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Volume 156, Issue 8

Regulation of the promoter: interplay between five transcription factors Free

Abstract

Under stressful conditions in nature, forms biofilms for long-term survival. Curli fimbriae are an essential architecture for cell–cell contacts within biofilms. Structural components and assembly factors of curli are encoded by two operons, and . The gene product controls transcription of both operons. Reflecting the response of expression to external stresses, a number of transcription factors participate in the regulation of the promoter. Analysis of the mRNA obtained from mutants in different transcription factors indicated that CpxR and H-NS act as repressors while OmpR, RstA and IHF act as activators. An acid-stress response regulator, RstA, activates only under acidic conditions. These five factors bind within a narrow region of about 200 bp upstream of the promoter. After pair-wise promoter-binding assays, the increase in transcription in the stationary phase was suggested to be due, at least in part, to the increase in IHF level cancelling the silencing effect of H-NS. In addition, we propose a novel regulation model of this complex promoter through cooperation between the two positive factors (OmpR–IHF and RstA–IHF) and also between the two negative factors (CpxR–H-NS).

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2010-08-01
2024-04-26
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References

  1. Aiba H., Nakasai F., Mizushima S., Mizuno T. 1989; Phosphorylaton of a bacterial activator protein, OmpR, by a protein kinase, EnvZ, results in stimulation of its DNA-binding ability. J Biochem 106:5–7
     [Google Scholar]
  2. Amit R., Oppenheim A. B., Stavans J. 2003; Increased bending rigidity of single DNA molecules by H-NS, a temperature and osmolarity sensor. Biophys J 84:2467–2473
     [Google Scholar]
  3. Arnqvist A., Olsen A., Normark S. 1994; Sigma S-dependent growth-phase induction of the csgBA promoter in Escherichia coli can be achieved in vivo by sigma 70 in the absence of the nucleoid-associated protein H-NS. Mol Microbiol 13:1021–1032
     [Google Scholar]
  4. Azam T. A., Ishihama A. 1999; Twelve species of DNA-binding protein from Escherichia coli: sequence recognition specificity and DNA binding affinity. J Biol Chem 274:33105–33113
     [Google Scholar]
  5. Azam T. A., Iwata A., Nishimura A., Ueda S., Ishihama A. 1999; Growth phase-dependent variation in the protein composition of Escherichia coli nucleoid. J Bacteriol 181:6361–6370
     [Google Scholar]
  6. Barnhart M. M., Chapman M. R. 2006; Curli biogenesis and function. Annu Rev Microbiol 60:131–147
     [Google Scholar]
  7. Beloin C., Valle J., Latour-Lambert P., Faure P., Kzreminski J., Balestriono D., Haagensen J. A., Molin S., Prensier G. other authors 2004; Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 51:659–674
     [Google Scholar]
  8. Bian Z., Brauner A., Li Y., Normark S. 2000; Expression of and cytokine activation by Escherichia coli curli fibers in human sepsis. J Infect Dis 181:602–612
     [Google Scholar]
  9. Bougdour A., Gottesman S. 2007; ppGpp regulation of RpoS degradation via anti-adaptor IraP. Proc Natl Acad Sci U S A 104:12896–12901
     [Google Scholar]
  10. Bougdour A., Lelong C., Geiselmann J. 2004; Crl, a low temperature-induced protein in Escherichia coli that binds directly to the stationary phase sigma subunit of RNA polymerase. J Biol Chem 279:19540–19550
     [Google Scholar]
  11. Brombacher E., Dorel C., Zehnder A. J., Landini P. 2003; The curli biosynthesis regulator CsgD co-ordinates the expression of both positive and negative determinants for biofilm formation in Escherichia coli. Microbiology 149:2847–2857
     [Google Scholar]
  12. Brombacher E., Baratto A., Dorel C., Landini P. 2006; Gene expression regulation by the curli activator CsgD protein: modulation of cellulose biosynthesis and control of negative determinants for microbial adhesion. J Bacteriol 188:2027–2037
     [Google Scholar]
  13. Brown P. K., Dozois C. M., Nickerson C. A., Zupardo A., Terlonge J., Curtiss R. III 2001; MlrA, a novel regulator curli (AgF) and exracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium. Mol Microbiol 41:349–363
     [Google Scholar]
  14. Busby S., Ebright R. 1999; Transcription activation by catabolite activator protein (CAP. J Mol Biol 293:199–213
     [Google Scholar]
  15. Cabeza M. L., Aguirre A., Soncini F. C., Vescovi E. G. 2007; Induction of RpoS degradation by the two-component system regulator RstA in Salmonella enterica. J Bacteriol 189:7335–7342
     [Google Scholar]
  16. Chapman M. R., Robinson L. S., Pinkner J. S., Roth R., Heuser J., Hammar M., Normark S., Hultgren S. J. 2002; Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295:851–855
     [Google Scholar]
  17. Chirwa N. T., Herrington M. B. 2003; CsgD, a regulator of curli and cellulose synthesis, also regulates serine hydroxymethyltransferase synthesis in Escherichia coli K-12. Microbiology 149:525–535
     [Google Scholar]
  18. Claret L., Hughes C. 2000; Functions of the subunits in the FlhD2C2 transcriptional master regulator of bacterial flagellum biogenesis and swarming. J Mol Biol 303:467–478
     [Google Scholar]
  19. Cookson A. L., Cooley W. A., Woodard W. J. 2002; The role of type 1 and curli fimbriae of Shiga toxin-producing Escherichia coli in adherence to abiotic surfaces. Int J Med Microbiol 292:195–205
     [Google Scholar]
  20. Dame R. T., Luijsterburg M. S., Krin E., Bertin P. N., Wagner R., Wuite G. J. L. 2005; DNA bridging: a property shared among H-NS-like proteins. J Bacteriol 187:1845–1848
     [Google Scholar]
  21. Dorman C. J. 2004; H-NS: a universal regulator for a dynamic genome. Nat Rev Microbiol 2:391–400
     [Google Scholar]
  22. Ferrieres L., Clarke D. J. 2003; The RcsC sensor kinase is required for normal biofilm formation in Escherichia coli K-12 and controls the expression of a regulon in response to growth on a solid surface. Mol Microbiol 50:1665–1682
     [Google Scholar]
  23. Gerstel U., Romling U. 2001; Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environ Microbiol 3:638–648
     [Google Scholar]
  24. Gerstel U., Park C., Romling U. 2003; Complex regulation of csgD promoter activity by global regulatory proteins. Mol Microbiol 49:639–654
     [Google Scholar]
  25. Gerstel U., Kolb A., Romling U. 2006; Regulatory components at the csgD promoter: additional roles for OmpR and integration host factor and role of the 5′ untranslated region. FEMS Microbiol Lett 261:109–117
     [Google Scholar]
  26. Gophna U., Barlev M., Seijffers R., Oelschlager T. A., Hacker J., Ron E. Z. 2001; Curli fibers mediate internalization of Escherichia coli by eukaryotic cells. Infect Immun 69:2659–2665
     [Google Scholar]
  27. Gualdi L., Tagliabue L., Landini P. 2007; Biofilm formation-gene expression relay system in Escherichia coli: modulation of sigma S-dependent gene expression by the CsgD regulatory protein via sigma S protein stabilization. J Bacteriol 189:8034–8043
     [Google Scholar]
  28. Hammar M., Arnqvist A., Bian Z., Olsen A., Normark S. 1995; Expression of two csg operons is required for production of fibronectin- and congo red-binding curli polymers in Escherichia coli K-12. Mol Microbiol 18:661–670
     [Google Scholar]
  29. Harlocker S. L., Bergstrom L., Inouye M. 1995; Tandem binding of six OmpR proteins to the ompF upstream regulatory sequence of Escherichia coli. J Biol Chem 270:26849–26856
     [Google Scholar]
  30. Ishihama A. 1993; Protein-protein communication within the transcription apparatus. J Bacteriol 175:2483–2489
     [Google Scholar]
  31. Ishihama A. 1999; Modulation of the nucleoid, the transcription apparatus, and the translation machinery in bacteria for stationary phase survival. Genes Cells 4:135–143
     [Google Scholar]
  32. Ishihama A. 2009; The nucleoid: an overview. In EcoSal – Escherichia coli and Salmonella: Cellular and Molecular Biology Edited by Boek A. and others Washington, DC: American Society for Microbiology;
     [Google Scholar]
  33. Ishihama A. 2010; Prokaryotic genome regulation: multi-factor promoters, multi-target regulators and multi-factor networks. FEMS Microbiol RevApr 14: [Epub ahead of print]
    [Google Scholar]
  34. Jishage M., Iwata A., Ueda S., Ishihama A. 1996; Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of four species of sigma subunit under various growth conditions. J Bacteriol 178:5447–5451
     [Google Scholar]
  35. Jubelin G., Vianney A., Beloin C., Ghigo J.-M., Lazzaroni J.-C., Lejeune P., Dorel C. 2005; CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J Bacteriol 187:2038–2049
     [Google Scholar]
  36. Kolb A., Kotlarz D., Kusano S., Ishihama A. 1995; Selectivity of the Escherichia coli RNA polymerase E σ38 for overlapping promoters and ability to support CRP activation. Nucleic Acids Res 23:819–826
     [Google Scholar]
  37. Lacqua A., Wanner O., Colanglo T., Martinotti M. G., Landini P. 2006; Emergence of biofilm-forming subpopulations upon exposure of Escherichia coli to environmental baceriophages. Appl Environ Microbiol 72:956–959
     [Google Scholar]
  38. Latasa C., Roux A., Toledo-Arana A., Ghigo J. M., Gamazo C., Penadés J. R., Lasa I. 2005; BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol Microbiol 58:1322–1339
     [Google Scholar]
  39. Loferer H., Hammar M., Normark S. 1997; Availability of the fibre subunit CsgA and the nucleator protein CsgB during assembly of fibronection binding curli is limited by the intracellular concentration of the novel lipoprotein CsgG. Mol Microbiol 26:11–23
     [Google Scholar]
  40. Maeda H., Jishage M., Nomura T., Fujita F., Ishihama A. 2000; Extracytoplasmic function sigma subunits, sigma E and sigma FecI, of Escherichia coli: promoter selectivity and intracellular levels. J Bacteriol 182:1181–1184
     [Google Scholar]
  41. Minagawa S., Ogasawara H., Kato A., Yamamoto K., Eguchi T., Mori H., Ishihama A., Utsumi R. 2003; Identification and molecular characterization of the Mg(II) stimulon of Escherichia coli. J Bacteriol 185:3696–3702
     [Google Scholar]
  42. Murakami K., Fujita N., Ishihama A. 1996; Transcription factor recognition surface on the RNA polymerase a subunit is involved in contact with the DNA enhancer element. EMBO J 15:4358–4367
     [Google Scholar]
  43. Navarre W.W., Porwollik S., Wang Y., McClelland M., Rosen H., Libby S. J., Fang F.C. 2006; Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313:236–238
     [Google Scholar]
  44. Niba E. T. E., Naka Y., Nagase M., Mori H., Kitakawa M. 2007; A genome-wide approach to identify the genes involved in biofilm formation in E. coli. DNA Res 14:237–246
     [Google Scholar]
  45. Ogasawara H., Hasegawa A., Kanda E., Miki T., Yamamoto K., Ishihama A. 2007a; Genomic SELEX search for target genes under the control of PhoQP-RstBA signal relay cascade. J Bacteriol 189:4791–4799
     [Google Scholar]
  46. Ogasawara H., Ishida Y., Yamada K., Yamamoto K., Ishihama A. 2007b; PdhR (pyruvate dehydrogenase complex regulator) controls the respiratory electron transport system in Escherichia coli. J Bacteriol 189:5534–5541
     [Google Scholar]
  47. Olsen A., Arnqqvist A., Hammar H., Sukupolvi S., Normark S. 1993; The RpoS sigma factor relieves H-NS-mediated transcriptional repression of csgA, the subunit gene of fibronectin-binding curli in Escherichia coli. Mol Microbiol 7:523–536
     [Google Scholar]
  48. Otto K., Silhavy T. J. 2002; Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc Natl Acad Sci U S A 99:2287–2292
     [Google Scholar]
  49. Pedersen A. G., Jensen L. J., Brunak S., Sterfeldt H. H., Ussery D. W. 2000; A DNA structural atlas for Escherichia coli. J Mol Biol 299:907–930
     [Google Scholar]
  50. Pogliano J., Lynch A. S., Berlin D., Lin E. C. C., Beckwith J. 1997; Regulation of Escherichia coli cell envelope proteins involved in protein folding and degradation by the Cpx two-component system. Genes Dev 11:1169–1182
     [Google Scholar]
  51. Pratt L. A., Silhavy T. J. 1995; Identification of base pairs important for OmpR-DNA interaction. Mol Microbiol 17:565–573
     [Google Scholar]
  52. Pratt L. A., Silhavy T. J. 1998; Crl stimulates RpoS activity during stationary phase. Mol Microbiol 29:1225–1236
     [Google Scholar]
  53. Prigent-Combaret C., Vidal O., Dorel C., Lejeune P. 1999; Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J Bacteriol 181:5993–6002
     [Google Scholar]
  54. Prigent-Combaret C., Prensier G., Le Thi T. T., Vidal O., Pejeunne P., Dorel C. 2000; Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ Microbiol 2:450–464
     [Google Scholar]
  55. Prigent-Combaret C., Brombacher E., Vidal O., Ambert A., Lejeune P., Landini P., Dorel C. 2001; Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J Bacteriol 183:7213–7223
     [Google Scholar]
  56. Raivio T. L., Silhavy T. J. 1997; Transduction of envelope stress in Escherichia coli by the Cpx two-component system. J Bacteriol 179:7724–7733
     [Google Scholar]
  57. Ren D., Bedzyk L. A., Thomas S. M., Ye R. W., Wood T. K. 2004; Gene expression in Escherichia coli biofilms. Appl Microbiol Biotechnol 64:515–524
     [Google Scholar]
  58. Rice P. A., Yang S., Mizuuchi K., Nash H. A. 1996; Crystal structure of an IHF-DNA complex; a protein-induced DNA U-turn. Cell 87:1295–1306
     [Google Scholar]
  59. Robbe-Saule V., Jaumouille V., Prevost M.-C., Gaudagnini S., Talhouarne C., Mathout H., Kolb A., Norel F. 2006; Crl activates transcription initiation of RpoS-regulated genes involved in the multicellular behavior of Salmonella enterica serovar typhimurium. J Bacteriol 188:3983–3994
     [Google Scholar]
  60. Romling U., Sierralta W. D., Eriksson K., Normark S. 1998; Multicellular and aggregative behavior of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol Microbiol 28:249–264
     [Google Scholar]
  61. Romling U., Rohde M., Olsen A., Normark S., Reinkoster J. 2000; AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 36:10–23
     [Google Scholar]
  62. Schembri M. A., Kjaergaard K., Klemm P. 2003; Global gene expression in Escherichia coli biofilms. Mol Microbiol 48:253–267
     [Google Scholar]
  63. Shimada T., Hirao K., Kori A., Yamamoto K., Ishihama A. 2007; RutR is the uracil/thymine-sensing master regulator of a set of genes for synthesis and degradation of pyrimdines. Mol Microbiol 66:744–757
     [Google Scholar]
  64. Simm R., Morr M., Kader A., Nimtz M., Romling U. 2004; GGDEF and EAL domains inversely regulate cyclic d-GMP levels and transition from sessility to motility. Mol Microbiol 53:1123–1134
     [Google Scholar]
  65. Simons R. W., Houman F., Kleckner N. 1987; Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53:85–96
     [Google Scholar]
  66. Snyder W. B., Davis L. J., Danese P. N., Cosma C. L., Silhavy T. J. 1995; Overproduction of NlpE, a new outer membrane lipoprotein, suppresses the toxicity of periplasmic LacZ by activation of the Cpx signal transduction pathway. J Bacteriol 177:4216–4223
     [Google Scholar]
  67. Sugiura M., Aiba H., Mizuno T. 2003; Identification and classification of two-component systems that affect rpoS expression in Escherichia coli. Biosci Biotechnol Biochem 67:1612–1615
     [Google Scholar]
  68. Sutherland I. 2001; Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147:3–9
     [Google Scholar]
  69. Suziedeliene E., Suziedelis V., Garbenciute V., Normark S. 1999; The acid-inducible asr gene in Escherichia coli: transcriptional control by the phoBR operon. J Bacteriol 181:2084–2093
     [Google Scholar]
  70. Tanaka K., Kusano S., Fujita N., Ishihama A., Takahashi H. 1995; Promoter determinants for Escherichia coli RNA polymerase holoenzyme containing σ38 (the rpoS gene product. Nucleic Acids Res 23:827–834
     [Google Scholar]
  71. Umezawa Y., Ogasawara H., Shimada T., Kori A., Ishihama A. 2008; The uncharacterized YdhM is the regulator of the nemA gene, coding for N-ethylmaleimide reductase. J Bacteriol 190:5890–5897
     [Google Scholar]
  72. Vianney A., Jubelin G., Renault S., Dorel C., Lejeune P., Lazzaroni J. C. 2005; Escherichia coli tol and rcs genes participate in the complex network affecting curli synthesis. Microbiology 151:2487–2497
     [Google Scholar]
  73. Vidal O., Longain R., Prigent-Combaret C., Dorel C., Hooreman M., Lejeune P. 1998; Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression. J Bacteriol 180:2442–2449
     [Google Scholar]
  74. Wang X., Preston J. F. III, Romeo T. 2004; The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J Bacteriol 186:2724–2734
     [Google Scholar]
  75. Wang X., Smith D. R., Jones J. W., Chapman M. R. 2007; In vitro polymerization of a functional Escherichia coli amyloid protein. J Biol Chem 282:3713–3719
     [Google Scholar]
  76. Yamamoto K., Ishihama A. 2006; Characterization of copper-inducible promoters regulated by CpxA/CpxR in Escherichia coli. Biosci Biotechnol Biochem 70:1688–1695
     [Google Scholar]
  77. Yamamoto K., Hirano K., Ohshima T., Aiba H., Utsumi R., Ishihama A. 2005; Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J Biol Chem 280:1448–1456
     [Google Scholar]
  78. Zheng D., Constantinidou C., Hobman J. L., Minchin S. D. 2004; Identification of the CRP regulon using in vitro and in vivo transcriptional profiling. Nucleic Acids Res 32:5874–5893
     [Google Scholar]
  79. Zogaj X., Nimtz M., Rohde M., Bokranz W., Romling U. 2001; The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as second component of the extracellular matrix. Mol Microbiol 39:1452–1463
     [Google Scholar]
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Regulation of the Escherichia coli csgD promoter: interplay between five transcription factors
Microbiology 156, 2470 (2010); https://doi.org/10.1099/mic.0.039131-0
/content/journal/micro/10.1099/mic.0.039131-0
/content/journal/micro/10.1099/mic.0.039131-0
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