The Evolution of Gene Regulatory Mechanisms in Bacteria

  • Charles J. DormanEmail author
  • Niamh Ní Bhriain
  • Matthew J. Dorman
Part of the Grand Challenges in Biology and Biotechnology book series (GCBB)


Modern bacteria regulate the expression of their genes through a spectrum of mechanisms ranging from the very simple to those that are highly complex. The regulatory mechanisms have evolved in concert with the means to detect changes to the physical or chemical environment, equipping the organism to respond to change. Regulation can be imposed at each stage of gene expression, and the networking of genes through coordinated control makes for multidimensional relationships that vary in time and space. Understanding how this regulatory complexity evolved is not a trivial matter, but it can be attempted. In one popular view, an ‘RNA world’ may have preceded the modern one with its DNA-based genomes. Looking for evidence of RNA-based gene regulation has been very fruitful and shows that gene control at this level is still very much in use: the conversion of genetic information held in RNA into protein by translation involves processes that are open to control at several levels. In DNA-based genomes, transcription is a fundamental process, and over evolutionary time bacterial cells have invested heavily in mechanisms that control it. Mechanisms that influence the activity of RNA polymerase are legion but fall into two categories: those that impede and those that assist the polymerase in the process of reading genetic information. It seems that simply turning genes on or off is rarely sufficient: it was necessary to evolve mechanisms for tuning transcription to the needs of the cell to promote survival, regardless of the size or level of sophistication of the organism’s genome. These regulatory mechanisms have evolved in ways that make their operations ‘noisy’, and this noise can be useful in generating physiological variety among genetically identical bacterial cells. It is becoming clear that the evolutionary forces that shape the bacterial nucleoid also guide the development of gene regulatory elements. For this reason the evolution of bacterial gene regulatory mechanisms will also be considered in the context of bacterial genome architecture.



We thank AP Dorman for useful comments on the manuscript. This work was supported by Science Foundation Ireland Principal Investigator Award 13/IA/1875 to CJD. MJD is supported by the Wellcome Trust (grant 206194).


  1. Ahmad M, Xue Y, Lee SK et al (2016) RNA topoisomerase is prevalent in all domains of life and associates with polyribosomes in animals. Nucleic Acids Res 44(13):6335–6349PubMedPubMedCentralCrossRefGoogle Scholar
  2. Ahmed W, Menon S, Karthik PV et al (2016) Autoregulation of topoisomerase I expression by supercoiling sensitive transcription. Nucleic Acids Res 44(4):1541–1552PubMedCrossRefPubMedCentralGoogle Scholar
  3. Bae W, Xia B, Inouye M et al (2000) Escherichia coli CspA-family chaperones are transcription antiterminators. Proc Natl Acad Sci USA 97(14):7784–7789PubMedCrossRefPubMedCentralGoogle Scholar
  4. Balandina A, Claret L, Hengge-Aronis R et al (2001) The Escherichia coli histone-like protein HU regulates rpoS translation. Mol Microbiol 39(4):1069–1079PubMedCrossRefPubMedCentralGoogle Scholar
  5. Ban N, Nissen P, Hansen J et al (2000) The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289(5481):905–920CrossRefGoogle Scholar
  6. Bang IS, Audia JP, Park YK et al (2002) Autoinduction of the ompR response regulator by acid shock and control of the Salmonella enterica acid tolerance response. Mol Microbiol 44(5):1235–1250PubMedCrossRefGoogle Scholar
  7. Barquist L, Vogel J (2015) Accelerating discovery and functional analysis of small RNAs with new technologies. Annu Rev Genet 49:367–394PubMedCrossRefGoogle Scholar
  8. Battesti A, Majdalani N, Gottesman S (2011) The RpoS-mediated general stress response in Escherichia coli. Annu Rev Microbiol 65:189–213PubMedCrossRefGoogle Scholar
  9. Bauer WR, Crick FHC, White JH (1980) Supercoiled DNA. Sci Am 243(1):100–113PubMedGoogle Scholar
  10. Beloin C, Exley R, Mahe A et al (2000) Characterisation of LrpC DNA-binding properties and regulation of Bacillus subtilis lrpC gene expression. J Bacteriol 182(16):414–4424CrossRefGoogle Scholar
  11. Boles TC, White JH, Cozzarelli NR (1990) Structure of plectonemically supercoiled DNA. J Mol Biol 213(4):931–951PubMedCrossRefGoogle Scholar
  12. Booth A, Mariscal C, Doolittle WF (2016) The modern synthesis in the light of microbial genomics. Annu Rev Microbiol 70:279–297PubMedCrossRefGoogle Scholar
  13. Bordes P, Conter A, Morales V, Bouvier J, Kolb A, Gutierrez C (2003) DNA supercoiling contributes to disconnect signaS accumulation from sigmaS-dependent transcription in Escherichia coli. Mol Microbiol 48(2):561–571PubMedCrossRefGoogle Scholar
  14. Bowman JC, Hud NV, Williams LD (2015) The ribosome challenge to the RNA world. J Mol Evol 80(3):143–161PubMedCrossRefGoogle Scholar
  15. 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(4):605–614CrossRefGoogle Scholar
  16. Brock TD (1990) The emergence of bacterial genetics. Cold Spring Harbor Press, Cold Spring HarborGoogle Scholar
  17. Browning DF, Busby SJ (2016) Local and global regulation of transcription initiation in bacteria. Nat Rev Microbiol 14(10):638–650PubMedCrossRefGoogle Scholar
  18. Bryant JA, Sellars LE, Busby SJ et al (2014) Chromosome position effects on gene expression in Escherichia coli K-12. Nucleic Acids Res 42(18):11383–11392PubMedPubMedCentralCrossRefGoogle Scholar
  19. Burgess BR, Richardson JP (2001) RNA passes through the hole of the protein hexamer in the complex with the Escherichia coli Rho factor. J Biol Chem 276(6):4182–4189PubMedCrossRefGoogle 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(3):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(1):85–101PubMedCrossRefGoogle Scholar
  22. Cameron AD, Dillon SC, Kröger C, Beran L, Dorman CJ (2017) Broad scale redistribution of mRNA abundance and transcriptional machinery in response to growth rate in Salmonella enterica serovar Typhimurium. Microb Genom 3(10):e000127PubMedPubMedCentralGoogle Scholar
  23. Cardinale CJ, Washburn RS, Tadigotia VR et al (2008) Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E. coli. Science 320(5878):935–938PubMedPubMedCentralCrossRefGoogle Scholar
  24. Carroll RK, Liao X, Morgan LK, Cicirelli EM, Li Y, Sheng W, Feng X, Kenney LJ (2009) Structural and functional analysis of the C-terminal DNA binding domain of the Salmonella typhimurium SPI-2 response regulator SsrB. J Biol Chem 284(18):12008–12019PubMedPubMedCentralCrossRefGoogle Scholar
  25. Cech TR (2009) Crawling out of the RNA world. Cell 136(4):599–602PubMedCrossRefGoogle Scholar
  26. Chakraborty S, Mizusaki H, Kenney LJ (2015) A FRET-based DNA biosensor tracks OmpR-dependent acidification of Salmonella during macrophage infection. PLoS Biol 13(4):e1002116PubMedPubMedCentralCrossRefGoogle Scholar
  27. Citti C, Blanchard A (2013) Mycoplasmas and their host: emerging and re-emerging minimal pathogens. Trends Microbiol 21(4):196–203CrossRefGoogle Scholar
  28. Colgan AM, Quinn HJ, Kary SC, Mitchenall LA, Maxwell A, Cameron ADS, Dorman CJ (2018) Negative supercoiling of DNA by gyrase is inhibited in serovar Typhimurium during adaptation to acid stress. Mol Microbiol 107(6):734–746PubMedCrossRefPubMedCentralGoogle Scholar
  29. 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(1):75–83PubMedCrossRefGoogle Scholar
  30. Cooper S, Helmstetter CE (1968) Chromosome replication and the division cycle of Escherichia coli B/r. J Mol Biol 31(3):519–540PubMedCrossRefPubMedCentralGoogle Scholar
  31. Corbett D, Bennett HJ, Askar H et al (2007) SlyA and H-NS regulate transcription of the Escherichia coli K5 capsule gene cluster, and expression of slyA in Escherichia coli is temperature-dependent, positively autoregulated, and independent of H-NS. J Biol Chem 282(46):33326–33335PubMedCrossRefPubMedCentralGoogle Scholar
  32. Crozat E, Philippe N, Lenski RE et al (2005) Long-term experimental evolution in Escherichia coli. XII. DNA topology as a key target of selection. Genetics 169(2):523–532PubMedPubMedCentralCrossRefGoogle Scholar
  33. Crozat E, Winkworth C, Gaffé J et al (2010) Parallel genetic and phenotypic evolution of DNA superhelicity in experimental populations of Escherichia coli. Mol Biol Evol 27(9):2113–2128PubMedCrossRefPubMedCentralGoogle Scholar
  34. Crozat E, Hindré T, Kühn L et al (2011) Altered regulation of the OmpF porin by Fis in Escherichia coli during an evolution experiment and between B and K-12 strains. J Bacteriol 193(2):429–440PubMedCrossRefPubMedCentralGoogle Scholar
  35. Dame RT, Noom MC, Wuite GJL (2006) Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature 444(7117):387–390PubMedCrossRefPubMedCentralGoogle Scholar
  36. Deighan P, Free A, Dorman CJ (2000) A role for the Escherichia coli H-NS-like protein StpA in OmpF porin expression through modulation of micF RNA stability. Mol Microbiol 38(1):126–139PubMedCrossRefPubMedCentralGoogle Scholar
  37. Desnoyers G, Morissette A, Prévost K, Massé E (2009) Small RNA-induced differential degradation of the polycistronic mRNA iscRSUA. EMBO J 28(11):1551–1561PubMedPubMedCentralCrossRefGoogle Scholar
  38. Dillon SC, Dorman CJ (2010) Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol 8(3):185–195PubMedCrossRefPubMedCentralGoogle Scholar
  39. Dillon SC, Cameron AD, Hokamp K et al (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(5):1250–1265PubMedCrossRefPubMedCentralGoogle Scholar
  40. Doose G, Alexis M, Kirsch R et al (2013) Mapping the RNA-Seq trash bin: unusual transcripts in prokaryotic transcriptome sequencing data. RNA Biol 10(7):1204–1210PubMedPubMedCentralCrossRefGoogle Scholar
  41. Dordet-Frisoni E, Sagne E, Baranowski E, Breton M, Nouvel LX, Blanchard A, Marenda MS, Tardy F, Pascal S-P, Citti C (2014) Chromosomal transfers in Mycoplasmas: when minimal genomes go mobile. MBio 5(6):e01958-14PubMedPubMedCentralCrossRefGoogle Scholar
  42. Dorman CJ (2007) H-NS, the genome sentinel. Nat Rev Microbiol 5(2):157–161PubMedCrossRefPubMedCentralGoogle Scholar
  43. Dorman CJ (2009) Regulatory integration of horizontally-transferred genes in bacteria. Front Biosci (Landmark Ed) 14:4103–4112Google Scholar
  44. Dorman CJ (2011) Regulation of transcription by DNA supercoiling in Mycoplasma genitalium: global control in the smallest known self-replicating genome. Mol Microbiol 81(2):302–304PubMedCrossRefPubMedCentralGoogle Scholar
  45. Dorman CJ (2013) Genome architecture and global gene regulation in bacteria: making progress towards a unified model? Nat Rev Microbiol 11(5):349–355PubMedCrossRefPubMedCentralGoogle Scholar
  46. Dorman CJ, Dorman MJ (2016) DNA supercoiling is a fundamental regulatory principle in the control of gene expression. Biophys Rev 8(3):209–220PubMedPubMedCentralCrossRefGoogle Scholar
  47. Dorman CJ, Dorman MJ (2017) Control of virulence gene transcription by indirect readout in Vibrio cholerae and Salmonella enterica serovar Typhimurium. Environ Microbiol 19(10):3834–3845. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Dorman CJ, Barr GC, Ní Bhriain N et al (1988) DNA supercoiling and the anaerobic and growth phase regulation of tonB gene expression. J Bacteriol 170(6):2816–2826PubMedPubMedCentralCrossRefGoogle Scholar
  49. Dorman CJ, Colgan A, Dorman MJ (2016) Bacterial pathogen gene regulation: a DNA-structure-centred view of a protein-dominated domain. Clin Sci (Lond) 130(14):1165–1177CrossRefGoogle Scholar
  50. Drolet M, Broccoli S, Rallu F et al (2003) The problem of hypernegative supercoiling and R-loop formation in transcription. Front Biosci 8:d210–d221PubMedCrossRefPubMedCentralGoogle Scholar
  51. Dutta D, Shatalin K, Ephstein V et al (2011) Linking RNA polymerase backtracking to genome instability in E. coli. Cell 146(4):533–543PubMedPubMedCentralCrossRefGoogle Scholar
  52. Ephstein V, Dutta D, Wade J et al (2010) An allosteric mechanism of Rho-dependent transcription termination. Nature 463(7278):245–249CrossRefGoogle Scholar
  53. Fass E, Groisman EA (2009) Control of Salmonella pathogenicity island-2 gene expression. Curr Opin Microbiol 12(2):199–204PubMedPubMedCentralCrossRefGoogle Scholar
  54. Fassler JS, Arnold GF, Tessman I (1986) Reduced superhelicity of plasmid DNA produced by the rho-15 mutation in Escherichia coli. Mol Gen Genet 204(3):424–429PubMedCrossRefPubMedCentralGoogle Scholar
  55. Feng Y, Zhang Y, Ebright RH (2016) Structural basis of transcription activation. Science 352(6291):1330–1333PubMedPubMedCentralCrossRefGoogle Scholar
  56. Fischer D, Eisenberg D (1997) Assigning folds to the proteins encoded by the genome of Mycoplasma genitalium. Proc Natl Acad Sci USA 94(22):11929–11934PubMedCrossRefPubMedCentralGoogle Scholar
  57. Fitzgerald S, Dillon SC, Chao TC et al (2015) Re-engineering cellular physiology by rewiring high-level global regulatory genes. Sci Rep 5:17653. CrossRefPubMedPubMedCentralGoogle Scholar
  58. Frost LS, Leplae R, Summers AO, Toussaint A (2005) Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3:722–732PubMedCrossRefPubMedCentralGoogle Scholar
  59. Fürtig B, Nozinovic S, Reining A et al (2015) Multiple conformational states of riboswitches fine-tune gene regulation. Curr Opin Struct Biol 30:112–124PubMedCrossRefPubMedCentralGoogle Scholar
  60. Gan W, Guan Z, Liu J et al (2011) R-loop-mediated genomic instability is caused by impairment of replication fork progression. Genes Dev 25(19):2041–2056PubMedPubMedCentralCrossRefGoogle Scholar
  61. Gerganova V, Berger M, Zaldastanishvili E et al (2015) Chromosomal position shift of a regulatory gene alters the bacterial phenotype. Nucleic Acids Res 43(17):8215–8226PubMedPubMedCentralCrossRefGoogle Scholar
  62. Gilbert W (1986) Origin of life: the RNA world. Nature 319:618CrossRefGoogle Scholar
  63. Gottesman S (2004) The small RNA regulators of Escherichia coli: roles and mechanisms. Annu Rev Microbiol 58:303–328PubMedCrossRefPubMedCentralGoogle Scholar
  64. Gourse RL, Ross W, Rutherford ST (2006) General pathway for turning on promoters transcribed by RNA polymerases containing alternative sigma factors. J Bacteriol 188(13):4589–4591PubMedPubMedCentralCrossRefGoogle Scholar
  65. Govindarajan S, Amster-Choder O (2016) Where are things inside a bacterial cell? Curr Opin Microbiol 33:83–90PubMedCrossRefPubMedCentralGoogle Scholar
  66. Grainger DC, Hurd D, Harrison M et al (2005) Studies of the distribution of Escherichia coli cAMP-receptor protein and RNA polymerase along the E. coli chromosome. Proc Natl Acad Sci USA 102(49):17693–17698PubMedCrossRefPubMedCentralGoogle Scholar
  67. Gruber TM, Gross CA (2003) Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57:441–466PubMedCrossRefPubMedCentralGoogle Scholar
  68. Grylak-Mielnicka A, Bidnenko V, Bardowski J et al (2016) Transcription termination factor Rho: a hub linking diverse physiological processes in bacteria. Microbiology 162(3):433–447PubMedCrossRefPubMedCentralGoogle Scholar
  69. Gutierrez-Preciado A, Henkin TM, Grundy FJ et al (2009) Biochemical features and functional implications of the RNA-based T-box regulatory mechanism. Microbiol Mol Biol Rev 73(1):36–61PubMedPubMedCentralCrossRefGoogle Scholar
  70. Haider F, Lithgow JK, Stapleton MR et al (2008) DNA recognition by the Salmonella enterica serovar Typhimurium transcription factor SlyA. Int Microbiol 11(4):245–250PubMedPubMedCentralGoogle Scholar
  71. Harinarayanan R, Gowrishankar J (2003) Host factor titration by chromosomal R-loops as a mechanism for runaway plasmid replication in transcription termination-defective mutants of Escherichia coli. J Mol Biol 332(1):31–46PubMedCrossRefPubMedCentralGoogle Scholar
  72. Haugen SP, Ross W, Gourse RL (2008) Advances in bacterial promoter recognition and its control by factors that do not bind DNA. Nat Rev Microbiol 6(7):507–519PubMedPubMedCentralCrossRefGoogle Scholar
  73. Hébrard M, Kröger C, Srikumar S et al (2012) sRNAs and the virulence of Salmonella enterica serovar Typhimurium. RNA Biol 9(4):437–445PubMedPubMedCentralCrossRefGoogle Scholar
  74. Helmann JD (1999) Anti-sigma factors. Curr Opin Microbiol 2:135–141PubMedCrossRefPubMedCentralGoogle Scholar
  75. Hengge R (2009) Proteolysis of sigmaS (RpoS) and the general stress response in Escherichia coli. Res Microbiol 160(9):667–676PubMedCrossRefPubMedCentralGoogle Scholar
  76. Hernday AD, Braaten BA, Low DA (2003) The mechanism by which DNA adenine methylase and PapI activate the pap epigenetic switch. Mol Cell 12(4):947–957PubMedCrossRefPubMedCentralGoogle Scholar
  77. Herrmann R, Reiner B (1998) Mycoplasma pneumonia and Mycoplasma genitalium: a comparison of two closely related bacterial species. Curr Opin Microbiol 1:572–579PubMedCrossRefPubMedCentralGoogle Scholar
  78. Higgins CF, Dorman CJ, Stirling DA et al (1988) A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell 52(4):569–584PubMedCrossRefPubMedCentralGoogle Scholar
  79. Hsieh LS, Rouvière-Yaniv J, Drlica K (1991) Bacterial DNA supercoiling and [ATP]/[ADP] ratio: changes associated with salt shock. J Bacteriol 173(12):3914–3917PubMedPubMedCentralCrossRefGoogle Scholar
  80. Isalan M, Lemerle C, Michalodimitrakis K et al (2008) Evolvability and hierarchy in rewired bacterial gene networks. Nature 452(7189):840–845PubMedPubMedCentralCrossRefGoogle Scholar
  81. Iyer LM, Koonin EV, Aravind L (2003) Evolutionary connection between the catalytic subunits of DNA-dependent RNA polymerases and eukaryotic RNA-dependent RNA polymerases and the origin of RNA polymerases. BMC Struct Biol 3:1PubMedPubMedCentralCrossRefGoogle Scholar
  82. Janga SC, Salgado H, Martinez-Antonio A (2009) Transcriptional regulation shapes the organization of genes on bacterial chromosomes. Nucleic Acids Res 37:3680–3688PubMedPubMedCentralCrossRefGoogle Scholar
  83. Jeong KS, Ahn J, Khodursky AB (2004) Spatial patterns of transcription activity in the chromosome of Escherichia coli. Genome Biol 5:R86PubMedPubMedCentralCrossRefGoogle Scholar
  84. Junier I, Rivoire O (2016) Conserved units of co-expression in bacterial genomes: an evolutionary insight into transcriptional regulation. PLoS One 11:e0155740PubMedPubMedCentralCrossRefGoogle Scholar
  85. Junier I, Hérison J, Képès F (2012) Genomic organization of evolutionarily correlated genes in bacteria: limits and strategies. J Mol Biol 419(5):369–386PubMedCrossRefGoogle Scholar
  86. 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(1):75–86PubMedCrossRefGoogle Scholar
  87. Képès F (2004) Periodic transcriptional organization of the E. coli chromosome. J Mol Biol 340(5):957–964PubMedCrossRefGoogle Scholar
  88. Klose KE, North AK, Stedman KM et al (1994) The major dimerization determinants of the nitrogen regulatory protein NtrC from enteric bacteria lie in its carboxy-terminal domain. J Mol Biol 241(2):233–245PubMedCrossRefPubMedCentralGoogle Scholar
  89. Koonin EV (2003) Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat Rev Microbiol 1(2):127–136PubMedCrossRefPubMedCentralGoogle Scholar
  90. Kotlajich MV, Hron DR, Boudreau BA et al (2015) Bridged filaments of histone-like nucleoid structuring protein pause RNA polymerase and aid termination in bacteria. elife 4:e04970PubMedCentralCrossRefGoogle Scholar
  91. Kröger C, Dillon SC, Cameron AD et al (2012) The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc Natl Acad Sci USA 109(20):E1277–E1286PubMedCrossRefGoogle Scholar
  92. Kudva R, Denks K, Kuhn P et al (2013) Protein translocation across the inner membrane of Gram-negative bacteria: the Sec and Tat dependent protein transport pathways. Res Microbiol 164(6):505–534PubMedCrossRefGoogle Scholar
  93. Lal A, Dhar A, Trostel A et al (2016) Genome scale patterns of supercoiling in a bacterial chromosome. Nat Commun 7:11055PubMedPubMedCentralCrossRefGoogle Scholar
  94. Lan G, Tu Y (2016) Information processing in bacteria: memory, computation, and statistical physics: a key issues review. Rep Prog Phys 79(5):052601PubMedPubMedCentralCrossRefGoogle Scholar
  95. Lawson CL, Swigon D, Murakami KS (2004) Catabolite activator protein: DNA binding and transcription activation. Curr Opin Struct Biol 14:1):10–1):20PubMedPubMedCentralCrossRefGoogle Scholar
  96. Lazarus LR, Travers AA (1993) The Escherichia coli FIS protein is not required for the activation of tyrT transcription on entry into exponential growth. EMBO J 12(6):2483–2494PubMedPubMedCentralCrossRefGoogle Scholar
  97. Lee EJ, Pontes MH, Groisman EA (2013) A bacterial virulence protein promotes pathogenicity by inhibiting the bacterium’s own F1Fo ATP synthase. Cell 154(1):146–156PubMedPubMedCentralCrossRefGoogle Scholar
  98. Leela JK, Syeda AH, Anupama K et al (2013) Rho-dependent transcription termination is essential to prevent excessive genome-wide R-loops in Escherichia coli. Proc Natl Acad Sci USA 110(1):258–263PubMedCrossRefGoogle Scholar
  99. Lithgow JK, Haider F, Roberts IS et al (2007) Alternate SlyA and H-NS nucleoprotein complexes control hlyE expression in Escherichia coli K-12. Mol Microbiol 66(3):685–698PubMedPubMedCentralCrossRefGoogle Scholar
  100. Liu LF, Wang JC (1987) Supercoiling of the DNA template during transcription. Proc Natl Acad Sci USA 84(20):7024–7027PubMedCrossRefGoogle Scholar
  101. Lloyd GS, Niu W, Tebbutt J et al (2002) Requirement for two copies of RNA polymerase alpha subunit C-terminal domain for synergistic transcription activation at complex bacterial promoters. Genes Dev 16(19):2557–2565PubMedPubMedCentralCrossRefGoogle Scholar
  102. Lucchini S, Rowley G, Goldberg MD et al (2006) H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog 2(8):e81PubMedPubMedCentralCrossRefGoogle Scholar
  103. Ma J, Wang M (2014) Interplay between DNA supercoiling and transcription elongation. Transcription 5(3):e28636PubMedPubMedCentralCrossRefGoogle Scholar
  104. Ma CK, Kolesnikow T, Rayner JC et al (1994) Control of translation by mRNA secondary structure: the importance of the kinetics of structure formation. Mol Microbiol 14(5):1033–1047PubMedCrossRefGoogle Scholar
  105. Majdalani N, Cunning C, Sledjeski D et al (1998) DsrA RNA regulates translation of RpoS message by an anti-sense mechanism, independent of its action as an antisilencer of transcription. Proc Natl Acad Sci USA 95(21):12462–12467PubMedCrossRefGoogle Scholar
  106. Majdalani N, Hernandez D, Gottesman S (2002) Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 46(3):813–826PubMedCrossRefGoogle Scholar
  107. Mandin P, Gottesman S (2010) Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J 29(18):3094–3107PubMedPubMedCentralCrossRefGoogle Scholar
  108. Mangan MW, Lucchini S, Danino V et al (2006) The integration host factor (IHF) integrates stationary-phase and virulence gene expression in Salmonella enterica serovar Typhimurium. Mol Microbiol 59(6):1831–1847PubMedCrossRefPubMedCentralGoogle Scholar
  109. Mangan MW, Lucchini S, Ó Croinin T et al (2011) Nucleoid-associated protein HU controls three regulons that coordinate virulence, response to stress and general physiology in Salmonella enterica serovar Typhimurium. Microbiology 157(4):1075–1087PubMedCrossRefPubMedCentralGoogle Scholar
  110. Martínez-Rodríguez L, García-Rodríguez FM, Molina-Sánchez MD et al (2014) Insights into the strategies used by related group II introns to adapt successfully for the colonisation of a bacterial genome. RNA Biol 11(8):1061–1071PubMedPubMedCentralCrossRefGoogle Scholar
  111. Massé E, Escorcia FE, Gottesman S (2003) Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev 17(19):2374–2383PubMedPubMedCentralCrossRefGoogle Scholar
  112. Mathelier A, Carbone A (2010) Chromosomal periodicity and positional networks of genes in Escherichia coli. Mol Syst Biol 6:366PubMedPubMedCentralCrossRefGoogle Scholar
  113. Mekler V, Kortkhonjia E, Mukhopadhyay J et al (2000) Structural organization of bacterial RNA polymerase holoenzyme and the RNA polymerase-promoter open complex. Cell 108(5):599–614CrossRefGoogle Scholar
  114. Montero Llopis P, Jackson AF, Sliusarenko O et al (2010) Spatial organization of the flow of genetic information in bacteria. Nature 466(7302):77–81PubMedCrossRefPubMedCentralGoogle Scholar
  115. Morett E, Bork P (1998) Evolution of new protein function: recombinational enhancer Fis originated by horizontal gene transfer from the transcriptional regulator NtrC. FEBS Lett 433(1–2):108–112PubMedCrossRefPubMedCentralGoogle Scholar
  116. Musatovova O, Dhandayuthapani S, Baseman JB (2006) Transcriptional heat shock response in the smallest known self-replicating cell, Mycoplasma genitalium. J Bacteriol 188(8):2845–2855PubMedPubMedCentralCrossRefGoogle Scholar
  117. Muskhelishvili G, Travers A (2003) Transcription factor as a topological homeostat. Front Biosci 8:d279–d285PubMedCrossRefPubMedCentralGoogle Scholar
  118. Navarre WW, Porwollik S, Wang Y et al (2006) Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313(5784):236–238PubMedCrossRefPubMedCentralGoogle Scholar
  119. Naville M, Gautheret D (2009) Transcription attenuation in bacteria: theme and variations. Brief Funct Genomic Proteomic 8(6):482–492PubMedCrossRefPubMedCentralGoogle Scholar
  120. Ní Bhriain N, Dorman CJ, Higgins CF (1989) An overlap between osmotic and anaerobic stress responses: a potential role for DNA supercoiling in the coordinate regulation of gene expression. Mol Microbiol 3(7):933–942PubMedCrossRefPubMedCentralGoogle Scholar
  121. Nilsson P, Uhlin BE (1991) Differential decay of a polycistronic Escherichia coli transcript is initiated by RNaseE-dependent endonucleolytic processing. Mol Microbiol 5(7):1791–1799PubMedCrossRefGoogle Scholar
  122. Nilsson L, Vanet A, Vijgenboom E et al (1990) The role of FIS in trans activation of stable RNA operons of E. coli. EMBO J 9(3):727–734PubMedPubMedCentralCrossRefGoogle Scholar
  123. Nomura M, Yates JL, Dean D et al (1980) Feedback regulation of ribosomal protein gene expression in Escherichia coli: structural homology of ribosomal RNA and ribosomal protein mRNA. Proc Natl Acad Sci USA 77(12):7084–7088PubMedCrossRefGoogle Scholar
  124. Novikova O, Topilina N, Belfort M (2014) Enigmatic distribution, evolution, and function of inteins. J Biol Chem 289(21):14490–14497PubMedPubMedCentralCrossRefGoogle Scholar
  125. Nudler E (2012) RNA polymerase backtracking in gene regulation and genome instability. Cell 149(7):1438–1445PubMedCrossRefGoogle Scholar
  126. Nudler E, Gottesman ME (2002) Transcription termination and anti-termination in E. coli. Genes Cells 7(8):755–768PubMedCrossRefGoogle Scholar
  127. Nyström T (2004) Growth versus maintenance: a trade-off dictated by RNA polymerase availability and sigma factor competition? Mol Microbiol 54(4):855–862PubMedCrossRefPubMedCentralGoogle Scholar
  128. O’Byrne CP, Dorman CJ (1994) The spv virulence operon of Salmonella typhimurium LT2 is regulated negatively by the cyclic AMP (cAMP)-cAMP receptor protein system. J Bacteriol 176(3):905–912PubMedPubMedCentralCrossRefGoogle Scholar
  129. 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(17):2467–2476PubMedCrossRefGoogle Scholar
  130. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405(6784):299–304CrossRefGoogle Scholar
  131. Oliver P, Peralta-Gil M, Tabche ML et al (2016) Molecular and structural considerations of TF-DNA binding for the generation of biologically meaningful and accurate phylogenetic footprinting analysis: the LysR-type transcriptional regulator family as a study model. BMC Genomics 17:686. CrossRefPubMedPubMedCentralGoogle Scholar
  132. Oshima T, Ishikawa S, Kurokawa K et al (2006) Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase. DNA Res 13(4):141–153PubMedCrossRefPubMedCentralGoogle Scholar
  133. Park HS, Ostberg Y, Johansson J et al (2010) Novel role for a bacterial nucleoid protein in translation of mRNAs with suboptimal ribosome-binding sites. Genes Dev 24(13):1345–1350PubMedPubMedCentralCrossRefGoogle Scholar
  134. Pedersen AG, Jensen LJ, Brunak S et al (2000) A DNA structural atlas for Escherichia coli. J Mol Biol 299(4):907–930PubMedCrossRefPubMedCentralGoogle Scholar
  135. Perez JC, Groisman EA (2009a) Evolution of transcriptional regulatory circuits in bacteria. Cell 138(2):233–244PubMedPubMedCentralCrossRefGoogle Scholar
  136. Perez JC, Groisman EA (2009b) Transcription factor function and promoter architecture govern the evolution of bacterial regulons. Proc Natl Acad Sci USA 106(11):4319–4324PubMedCrossRefPubMedCentralGoogle Scholar
  137. Perez JC, Latifi T, Groisman EA (2008) Overcoming H-NS-mediated transcriptional silencing of horizontally acquired genes by the PhoP and SlyA proteins in Salmonella enterica. J Biol Chem 283(16):10773–10783PubMedPubMedCentralCrossRefGoogle Scholar
  138. Peterson SN, Reich NO (2010) LRP: a nucleoid-associated protein with gene regulatory properties. In: Dame RT, Dorman CJ (eds) Bacterial chromatin. Springer, Dordrecht, pp 353–364CrossRefGoogle Scholar
  139. Peterson SN, Dahlquist FD, Reich NO (2007) The role of high affinity non-specific DNA binding by Lrp in transcriptional regulation and DNA organization. J Mol Biol 369(5):1307–1317PubMedCrossRefPubMedCentralGoogle Scholar
  140. Price MN, Dehal PS, Arkin AP (2008) Horizontal gene transfer and the evolution of transcriptional regulation in Escherichia coli. Genome Biol 9:R4PubMedPubMedCentralCrossRefGoogle Scholar
  141. Price MN, Wetmore KM, Deutschbauer AM et al (2016) A comparison of the costs and benefits of bacterial gene expression. PLoS One 11(10):e0164314PubMedPubMedCentralCrossRefGoogle Scholar
  142. Puente JL, Verdugo-Rodríguez A, Calva E (1991) Expression of Salmonella typhi and Escherichia coli OmpC is influenced differently by medium osmolarity; dependence on Escherichia coli OmpR. Mol Microbiol 5(5):1205–1210PubMedCrossRefPubMedCentralGoogle Scholar
  143. 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(3):e1004215PubMedPubMedCentralCrossRefGoogle Scholar
  144. Rajkowitsch L, Schroeder R (2007) Dissecting RNA chaperone activity. RNA 13(12):2053–2060PubMedPubMedCentralCrossRefGoogle Scholar
  145. Richardson JP (1982) Activation of Rho protein ATPase requires simultaneous interaction at two kinds of nucleic acid binding sites. J Biol Chem 257(10):5760–5766PubMedPubMedCentralGoogle Scholar
  146. Roh K, Safaei FR, Hespanha JP, Proulx SR (2013) Evolution of transcription networks in response to temporal fluctuations. Evolution 67(4):1091–1104PubMedCrossRefPubMedCentralGoogle Scholar
  147. Rohs R, West SM, Sosinsky A, Liu P, Mann RS, Honig B (2009) The role of DNA shape in protein-DNA recognition. Nature 461(7268):1248–1253PubMedPubMedCentralCrossRefGoogle Scholar
  148. Ross W, Gourse RL (2009) Analysis of RNA polymerase-promoter complex formation. Methods 47(1):13–24PubMedCrossRefPubMedCentralGoogle Scholar
  149. Ross W, Thompson JF, Newlands JT et al (1990) E. coli FIS protein activates ribosomal RNA transcription in vitro and in vivo. EMBO J 9(11):3733–3742PubMedPubMedCentralCrossRefGoogle Scholar
  150. Ross W, Gosink KK, Salomon J et al (1993) A third recognition element in bacterial promoters: DNA binding by the alpha subunit of RNA polymerase. Science 262(5138):1407–1413PubMedCrossRefPubMedCentralGoogle Scholar
  151. Saxena S, Gowrishankar J (2011) Compromised factor-dependent transcription termination in a nusA mutant of Escherichia coli: spectrum of termination efficiencies generated by perturbations of Rho, NusG, and H-NS family proteins. J Bacteriol 193(15):3842–3850PubMedPubMedCentralCrossRefGoogle Scholar
  152. Schell MA (1993) Molecular biology of the LysR family of transcriptional regulators. Annu Rev Microbiol 47:597–626PubMedCrossRefPubMedCentralGoogle Scholar
  153. Schellhorn HE (2014) Elucidating the function of the RpoS regulon. Future Microbiol 9(4):497–507PubMedCrossRefPubMedCentralGoogle Scholar
  154. Schneewind O, Missiakas D (2014) Sec-secretion and sortase-mediated anchoring of proteins in Gram-positive bacteria. Biochim Biophys Acta 1843(8):1687–1697PubMedCrossRefPubMedCentralGoogle Scholar
  155. Sedlyarova N, Shamovsky I, Bharati BK et al (2016) sRNA-mediated control of transcription termination in E. coli. Cell 167(1):111–121PubMedPubMedCentralCrossRefGoogle Scholar
  156. Sheehan BJ, Dorman CJ (1988) 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(1):91–105CrossRefGoogle Scholar
  157. Singh SS, Singh N, Bonocora RP et al (2014) Widespread suppression of intragenic transcription initiation by H-NS. Genes Dev 28(3):214–219PubMedPubMedCentralCrossRefGoogle Scholar
  158. Skordalakes E, Berger JM (2003) Structure of the Rho transcription terminator: mechanism of mRNA recognition and helicase loading. Cell 114(1):135–146PubMedCrossRefPubMedCentralGoogle Scholar
  159. Slattery M, Zhou T, Yang L, Dantas Machado AC, Gordân R, Rohs R (2014) Absence of a simple code: how transcription factors read the genome. Trends Biochem Sci 39(9):381–399PubMedPubMedCentralCrossRefGoogle Scholar
  160. Snoep JL, van der Weijden CC, Andersen HW et al (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(6):1662–1669PubMedCrossRefPubMedCentralGoogle Scholar
  161. 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 USA 109(2):E42–E50PubMedCrossRefGoogle Scholar
  162. Steitz TA (2009) The structural changes of T7 RNA polymerase from transcription initiation to elongation. Curr Opin Struct Biol 19(6):683–690PubMedPubMedCentralCrossRefGoogle Scholar
  163. Stincone A, Daudi N, Rahman AS et al (2011) A systems biology approach sheds new light on Escherichia coli acid resistance. Nucleic Acids Res 39(17):7512–7528PubMedPubMedCentralCrossRefGoogle Scholar
  164. Stoebel DM, Free A, Dorman CJ (2008) Anti-silencing: overcoming H-NS-mediated repression of transcription in Gram-negative enteric bacteria. Microbiology 154(9):2533–2545PubMedCrossRefPubMedCentralGoogle Scholar
  165. Syvanen M (2012) Evolutionary implications of horizontal gene transfer. Annu Rev Genet 46:341–358PubMedCrossRefPubMedCentralGoogle Scholar
  166. Tapias A, Lopez G, Ayora S (2000) Bacillus subtilis LrpC is a sequence-independent DNA-binding and DNA-bending protein which bridges DNA. Nucleic Acids Res 28(2):552–559PubMedPubMedCentralCrossRefGoogle Scholar
  167. Thomas CM, Nielsen KM (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3(9):711–721PubMedCrossRefPubMedCentralGoogle Scholar
  168. Travers A, Muskhelishvili G (2005) DNA supercoiling – a global transcriptional regulator for enterobacterial growth? Nat Rev Microbiol 3(2):157–169PubMedCrossRefPubMedCentralGoogle Scholar
  169. Trentini DB, Suskiewicz MJ, Heuck A et al (2016) Arginine phosphorylation marks proteins for degradation by a Clp protease. Nature 539(7627):48–53PubMedCrossRefPubMedCentralGoogle Scholar
  170. van Workum M, van Dooren SJ, Oldenburg N et al (1996) DNA supercoiling depends on the phosphorylation potential in Escherichia coli. Mol Microbiol 20(2):351–360PubMedCrossRefPubMedCentralGoogle Scholar
  171. Verstraeten N, Knapen W, Fauvart M et al (2016) A historical perspective on bacterial persistence. Methods Mol Biol 1333:3–13PubMedCrossRefPubMedCentralGoogle Scholar
  172. Vinograd J, Lebowitz J, Radloff R et al (1965) The twisted circular form of polyoma viral DNA. Proc Natl Acad Sci USA 53(5):1104–1111PubMedCrossRefPubMedCentralGoogle Scholar
  173. Wagner EG, Romby P (2015) Small RNAs in bacteria and archaea: who they are, what they do, and how they do it. Adv Genet 90:133–208PubMedPubMedCentralGoogle Scholar
  174. Wagner EG, Simons RW (1994) Antisense RNA control in bacteria, phages, and plasmids. Annu Rev Microbiol 48:713–742PubMedCrossRefPubMedCentralGoogle Scholar
  175. Waldron DE, Owen P, Dorman CJ (2002) Competitive interaction of the OxyR DNA-binding protein and the Dam methylase at the antigen 43 gene regulatory region in Escherichia coli. Mol Microbiol 44(2):509–520PubMedCrossRefPubMedCentralGoogle Scholar
  176. Wang JD, Levin PA (2009) Metabolism, cell growth and the bacterial cell cycle. Nat Rev Microbiol 7(11):822–827PubMedPubMedCentralCrossRefGoogle Scholar
  177. Wang D, Guo C, Gu L et al (2014) Comparative study of the marR genes within the family Enterobacteriaceae. J Microbiol 52(6):452–459PubMedCrossRefGoogle Scholar
  178. Weiss V, Kramer G, Dünnebier T et al (2002) Mechanism of regulation of the bifunctional histidine kinase NtrB in Escherichia coli. J Mol Microbiol Biotechnol 4(3):229–233PubMedGoogle Scholar
  179. Werner F, Grohmann D (2011) Evolution of multisubunit RNA polymerases in the three domains of life. Nat Rev Microbiol 9(2):85–98PubMedCrossRefGoogle Scholar
  180. Wimberly H, Shee C, Thornton PC et al (2013) R-loops and nicks initiate DNA breakage and genome instability in non-growing Escherichia coli. Nat Commun 4:2115PubMedPubMedCentralCrossRefGoogle Scholar
  181. Wright MA, Kharchenko P, Church GM, Segrè D (2007) Chromosomal periodicity of evolutionarily conserved gene pairs. Proc Natl Acad Sci USA 104(25):10559–10564PubMedCrossRefGoogle Scholar
  182. Wu HY, Shyy SH, Wang JC et al (1988) Transcription generates positively and negatively supercoiled domains in the template. Cell 53(3):433–440PubMedCrossRefGoogle Scholar
  183. 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(3):445–451PubMedCrossRefGoogle Scholar
  184. Yanofsky C, Platt T, Crawford IP et al (1981) The complete nucleotide sequence of the tryptophan operon of Escherichia coli. Nucleic Acids Res 9(24):6647–6668PubMedPubMedCentralCrossRefGoogle Scholar
  185. Zenkin N (2014) Ancient RNA stems that terminate transcription. RNA Biol 11(4):295–297PubMedPubMedCentralCrossRefGoogle Scholar
  186. Zhang W, Baseman JB (2014) Functional characterization of osmotically inducible protein C (MG_427) from Mycoplasma genitalium. J Bacteriol 196(5):1012–1019PubMedPubMedCentralCrossRefGoogle Scholar
  187. Zhang X, Schleif R (1998) Catabolite gene activator protein mutations affecting activity of the araBAD promoter. J Bacteriol 180(2):195–200PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Charles J. Dorman
    • 1
    Email author
  • Niamh Ní Bhriain
    • 1
  • Matthew J. Dorman
    • 2
  1. 1.Department of MicrobiologyMoyne Institute of Preventive MedicineDublin 2Ireland
  2. 2.Wellcome Sanger Institute, Wellcome Genome CampusHinxtonUK

Personalised recommendations