Skip to main content
Log in

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

  • Review
  • Published:
Biophysical Reviews Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahmed W, Menon S, Karthik PVDNB, Nagaraja V (2016) Autoregulation of topoisomerase I expression by supercoiling sensitive transcription. Nucleic Acids Res 44:1541–1552

    Article  PubMed  Google Scholar 

  • 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 69:1995–2007

    Article  CAS  PubMed  Google Scholar 

  • Alice AF, Sanchez-Rivas C (1997) DNA supercoiling and osmoresistance in Bacillus subtilis 168. Curr Microbiol 35:309–315

    Article  CAS  PubMed  Google Scholar 

  • 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 48:1281–1288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balke VL, Gralla JD (1987) Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli. J Bacteriol 169:4499–4506

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 44:1235–1250

    Article  CAS  PubMed  Google Scholar 

  • Bates AD, Maxwell A (2007) Energy coupling in type II topoisomerases: why do they hydrolyze ATP? Biochemistry 46:7929–7941

    Article  CAS  PubMed  Google Scholar 

  • Bauer WR, Crick FHC, White JH (1980) Supercoiled DNA. Sci Am 243:100–113

    CAS  PubMed  Google Scholar 

  • Bebbington KJ, Williams HD (2001) A role for DNA supercoiling in the regulation of the cytochrome bd oxidase of Escherichia coli. Microbiology 147:591–598

    Article  CAS  PubMed  Google Scholar 

  • Beltrametti F, Kresse AU, Guzmán CA (1999) Transcriptional regulation of the esp genes of enterohemorrhagic Escherichia coli. J Bacteriol 181:3409–3418

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bliska JB, Cozzarelli NR (1987) Use of site-specific recombination as a probe of DNA structure and metabolism in vivo. J Mol Biol 194:205–218

    Article  CAS  PubMed  Google Scholar 

  • Bohrer CH, Roberts E (2016) A biophysical model of supercoiling dependent transcription predicts a structural aspect to gene regulation. BMC Biophys 9:2

    Article  PubMed  PubMed Central  Google Scholar 

  • Boles TC, White JH, Cozzarelli NR (1990) Structure of plectonemically supercoiled DNA. J Mol Biol 213:931–951

    Article  CAS  PubMed  Google Scholar 

  • Booker BM, Deng S, Higgins NP (2010) DNA topology of highly transcribed operons in Salmonella enterica serovar Typhimurium. Mol Microbiol 78:1348–1364

    Article  CAS  PubMed  Google Scholar 

  • 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 48:561–571

    Article  CAS  PubMed  Google Scholar 

  • 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 14:441–448

    Article  CAS  PubMed  Google Scholar 

  • 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) 5:605–614

    Article  CAS  Google Scholar 

  • Brennan RG (1993) The winged-helix DNA-binding motif: another helix-turn-helix takeoff. Cell 74:773–776

    Article  CAS  PubMed  Google Scholar 

  • Bryant JA, Sellars LE, Busby SJ, Lee DJ (2014) Chromosome position effects on gene expression in Escherichia coli K-12. Nucleic Acids Res 42:11383–11392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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, e1002615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 80:85–101

    Article  CAS  PubMed  Google Scholar 

  • 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, e84382

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 284:875–883

    Article  CAS  PubMed  Google Scholar 

  • Champion K, Higgins NP (2007) Growth rate toxicity phenotypes and homeostatic supercoil control differentiate Escherichia coli from Salmonella enterica serovar Typhimurium. J Bacteriol 189:5839–5849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen CC, Wu HY (2005) LeuO protein delimits the transcriptionally active and repressive domains on the bacterial chromosome. J Biol Chem 280:15111–15121

    Article  CAS  PubMed  Google Scholar 

  • 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 89:8784–8788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen CC, Ghole M, Majumder A, Wang Z, Chandana S, Wu HY (2003) LeuO-mediated transcriptional derepression. J Biol Chem 278:38094–38103

    Article  CAS  PubMed  Google Scholar 

  • 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 280:5101–5112

    Article  CAS  PubMed  Google Scholar 

  • 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 13:206–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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–D109

    Article  PubMed  Google Scholar 

  • Chong S, Chen C, Ge H, Xie XS (2014) Mechanism of transcriptional bursting in bacteria. Cell 158:314–326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 273:75–83

    Article  CAS  PubMed  Google Scholar 

  • 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, e1002380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 126:115–124

    Article  CAS  PubMed  Google Scholar 

  • Cotter PA, DiRita VJ (2000) Bacterial virulence gene regulation: an evolutionary perspective. Annu Rev Microbiol 54:519–565

    Article  CAS  PubMed  Google Scholar 

  • Dame RT, Noom MC, Wuite GJ (2006) Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature 444:387–390

    Article  CAS  PubMed  Google Scholar 

  • 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 68:4209–4215

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 99:12126–12131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 76:1250–1265

    Article  CAS  PubMed  Google Scholar 

  • 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 85:1072–1089

    Article  CAS  PubMed  Google Scholar 

  • 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 111:15402–15407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon RA, Henderson NC, Austin S (1988) DNA supercoiling and aerobic regulation of transcription from the Klebsiella pneumoniae nifLA promoter. Nucleic Acids Res 16:9933–9946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 286:22178–22185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dorman CJ (1991) DNA supercoiling and environmental regulation of gene expression in pathogenic bacteria. Infect Immun 59:745–749

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dorman CJ (2006) DNA supercoiling and bacterial gene expression. Sci Prog 89:151–166

    Article  CAS  PubMed  Google Scholar 

  • Dorman CJ (2007) H-NS, the genome sentinel. Nat Rev Microbiol 5:157–161

    Article  CAS  PubMed  Google Scholar 

  • Dorman CJ (2013) Genome architecture and global gene regulation in bacteria: making progress towards a unified model? Nat Rev Microbiol 11:349–355

    Article  CAS  PubMed  Google Scholar 

  • Dorman CJ, Corcoran CP (2009) Bacterial DNA topology and infectious disease. Nucleic Acids Res 37:672–678

    Article  CAS  PubMed  Google Scholar 

  • 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 170:2816–2826

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dorman CJ, Ni Bhriain N, Higgins CF (1990) DNA supercoiling and environmental regulation of virulence gene expression in Shigella flexneri. Nature 344:789–792

    Article  CAS  PubMed  Google Scholar 

  • Drolet M (2006) Growth inhibition mediated by excess negative supercoiling: the interplay between transcription elongation, R-loop formation and DNA topology. Mol Microbiol 59:723–730

    Article  CAS  PubMed  Google Scholar 

  • El Hanafi D, Bossi L (2000) Activation and silencing of leu-500 promoter by transcription-induced DNA supercoiling in the Salmonella chromosome. Mol Microbiol 37:583–594

    Article  PubMed  Google Scholar 

  • Fang M, Wu HY (1998a) A promoter relay mechanism for sequential gene activation. J Bacteriol 180:626–633

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fang M, Wu HY (1998b) Suppression of leu-500 mutation in topA+ Salmonella typhimurium strains. The promoter relay at work. J Biol Chem 273:29929–29934

    Article  CAS  PubMed  Google Scholar 

  • Fass E, Groisman EA (2009) Control of Salmonella pathogenicity island-2 gene expression. Curr Opin Microbiol 12:199–204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 54:823–835

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 150:3807–3819

    Article  CAS  PubMed  Google Scholar 

  • Friedman SB, Margolin P (1968) Evidence for an altered operator specificity: catabolite repression control of the leucine operon in Salmonella typhimurium. J Bacteriol 95:2263–2269

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galán JE, Curtiss R 3rd (1990) Expression of Salmonella typhimurium genes required for invasion is regulated by changes in DNA supercoiling. Infect Immun 58:1879–1885

    PubMed  PubMed Central  Google Scholar 

  • 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 73:3872–3876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 43:8215–8226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein E, Drlica K (1984) Regulation of bacterial DNA supercoiling: plasmid linking numbers vary with growth temperature. Proc Natl Acad Sci U S A 81:4046–4050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graeff-Wohlleben H, Deppisch H, Gross R (1995) Global regulatory mechanisms affect virulence gene expression in Bordetella pertussis. Mol Gen Genet 247:86–94

    Article  CAS  PubMed  Google Scholar 

  • Graf LH Jr, Burns RO (1973) The supX-leu-500 mutations and expression of the leucine operon. Mol Gen Genet 126:291–301

    Article  CAS  PubMed  Google Scholar 

  • Groisman EA, Casadesús J (2005) The origin and evolution of human pathogens. Mol Microbiol 56:1–7

    Article  CAS  PubMed  Google Scholar 

  • 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 196:2143–2154

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hardy CD, Cozzarelli NR (2003) Alteration of Escherichia coli topoisomerase IV to novobiocin resistance. Antimicrob Agents Chemother 47:941–947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 12:1497–1507

    Article  CAS  PubMed  Google Scholar 

  • 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 166:1113–1117

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hay AJ, Zhu J (2015) Host intestinal signal-promoted biofilm dispersal induces Vibrio cholerae colonization. Infect Immun 83:317–323

    Article  PubMed  Google Scholar 

  • 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 16:734–745

    Article  PubMed  CAS  Google Scholar 

  • 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, e1005796

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Higgins NP (2014) RNA polymerase: chromosome domain boundary maker and regulator of supercoil density. Curr Opin Microbiol 22:138–143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higgins NP, Vologodskii AV (2015) Topological behavior of plasmid DNA. Microbiol Spectr 3(2). doi: 10.1128/microbiolspec.PLAS-0036-2014

  • 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 75:1773–1777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 52:569–584

    Article  CAS  PubMed  Google Scholar 

  • Hsieh LS, Burger RM, Drlica K (1991a) Bacterial DNA supercoiling and [ATP]/[ADP]. Changes associated with a transition to anaerobic growth. J Mol Biol 219:443–450

    Article  CAS  PubMed  Google Scholar 

  • Hsieh LS, Rouviere-Yaniv J, Drlica K (1991b) Bacterial DNA supercoiling and [ATP]/[ADP] ratio: changes associated with salt shock. J Bacteriol 173:3914–3917

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jain P, Nagaraja V (2005) An atypical type II topoisomerase from Mycobacterium smegmatis with positive supercoiling activity. Mol Microbiol 58:1392–1405

    Article  CAS  PubMed  Google Scholar 

  • Karem K, Foster JW (1993) The influence of DNA topology on the environmental regulation of a pH-regulated locus in Salmonella typhimurium. Mol Microbiol 10:75–86

    Article  CAS  PubMed  Google Scholar 

  • Kato J, Nishimura Y, Imamura R, Niki H, Hiraga S, Suzuki H (1990) New topoisomerase essential for chromosome segregation in E. coli. Cell 63:393–404

    Article  CAS  PubMed  Google Scholar 

  • Kenney LJ (2002) Structure/function relationships in OmpR and other winged-helix transcription factors. Curr Opin Microbiol 5:135–141

    Article  CAS  PubMed  Google Scholar 

  • Khodursky AB, Zechiedrich EL, Cozzarelli NR (1995) Topoisomerase IV is a target of quinolones in Escherichia coli. Proc Natl Acad Sci U S A 92:11801–11805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koster DA, Crut A, Shuman S, Bjornsti M-A, Dekker NH (2010) Cellular strategies for regulating DNA supercoiling: a single-molecule perspective. Cell 142:519–530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

  • 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 15:146–154

    Article  CAS  PubMed  Google Scholar 

  • 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 101:1–11

    Article  CAS  PubMed  Google Scholar 

  • 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 35:6330–6337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leclerc GJ, Tartera C, Metcalf ES (1998) Environmental regulation of Salmonella typhi invasion-defective mutants. Infect Immun 66:682–691

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 99:9139–9144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis M (2011) A tale of two repressors. J Mol Biol 409:14–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 3:269–273

    Article  CAS  PubMed  Google Scholar 

  • Lilley DM, Higgins CF (1991) Local DNA topology and gene expression: the case of the leu-500 promoter. Mol Microbiol 5:779–783

    Article  CAS  PubMed  Google Scholar 

  • Liu LF, Wang JC (1987) Supercoiling of the DNA template during transcription. Proc Natl Acad Sci U S A 84:7024–7027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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, e81

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma J, Wang M (2014a) Interplay between DNA supercoiling and transcription elongation. Transcription 5, e28636

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma J, Wang MD (2014b) RNA polymerase is a powerful torsional motor. Cell Cycle 13:337–338

    Article  CAS  PubMed  Google Scholar 

  • Ma J, Bai L, Wang MD (2013) Transcription under torsion. Science 340:1580–1583

    Article  CAS  PubMed  Google Scholar 

  • Malkhosyan SR, Panchenko YuA, Rekesh AN (1991) A physiological role for DNA supercoiling in the anaerobic regulation of colicin gene expression. Mol Gen Genet 225:342–345

    Article  CAS  PubMed  Google Scholar 

  • 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 82:5437–5441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martínez-Hackert E, Stock AM (1997) Structural relationships in the OmpR family of winged-helix transcription factors. J Mol Biol 269:301–312

    Article  PubMed  Google Scholar 

  • 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 387:1261–1276

    Article  CAS  PubMed  Google Scholar 

  • McGovern V, Higgins NP, Chiz RS, Jaworski A (1994) H-NS over-expression induces an artificial stationary phase by silencing global transcription. Biochimie 76:1019–10129

    Article  CAS  PubMed  Google Scholar 

  • Menzel R, Gellert M (1983) Regulation of the genes for E. coli DNA gyrase: homeostatic control of DNA supercoiling. Cell 34:105–113

    Article  CAS  PubMed  Google Scholar 

  • 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 84:4185–4189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 417:642–645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meury J, Kohiyama M (1992) Potassium ions and changes in bacterial DNA supercoiling under osmotic stress. FEMS Microbiol Lett 78:159–164

    Article  CAS  PubMed  Google Scholar 

  • Naughton C, Corless S, Gilbert N (2013) Divergent RNA transcription: a role in promoter unwinding? Transcription 4:162–166

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 313:236–238

    Article  CAS  PubMed  Google Scholar 

  • Niehus E, Cheng E, Tan M (2008) DNA supercoiling-dependent gene regulation in Chlamydia. J Bacteriol 190:6419–6427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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–R914

    Article  CAS  PubMed  Google Scholar 

  • Nurse P, Levine C, Hassing H, Marians KJ (2003) Topoisomerase III can serve as the cellular decatenase in Escherichia coli. J Biol Chem 278:8653–8660

    Article  CAS  PubMed  Google Scholar 

  • 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 62:869–882

    Article  PubMed  CAS  Google Scholar 

  • 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 6:2467–2476

    Article  PubMed  Google Scholar 

  • Oguey C, Foloppe N, Hartmann B (2010) Understanding the sequence-dependence of DNA groove dimensions: implications for DNA interactions. PLoS One 5, e15931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 39:191–198

    Article  CAS  PubMed  Google Scholar 

  • Oppenheim AB, Kobiler O, Stavans J, Court DL, Adhya S (2005) Switches in bacteriophage lambda development. Annu Rev Genet 39:409–429

    Article  CAS  PubMed  Google Scholar 

  • 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 13:141–153

    Article  CAS  PubMed  Google Scholar 

  • 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 174:5211–5218

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perez-Cheeks BA, Lee C, Hayama R, Marians KJ (2012) A role for topoisomerase III in Escherichia coli chromosome segregation. Mol Microbiol 86:1007–1022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pettijohn DE, Pfenninger O (1980) Supercoils in prokaryotic DNA restrained in vivo. Proc Natl Acad Sci U S A 77:1331–1335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porwollik S, McClelland M (2003) Lateral gene transfer in Salmonella. Microbes Infect 5:977–989

    Article  CAS  PubMed  Google Scholar 

  • Pruss GJ, Drlica K (1985) DNA supercoiling and suppression of the leu-500 promoter mutation. J Bacteriol 164:947–949

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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, e1004215

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rahmouni AR, Wells RD (1992) Direct evidence for the effect of transcription on local DNA supercoiling in vivo. J Mol Biol 223:131–144

    Article  CAS  PubMed  Google Scholar 

  • 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 96:14294–14299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richardson SM, Higgins CF, Lilley DM (1984) The genetic control of DNA supercoiling in Salmonella typhimurium. EMBO J 3:1745–1752

    CAS  PubMed  PubMed Central  Google Scholar 

  • Richardson SM, Higgins CF, Lilley DM (1988) DNA supercoiling and the leu-500 promoter mutation of Salmonella typhimurium. EMBO J 7:1863–1869

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rohde JR, Fox JM, Minnich SA (1994) Thermoregulation in Yersinia enterocolitica is coincident with changes in DNA supercoiling. Mol Microbiol 12:187–199

    Article  CAS  PubMed  Google Scholar 

  • Rohs R, West SM, Sosinsky A, Liu P, Mann RS, Honig B (2009) The role of DNA shape in protein-DNA recognition. Nature 461:1248–1253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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, e1002845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 59:4662–4668

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schell MA (1993) Molecular biology of the LysR family of transcriptional regulators. Annu Rev Microbiol 47:597–626

    Article  CAS  PubMed  Google Scholar 

  • Schleif RF (2013) Modulation of DNA binding by gene-specific transcription factors. Biochemistry 52:6755–6765

    Article  CAS  PubMed  Google Scholar 

  • 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 15:291

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Semsey S, Virnik K, Adhya S (2005) A gamut of loops: meandering DNA. Trends Biochem Sci 30:334–341

    Article  CAS  PubMed  Google Scholar 

  • 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 30:91–105

    Article  CAS  PubMed  Google Scholar 

  • 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 232:49–57

    Article  CAS  PubMed  Google Scholar 

  • 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 82:378–397

    Article  CAS  PubMed  Google Scholar 

  • 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 269:1662–1669

    Article  CAS  PubMed  Google Scholar 

  • Sobetzko P (2016) Transcription-coupled DNA supercoiling dictates the chromosomal arrangement of bacterial genes. Nucleic Acids Res 44:1514–1524

    Article  PubMed  PubMed Central  Google Scholar 

  • 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–E50

    Article  CAS  PubMed  Google Scholar 

  • Soucy SM, Huang J, Gogarten JP (2015) Horizontal gene transfer: building the web of life. Nat Rev Genet 16:472–482

    Article  CAS  PubMed  Google Scholar 

  • 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 176:5999–6006

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 75:4838–4842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Touchon M, Rocha EP (2016) Coevolution of the organization and structure of prokaryotic genomes. Cold Spring Harb Perspect Biol 8:a018168

    Article  PubMed  Google Scholar 

  • Tsao YP, Wu HY, Liu LF (1989) Transcription-driven supercoiling of DNA: direct biochemical evidence from in vitro studies. Cell 56:111–118

    Article  CAS  PubMed  Google Scholar 

  • Unniraman S, Nagaraja V (1999) Regulation of DNA gyrase operon in Mycobacterium smegmatis: a distinct mechanism of relaxation stimulated transcription. Genes Cells 4:697–706

    Article  CAS  PubMed  Google Scholar 

  • Unniraman S, Chatterji M, Nagaraja V (2002) DNA gyrase genes in Mycobacterium tuberculosis: a single operon driven by multiple promoters. J Bacteriol 184:5449–5456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Loenhout MT, de Grunt MV, Dekker C (2012) Dynamics of DNA supercoils. Science 338:94–97

    Article  PubMed  CAS  Google Scholar 

  • 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 20:351–360

    Article  PubMed  Google Scholar 

  • 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 53:1104–1111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JC (1971) Interaction between DNA and an Escherichia coli protein omega. J Mol Biol 55:523–533

    Article  CAS  PubMed  Google Scholar 

  • 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 7:883–891

    Article  CAS  PubMed  Google Scholar 

  • 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:e00273-13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 35:1413–1420

    Article  CAS  PubMed  Google Scholar 

  • Westerhoff HV, van Workum M (1990) Control of DNA structure and gene expression. Biomed Biochim Acta 49:839–853

    CAS  PubMed  Google Scholar 

  • 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 64:3–16

    Article  CAS  PubMed  Google Scholar 

  • Wu HY, Shyy SH, Wang JC, Liu LF (1988) Transcription generates positively and negatively supercoiled domains in the template. Cell 53:433–440

    Article  CAS  PubMed  Google Scholar 

  • 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 82:445–451

    Article  CAS  PubMed  Google Scholar 

  • 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 53:5601–5612

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto N, Droffner ML (1985) Mechanisms determining aerobic or anaerobic growth in the facultative anaerobe Salmonella typhimurium. Proc Natl Acad Sci U S A 82:2077–2081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 297:65–81

    Article  CAS  PubMed  Google Scholar 

  • 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 13:2587–2596

    Article  CAS  PubMed  Google Scholar 

  • Zechiedrich EL, Khodursky AB, Bachellier S, Schneider R, Chen D, Lilley DM, Cozzarelli NR (2000) Roles of topoisomerases in maintaining steady-state DNA supercoiling in Escherichia coli. J Biol Chem 275:8103–8113

    Article  CAS  PubMed  Google Scholar 

  • Zhi X, Leng F (2013) Dependence of transcription-coupled DNA supercoiling on promoter strength in Escherichia coli topoisomerase I deficient strains. Gene 514:82–90

    Article  CAS  PubMed  Google Scholar 

  • 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–W62

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

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

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Charles J. Dorman.

Ethics declarations

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dorman, C.J., Dorman, M.J. DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression. Biophys Rev 8, 209–220 (2016). https://doi.org/10.1007/s12551-016-0205-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12551-016-0205-y

Keywords

Navigation