of Escherichia coli K12. J Mol Biol 273:75–83PubMedCrossRefGoogle Scholar
  33. Cordeiro TN, Schmidt H, Madrid C, Juárez A, Bernadó P, Griesinger C, García J, Pons M (2011) Indirect DNA readout by an H-NS related protein: structure of the DNA complex of the C-terminal domain of Ler. PLoS Pathog 7, e1002380PubMedPubMedCentralCrossRefGoogle Scholar
  34. Cortassa S, Aon MA (1993) Altered topoisomerase activities may be involved in the regulation of DNA supercoiling in aerobic-anaerobic transitions in Escherichia coli. Mol Cell Biochem 126:115–124PubMedCrossRefGoogle Scholar
  35. Cotter PA, DiRita VJ (2000) Bacterial virulence gene regulation: an evolutionary perspective. Annu Rev Microbiol 54:519–565PubMedCrossRefGoogle Scholar
  36. Dame RT, Noom MC, Wuite GJ (2006) Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature 444:387–390PubMedCrossRefGoogle Scholar
  37. Dedieu L, Pagès JM, Bolla JM (2002) Environmental regulation of Campylobacter jejuni major outer membrane protein porin expression in Escherichia coli monitored by using green fluorescent protein. Appl Environ Microbiol 68:4209–4215PubMedPubMedCentralCrossRefGoogle Scholar
  38. Dekker NH, Rybenkov VV, Duguet M, Crisona NJ, Cozzarelli NR, Bensimon D, Croquette V (2002) The mechanism of type IA topoisomerases. Proc Natl Acad Sci U S A 99:12126–12131PubMedPubMedCentralCrossRefGoogle Scholar
  39. Dillon SC, Cameron AD, Hokamp K, Lucchini S, Hinton JC, Dorman CJ (2010) Genome-wide analysis of the H-NS and Sfh regulatory networks in Salmonella Typhimurium identifies a plasmid-encoded transcription silencing mechanism. Mol Microbiol 76:1250–1265PubMedCrossRefGoogle Scholar
  40. Dillon SC, Espinosa E, Hokamp K, Ussery DW, Casadesús J, Dorman CJ (2012) LeuO is a global regulator of gene expression in Salmonella enterica serovar Typhimurium. Mol Microbiol 85:1072–1089PubMedCrossRefGoogle Scholar
  41. Ding Y, Manzo C, Fulcrand G, Leng F, Dunlap D, Finzi L (2014) DNA supercoiling: a regulatory signal for the λ repressor. Proc Natl Acad Sci U S A 111:15402–15407PubMedPubMedCentralCrossRefGoogle Scholar
  42. Dixon RA, Henderson NC, Austin S (1988) DNA supercoiling and aerobic regulation of transcription from the Klebsiella pneumoniae nifLA promoter. Nucleic Acids Res 16:9933–9946PubMedPubMedCentralCrossRefGoogle Scholar
  43. Dolan KT, Duguid EM, He C (2011) Crystal structures of SlyA protein, a master virulence regulator of Salmonella, in free and DNA-bound states. J Biol Chem 286:22178–22185PubMedPubMedCentralCrossRefGoogle Scholar
  44. Dorman CJ (1991) DNA supercoiling and environmental regulation of gene expression in pathogenic bacteria. Infect Immun 59:745–749PubMedPubMedCentralGoogle Scholar
  45. Dorman CJ (2006) DNA supercoiling and bacterial gene expression. Sci Prog 89:151–166PubMedCrossRefGoogle Scholar
  46. Dorman CJ (2007) H-NS, the genome sentinel. Nat Rev Microbiol 5:157–161PubMedCrossRefGoogle Scholar
  47. Dorman CJ (2013) Genome architecture and global gene regulation in bacteria: making progress towards a unified model? Nat Rev Microbiol 11:349–355PubMedCrossRefGoogle Scholar
  48. Dorman CJ, Corcoran CP (2009) Bacterial DNA topology and infectious disease. Nucleic Acids Res 37:672–678PubMedCrossRefGoogle Scholar
  49. Dorman CJ, Barr GC, Ní Bhriain N, Higgins CF (1988) DNA supercoiling and the anaerobic and growth phase regulation of tonB gene expression. J Bacteriol 170:2816–2826PubMedPubMedCentralCrossRefGoogle Scholar
  50. Dorman CJ, Ni Bhriain N, Higgins CF (1990) DNA supercoiling and environmental regulation of virulence gene expression in Shigella flexneri. Nature 344:789–792PubMedCrossRefGoogle Scholar
  51. Drolet M (2006) Growth inhibition mediated by excess negative supercoiling: the interplay between transcription elongation, R-loop formation and DNA topology. Mol Microbiol 59:723–730PubMedCrossRefGoogle Scholar
  52. El Hanafi D, Bossi L (2000) Activation and silencing of leu-500 promoter by transcription-induced DNA supercoiling in the Salmonella chromosome. Mol Microbiol 37:583–594PubMedCrossRefGoogle Scholar
  53. Fang M, Wu HY (1998a) A promoter relay mechanism for sequential gene activation. J Bacteriol 180:626–633PubMedPubMedCentralGoogle Scholar
  54. Fang M, Wu HY (1998b) Suppression of leu-500 mutation in topA+ Salmonella typhimurium strains. The promoter relay at work. J Biol Chem 273:29929–29934PubMedCrossRefGoogle Scholar
  55. Fass E, Groisman EA (2009) Control of Salmonella pathogenicity island-2 gene expression. Curr Opin Microbiol 12:199–204PubMedPubMedCentralCrossRefGoogle Scholar
  56. Feng X, Walthers D, Oropeza R, Kenney LJ (2004) The response regulator SsrB activates transcription and binds to a region overlapping OmpR binding sites at Salmonella pathogenicity island 2. Mol Microbiol 54:823–835PubMedCrossRefGoogle Scholar
  57. Fitzgerald S, Dillon SC, Chao TC, Wiencko HL, Hokamp K, Cameron AD, Dorman CJ (2015) Re-engineering cellular physiology by rewiring high-level global regulatory genes. Sci Rep 5:17653. doi: 10.1038/srep17653 PubMedPubMedCentralCrossRefGoogle Scholar
  58. Fournier B, Klier A (2004) Protein A gene expression is regulated by DNA supercoiling which is modified by the ArlS-ArlR two-component system of Staphylococcus aureus. Microbiology 150:3807–3819PubMedCrossRefGoogle Scholar
  59. Friedman SB, Margolin P (1968) Evidence for an altered operator specificity: catabolite repression control of the leucine operon in Salmonella typhimurium. J Bacteriol 95:2263–2269PubMedPubMedCentralGoogle Scholar
  60. Fulcrand G, Dages S, Zhi X, Chapagain P, Gerstman BS, Dunlap D, Leng F (2016) DNA supercoiling, a critical signal regulating the basal expression of the lac operon in Escherichia coli. Sci Rep 6:19243. doi: 10.1038/srep19243 PubMedPubMedCentralCrossRefGoogle Scholar
  61. Galán JE, Curtiss R 3rd (1990) Expression of Salmonella typhimurium genes required for invasion is regulated by changes in DNA supercoiling. Infect Immun 58:1879–1885PubMedPubMedCentralGoogle Scholar
  62. Gellert M, Mizuuchi K, O’Dea MH, Nash HA (1976) DNA gyrase: an enzyme that introduces superhelical turns into DNA. Proc Natl Acad Sci U S A 73:3872–3876PubMedPubMedCentralCrossRefGoogle Scholar
  63. Gerganova V, Berger M, Zaldastanishvili E, Sobetzko P, Lafon C, Mourez M, Travers A, Muskhelishvili G (2015) Chromosomal position shift of a regulatory gene alters the bacterial phenotype. Nucleic Acids Res 43:8215–8226PubMedPubMedCentralCrossRefGoogle Scholar
  64. Goldstein E, Drlica K (1984) Regulation of bacterial DNA supercoiling: plasmid linking numbers vary with growth temperature. Proc Natl Acad Sci U S A 81:4046–4050PubMedPubMedCentralCrossRefGoogle Scholar
  65. Graeff-Wohlleben H, Deppisch H, Gross R (1995) Global regulatory mechanisms affect virulence gene expression in Bordetella pertussis. Mol Gen Genet 247:86–94PubMedCrossRefGoogle Scholar
  66. Graf LH Jr, Burns RO (1973) The supX-leu-500 mutations and expression of the leucine operon. Mol Gen Genet 126:291–301PubMedCrossRefGoogle Scholar
  67. Groisman EA, Casadesús J (2005) The origin and evolution of human pathogens. Mol Microbiol 56:1–7PubMedCrossRefGoogle Scholar
  68. Guadarrama C, Medrano-López A, Oropeza R, Hernández-Lucas I, Calva E (2014) The Salmonella enterica serovar Typhi LeuO global regulator forms tetramers: residues involved in oligomerization, DNA binding, and transcriptional regulation. J Bacteriol 196:2143–2154PubMedPubMedCentralCrossRefGoogle Scholar
  69. Hardy CD, Cozzarelli NR (2003) Alteration of Escherichia coli topoisomerase IV to novobiocin resistance. Antimicrob Agents Chemother 47:941–947PubMedPubMedCentralCrossRefGoogle Scholar
  70. Harms A, Stanger FV, Scheu PD, de Jong IG, Goepfert A, Glatter T, Gerdes K, Schirmer T, Dehio C (2015) Adenylylation of gyrase and Topo IV by FicT toxins disrupts bacterial DNA topology. Cell Rep 12:1497–1507PubMedCrossRefGoogle Scholar
  71. Haughn GW, Wessler SR, Gemmill RM, Calvo JM (1986) High A + T content conserved in DNA sequences upstream of leuABCD in Escherichia coli and Salmonella typhimurium. J Bacteriol 166:1113–1117PubMedPubMedCentralCrossRefGoogle Scholar
  72. Hay AJ, Zhu J (2015) Host intestinal signal-promoted biofilm dispersal induces Vibrio cholerae colonization. Infect Immun 83:317–323PubMedCrossRefGoogle Scholar
  73. Hérault E, Reverchon S, Nasser W (2014) Role of the LysR-type transcriptional regulator PecT and DNA supercoiling in the thermoregulation of pel genes, the major virulence factors in Dickeya dadantii. Environ Microbiol 16:734–745PubMedCrossRefGoogle Scholar
  74. Higashi K, Tobe T, Kanai A, Uyar E, Ishikawa S, Suzuki Y, Ogasawara N, Kurokawa K, Oshima T (2016) H-NS facilitates sequence diversification of horizontally transferred DNAs during their integration in host chromosomes. PLoS Genet 12, e1005796PubMedPubMedCentralCrossRefGoogle Scholar
  75. Higgins NP (2014) RNA polymerase: chromosome domain boundary maker and regulator of supercoil density. Curr Opin Microbiol 22:138–143PubMedPubMedCentralCrossRefGoogle Scholar
  76. Higgins NP, Vologodskii AV (2015) Topological behavior of plasmid DNA. Microbiol Spectr 3(2). doi:  10.1128/microbiolspec.PLAS-0036-2014
  77. Higgins NP, Peebles CL, Sugino A, Cozzarelli NR (1978) Purification of subunits of Escherichia coli DNA gyrase and reconstitution of enzymatic activity. Proc Natl Acad Sci U S A 75:1773–1777PubMedPubMedCentralCrossRefGoogle Scholar
  78. Higgins CF, Dorman CJ, Stirling DA, Waddell L, Booth IR, May G, Bremer E (1988) A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell 52:569–584PubMedCrossRefGoogle Scholar
  79. Hsieh LS, Burger RM, Drlica K (1991a) Bacterial DNA supercoiling and [ATP]/[ADP]. Changes associated with a transition to anaerobic growth. J Mol Biol 219:443–450PubMedCrossRefGoogle Scholar
  80. Hsieh LS, Rouviere-Yaniv J, Drlica K (1991b) Bacterial DNA supercoiling and [ATP]/[ADP] ratio: changes associated with salt shock. J Bacteriol 173:3914–3917PubMedPubMedCentralCrossRefGoogle Scholar
  81. Jain P, Nagaraja V (2005) An atypical type II topoisomerase from Mycobacterium smegmatis with positive supercoiling activity. Mol Microbiol 58:1392–1405PubMedCrossRefGoogle Scholar
  82. Karem K, Foster JW (1993) The influence of DNA topology on the environmental regulation of a pH-regulated locus in Salmonella typhimurium. Mol Microbiol 10:75–86PubMedCrossRefGoogle Scholar
  83. Kato J, Nishimura Y, Imamura R, Niki H, Hiraga S, Suzuki H (1990) New topoisomerase essential for chromosome segregation in E. coli. Cell 63:393–404PubMedCrossRefGoogle Scholar
  84. Kenney LJ (2002) Structure/function relationships in OmpR and other winged-helix transcription factors. Curr Opin Microbiol 5:135–141PubMedCrossRefGoogle Scholar
  85. Khodursky AB, Zechiedrich EL, Cozzarelli NR (1995) Topoisomerase IV is a target of quinolones in Escherichia coli. Proc Natl Acad Sci U S A 92:11801–11805PubMedPubMedCentralCrossRefGoogle Scholar
  86. Koster DA, Crut A, Shuman S, Bjornsti M-A, Dekker NH (2010) Cellular strategies for regulating DNA supercoiling: a single-molecule perspective. Cell 142:519–530PubMedPubMedCentralCrossRefGoogle Scholar
  87. Kotlajich MV, Hron DR, Boudreau BA, Sun Z, Lyubchenko YL, Landick R (2015) Bridged filaments of histone-like nucleoid structuring protein pause RNA polymerase and aid termination in bacteria. Elife 4 doi:  10.7554/eLife.04970
  88. Kouzine F, Sanford S, Elisha-Feil Z, Levens D (2008) The functional response of upstream DNA to dynamic supercoiling in vivo. Nat Struct Mol Biol 15:146–154PubMedCrossRefGoogle Scholar
  89. Kravatskaya GI, Chechetkin VR, Kravatsky YV, Tumanyan VG (2013) Structural attributes of nucleotide sequences in promoter regions of supercoiling-sensitive genes: how to relate microarray expression data with genomic sequences. Genomics 101:1–11PubMedCrossRefGoogle Scholar
  90. Lang B, Blot N, Bouffartigues E, Buckle M, Geertz M, Gualerzi CO, Mavathur R, Muskhelishvili G, Pon CL, Rimsky S, Stella S, Babu MM, Travers A (2007) High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res 35:6330–6337PubMedPubMedCentralCrossRefGoogle Scholar
  91. Leclerc GJ, Tartera C, Metcalf ES (1998) Environmental regulation of Salmonella typhi invasion-defective mutants. Infect Immun 66:682–691PubMedPubMedCentralGoogle Scholar
  92. Leng F, McMacken R (2002) Potent stimulation of transcription-coupled DNA supercoiling by sequence-specific DNA-binding proteins. Proc Natl Acad Sci U S A 99:9139–9144PubMedPubMedCentralCrossRefGoogle Scholar
  93. Lewis M (2011) A tale of two repressors. J Mol Biol 409:14–27PubMedPubMedCentralCrossRefGoogle Scholar
  94. Liebart JC, Paolozzi L, Camera MG, Pedrini AM, Ghelardini P (1989) The expression of the DNA ligase gene of Escherichia coli is stimulated by relaxation of chromosomal supercoiling. Mol Microbiol 3:269–273PubMedCrossRefGoogle Scholar
  95. Lilley DM, Higgins CF (1991) Local DNA topology and gene expression: the case of the leu-500 promoter. Mol Microbiol 5:779–783PubMedCrossRefGoogle Scholar
  96. Liu LF, Wang JC (1987) Supercoiling of the DNA template during transcription. Proc Natl Acad Sci U S A 84:7024–7027PubMedPubMedCentralCrossRefGoogle Scholar
  97. Lucchini S, Rowley G, Goldberg MD, Hurd D, Harrison M, Hinton JC (2006) H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog 2, e81PubMedPubMedCentralCrossRefGoogle Scholar
  98. Ma J, Wang M (2014a) Interplay between DNA supercoiling and transcription elongation. Transcription 5, e28636PubMedPubMedCentralCrossRefGoogle Scholar
  99. Ma J, Wang MD (2014b) RNA polymerase is a powerful torsional motor. Cell Cycle 13:337–338PubMedCrossRefGoogle Scholar
  100. Ma J, Bai L, Wang MD (2013) Transcription under torsion. Science 340:1580–1583PubMedCrossRefGoogle Scholar
  101. Malkhosyan SR, Panchenko YuA, Rekesh AN (1991) A physiological role for DNA supercoiling in the anaerobic regulation of colicin gene expression. Mol Gen Genet 225:342–345PubMedCrossRefGoogle Scholar
  102. Margolin P, Zumstein L, Sternglanz R, Wang JC (1985) The Escherichia coli supX locus is topA, the structural gene for DNA topoisomerase I. Proc Natl Acad Sci U S A 82:5437–5441PubMedPubMedCentralCrossRefGoogle Scholar
  103. Martínez-Hackert E, Stock AM (1997) Structural relationships in the OmpR family of winged-helix transcription factors. J Mol Biol 269:301–312PubMedCrossRefGoogle Scholar
  104. Maurer S, Fritz J, Muskhelishvili G (2009) A systematic in vitro study of nucleoprotein complexes formed by bacterial nucleoid-associated proteins revealing novel types of DNA organization. J Mol Biol 387:1261–1276PubMedCrossRefGoogle Scholar
  105. McGovern V, Higgins NP, Chiz RS, Jaworski A (1994) H-NS over-expression induces an artificial stationary phase by silencing global transcription. Biochimie 76:1019–10129PubMedCrossRefGoogle Scholar
  106. Menzel R, Gellert M (1983) Regulation of the genes for E. coli DNA gyrase: homeostatic control of DNA supercoiling. Cell 34:105–113PubMedCrossRefGoogle Scholar
  107. Menzel R, Gellert M (1987) Modulation of transcription by DNA supercoiling: a deletion analysis of the Escherichia coli gyrA and gyrB promoters. Proc Natl Acad Sci U S A 84:4185–4189PubMedPubMedCentralCrossRefGoogle Scholar
  108. Merrell DS, Butler SM, Qadri F, Dolganov NA, Alam A, Cohen MB, Calderwood SB, Schoolnik GK, Camilli A (2002) Host-induced epidemic spread of the cholera bacterium. Nature 417:642–645PubMedPubMedCentralCrossRefGoogle Scholar
  109. Meury J, Kohiyama M (1992) Potassium ions and changes in bacterial DNA supercoiling under osmotic stress. FEMS Microbiol Lett 78:159–164PubMedCrossRefGoogle Scholar
  110. Naughton C, Corless S, Gilbert N (2013) Divergent RNA transcription: a role in promoter unwinding? Transcription 4:162–166PubMedPubMedCentralCrossRefGoogle Scholar
  111. Navarre WW, Porwollik S, Wang Y, McClelland M, Rosen H, Libby SJ, Fang FC (2006) Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313:236–238PubMedCrossRefGoogle Scholar
  112. Niehus E, Cheng E, Tan M (2008) DNA supercoiling-dependent gene regulation in Chlamydia. J Bacteriol 190:6419–6427PubMedPubMedCentralCrossRefGoogle Scholar
  113. Noom MC, Navarre WW, Oshima T, Wuite GJ, Dame RT (2007) H-NS promotes looped domain formation in the bacterial chromosome. Curr Biol 17:R913–R914PubMedCrossRefGoogle Scholar
  114. Nurse P, Levine C, Hassing H, Marians KJ (2003) Topoisomerase III can serve as the cellular decatenase in Escherichia coli. J Biol Chem 278:8653–8660PubMedCrossRefGoogle Scholar
  115. Ó Cróinín T, Carroll RK, Kelly A, Dorman CJ (2006) Roles for DNA supercoiling and the Fis protein in modulating expression of virulence genes during intracellular growth of Salmonella enterica serovar Typhimurium. Mol Microbiol 62:869–882PubMedCrossRefGoogle Scholar
  116. O’Byrne CP, Ní Bhriain N, Dorman CJ (1992) The DNA supercoiling-sensitive expression of the Salmonella typhimurium his operon requires the his attenuator and is modulated by anaerobiosis and by osmolarity. Mol Microbiol 6:2467–2476PubMedCrossRefGoogle Scholar
  117. Oguey C, Foloppe N, Hartmann B (2010) Understanding the sequence-dependence of DNA groove dimensions: implications for DNA interactions. PLoS One 5, e15931PubMedPubMedCentralCrossRefGoogle Scholar
  118. Opel ML, Hatfield GW (2001) DNA supercoiling-dependent transcriptional coupling between the divergently transcribed promoters of the ilvYC operon of Escherichia coli is proportional to promoter strengths and transcript lengths. Mol Microbiol 39:191–198PubMedCrossRefGoogle Scholar
  119. Oppenheim AB, Kobiler O, Stavans J, Court DL, Adhya S (2005) Switches in bacteriophage lambda development. Annu Rev Genet 39:409–429PubMedCrossRefGoogle Scholar
  120. Oshima T, Ishikawa S, Kurokawa K, Aiba H, Ogasawara N (2006) Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase. DNA Res 13:141–153PubMedCrossRefGoogle Scholar
  121. Parsot C, Mekalanos JJ (1992) Structural analysis of the acfA and acfD genes of Vibrio cholerae: effects of DNA topology and transcriptional activators on expression. J Bacteriol 174:5211–5218PubMedPubMedCentralCrossRefGoogle Scholar
  122. Perez-Cheeks BA, Lee C, Hayama R, Marians KJ (2012) A role for topoisomerase III in Escherichia coli chromosome segregation. Mol Microbiol 86:1007–1022PubMedPubMedCentralCrossRefGoogle Scholar
  123. Pettijohn DE, Pfenninger O (1980) Supercoils in prokaryotic DNA restrained in vivo. Proc Natl Acad Sci U S A 77:1331–1335PubMedPubMedCentralCrossRefGoogle Scholar
  124. Porwollik S, McClelland M (2003) Lateral gene transfer in Salmonella. Microbes Infect 5:977–989PubMedCrossRefGoogle Scholar
  125. Pruss GJ, Drlica K (1985) DNA supercoiling and suppression of the leu-500 promoter mutation. J Bacteriol 164:947–949PubMedPubMedCentralGoogle Scholar
  126. Quinn HJ, Cameron AD, Dorman CJ (2014) Bacterial regulon evolution: distinct responses and roles for the identical OmpR proteins of Salmonella Typhimurium and Escherichia coli in the acid stress response. PLoS Genet 10, e1004215PubMedPubMedCentralCrossRefGoogle Scholar
  127. Rahmouni AR, Wells RD (1992) Direct evidence for the effect of transcription on local DNA supercoiling in vivo. J Mol Biol 223:131–144PubMedCrossRefGoogle Scholar
  128. Rhee KY, Opel M, Ito E, Hung Sp, Arfin SM, Hatfield GW (1999) Transcriptional coupling between the divergent promoters of a prototypic LysR-type regulatory system, the ilvYC operon of Escherichia coli. Proc Natl Acad Sci U S A 96:14294–14299PubMedPubMedCentralCrossRefGoogle Scholar
  129. Richardson SM, Higgins CF, Lilley DM (1984) The genetic control of DNA supercoiling in Salmonella typhimurium. EMBO J 3:1745–1752PubMedPubMedCentralGoogle Scholar
  130. Richardson SM, Higgins CF, Lilley DM (1988) DNA supercoiling and the leu-500 promoter mutation of Salmonella typhimurium. EMBO J 7:1863–1869PubMedPubMedCentralGoogle Scholar
  131. Rohde JR, Fox JM, Minnich SA (1994) Thermoregulation in Yersinia enterocolitica is coincident with changes in DNA supercoiling. Mol Microbiol 12:187–199PubMedCrossRefGoogle Scholar
  132. Rohs R, West SM, Sosinsky A, Liu P, Mann RS, Honig B (2009) The role of DNA shape in protein-DNA recognition. Nature 461:1248–1253PubMedPubMedCentralCrossRefGoogle Scholar
  133. 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, e1002845PubMedPubMedCentralCrossRefGoogle Scholar
  134. Sánchez-Céspedes J, Sáez-López E, Frimodt-Møller N, Vila J, Soto SM (2015) Effects of a mutation in the gyrA Gene on the virulence of uropathogenic Escherichia coli. Antimicrob Agents Chemother 59:4662–4668PubMedPubMedCentralCrossRefGoogle Scholar
  135. Schell MA (1993) Molecular biology of the LysR family of transcriptional regulators. Annu Rev Microbiol 47:597–626PubMedCrossRefGoogle Scholar
  136. Schleif RF (2013) Modulation of DNA binding by gene-specific transcription factors. Biochemistry 52:6755–6765PubMedCrossRefGoogle Scholar
  137. Schröder W, Bernhardt J, Marincola G, Klein-Hitpass L, Herbig A, Krupp G, Nieselt K, Wolz C (2014) Altering gene expression by aminocoumarins: the role of DNA supercoiling in Staphylococcus aureus. BMC Genomics 15:291PubMedPubMedCentralCrossRefGoogle Scholar
  138. Semsey S, Virnik K, Adhya S (2005) A gamut of loops: meandering DNA. Trends Biochem Sci 30:334–341PubMedCrossRefGoogle Scholar
  139. Sheehan BJ, Dorman CJ (1998) In vivo analysis of the interactions of the LysR-like regulator SpvR with the operator sequences of the spvA and spvR virulence genes of Salmonella typhimurium. Mol Microbiol 30:91–105PubMedCrossRefGoogle Scholar
  140. Sheehan BJ, Foster TJ, Dorman CJ, Park S, Stewart GS (1992) Osmotic and growth-phase dependent regulation of the eta gene of Staphylococcus aureus: a role for DNA supercoiling. Mol Gen Genet 232:49–57PubMedCrossRefGoogle Scholar
  141. Shimada T, Bridier A, Briandet R, Ishihama A (2011) Novel roles of LeuO in transcription regulation of E. coli genome: antagonistic interplay with the universal silencer H-NS. Mol Microbiol 82:378–397PubMedCrossRefGoogle Scholar
  142. Snoep JL, van der Weijden CC, Andersen HW, Westerhoff HV, Jensen PR (2002) DNA supercoiling in Escherichia coli is under tight and subtle homeostatic control, involving gene-expression and metabolic regulation of both topoisomerase I and DNA gyrase. Eur J Biochem 269:1662–1669PubMedCrossRefGoogle Scholar
  143. Sobetzko P (2016) Transcription-coupled DNA supercoiling dictates the chromosomal arrangement of bacterial genes. Nucleic Acids Res 44:1514–1524PubMedPubMedCentralCrossRefGoogle Scholar
  144. Sobetzko P, Travers A, Muskhelishvili G (2012) Gene order and chromosome dynamics coordinate spatiotemporal gene expression during the bacterial growth cycle. Proc Natl Acad Sci U S A 109:E42–E50PubMedCrossRefGoogle Scholar
  145. Soucy SM, Huang J, Gogarten JP (2015) Horizontal gene transfer: building the web of life. Nat Rev Genet 16:472–482PubMedCrossRefGoogle Scholar
  146. Straney R, Krah R, Menzel R (1994) Mutations in the -10 TATAAT sequence of the gyrA promoter affect both promoter strength and sensitivity to DNA supercoiling. J Bacteriol 176:5999–6006PubMedPubMedCentralCrossRefGoogle Scholar
  147. Sugino A, Higgins NP, Brown PO, Peebles CL, Cozzarelli NR (1978) Energy coupling in DNA gyrase and the mechanism of action of novobiocin. Proc Natl Acad Sci U S A 75:4838–4842PubMedPubMedCentralCrossRefGoogle Scholar
  148. Touchon M, Rocha EP (2016) Coevolution of the organization and structure of prokaryotic genomes. Cold Spring Harb Perspect Biol 8:a018168PubMedCrossRefGoogle Scholar
  149. Tsao YP, Wu HY, Liu LF (1989) Transcription-driven supercoiling of DNA: direct biochemical evidence from in vitro studies. Cell 56:111–118PubMedCrossRefGoogle Scholar
  150. Unniraman S, Nagaraja V (1999) Regulation of DNA gyrase operon in Mycobacterium smegmatis: a distinct mechanism of relaxation stimulated transcription. Genes Cells 4:697–706PubMedCrossRefGoogle Scholar
  151. Unniraman S, Chatterji M, Nagaraja V (2002) DNA gyrase genes in Mycobacterium tuberculosis: a single operon driven by multiple promoters. J Bacteriol 184:5449–5456PubMedPubMedCentralCrossRefGoogle Scholar
  152. van Loenhout MT, de Grunt MV, Dekker C (2012) Dynamics of DNA supercoils. Science 338:94–97PubMedCrossRefGoogle Scholar
  153. van Workum M, van Dooren SJ, Oldenburg N, Molenaar D, Jensen PR, Snoep JL, Westerhoff HV (1996) DNA supercoiling depends on the phosphorylation potential in Escherichia coli. Mol Microbiol 20:351–360PubMedCrossRefGoogle Scholar
  154. Vinograd J, Lebowitz J, Radloff R, Watson R, Laipis P (1965) The twisted circular form of polyoma viral DNA. Proc Natl Acad Sci U S A 53:1104–1111PubMedPubMedCentralCrossRefGoogle Scholar
  155. Wang JC (1971) Interaction between DNA and an Escherichia coli protein omega. J Mol Biol 55:523–533PubMedCrossRefGoogle Scholar
  156. Wang Q, Sacco M, Ricca E, Lago CT, De Felice M, Calvo JM (1993) Organization of Lrp-binding sites upstream of ilvIH in Salmonella typhimurium. Mol Microbiol 7:883–891PubMedCrossRefGoogle Scholar
  157. Webber MA, Ricci V, Whitehead R, Patel M, Fookes M, Ivens A, Piddock LJ (2013) Clinically relevant mutant DNA gyrase alters supercoiling, changes the transcriptome, and confers multidrug resistance. MBio 4:e00273-13PubMedPubMedCentralCrossRefGoogle Scholar
  158. Weinstein-Fischer D, Elgrably-Weiss M, Altuvia S (2000) Escherichia coli response to hydrogen peroxide: a role for DNA supercoiling, topoisomerase I and Fis. Mol Microbiol 35:1413–1420PubMedCrossRefGoogle Scholar
  159. Westerhoff HV, van Workum M (1990) Control of DNA structure and gene expression. Biomed Biochim Acta 49:839–853PubMedGoogle Scholar
  160. Wilson CJ, Zhan H, Swint-Kruse L, Matthews KS (2007) The lactose repressor system: paradigms for regulation, allosteric behavior and protein folding. Cell Mol Life Sci 64:3–16PubMedCrossRefGoogle Scholar
  161. Wu HY, Shyy SH, Wang JC, Liu LF (1988) Transcription generates positively and negatively supercoiled domains in the template. Cell 53:433–440PubMedCrossRefGoogle Scholar
  162. Wu HY, Tan J, Fang M (1995) Long-range interaction between two promoters: activation of the leu-500 promoter by a distant upstream promoter. Cell 82:445–451PubMedCrossRefGoogle Scholar
  163. Xu X, Ben Imeddourene A, Zargarian L, Foloppe N, Mauffret O, Hartmann B (2014) NMR studies of DNA support the role of pre-existing minor groove variations in nucleosome indirect readout. Biochemistry 53:5601–5612PubMedCrossRefGoogle Scholar
  164. Yamamoto N, Droffner ML (1985) Mechanisms determining aerobic or anaerobic growth in the facultative anaerobe Salmonella typhimurium. Proc Natl Acad Sci U S A 82:2077–2081PubMedPubMedCentralCrossRefGoogle Scholar
  165. Ye F, Brauer T, Niehus E, Drlica K, Josenhans C, Suerbaum S (2007) Flagellar and global gene regulation in Helicobacter pylori modulated by changes in DNA supercoiling. Int J Med Microbiol 297:65–81PubMedCrossRefGoogle Scholar
  166. Zawadzki P, Stracy M, Ginda K, Zawadzka K, Lesterlin C, Kapanidis AN, Sherratt DJ (2015) The localization and action of topoisomerase IV in Escherichia coli chromosome segregation is coordinated by the SMC complex, MukBEF. Cell Rep 13:2587–2596PubMedPubMedCentralCrossRefGoogle Scholar
  167. Zechiedrich EL, Khodursky AB, Bachellier S, Schneider R, Chen D, Lilley DM, Cozzarelli NR (2000) Roles of topoisomerases in maintaining steady-state DNA supercoiling in Escherichia coli. J Biol Chem 275:8103–8113PubMedCrossRefGoogle Scholar
  168. Zhi X, Leng F (2013) Dependence of transcription-coupled DNA supercoiling on promoter strength in Escherichia coli topoisomerase I deficient strains. Gene 514:82–90PubMedCrossRefGoogle Scholar
  169. Zhou T, Yang L, Lu Y, Dror I, Dantas Machado AC, Ghane T, Di Felice R, Rohs R (2013) DNAshape: a method for the high-throughput prediction of DNA structural features on a genomic scale. Nucleic Acids Res 41:W56–W62PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Microbiology, Moyne Institute of Preventive MedicineTrinity College DublinDublin 2Ireland
  2. 2.Department of Genetics, Smurfit Institute of GeneticsTrinity College DublinDublin 2Ireland
  3. 3.Wellcome Trust Sanger InstituteHinxton, CambridgeUK

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