1887

Abstract

Curli are necessary for the adherence of to surfaces, and to each other, during biofilm formation, and the and operons are both required for their synthesis. A recent survey of gene expression in biofilms has identified as a gene activated in biofilms. The genes play a fundamental role in maintaining the outer-membrane integrity of Gram-negative bacteria. RcsC, the sensor of the RcsBCD phosphorelay, is involved, together with RcsA, in colanic acid capsule synthesis, and also modulates the expression of and . In addition, the RcsBCD phosphorelay is activated in mutants or when Tol proteins are overexpressed. These results led the authors to investigate the role of the genes in biofilm formation in laboratory and clinical isolates of . It was shown that the adherence of cells was lowered in the mutants. This could be the result of a drastic decrease in the expression of the operon, even though the expression of was slightly increased under such conditions. It was also shown that the Rcs system negatively controls the expression of the two operons in an RcsA-dependent manner. In the mutants, activation of occurred via OmpR and was dominant upon repression by RcsB and RcsA, while these two regulatory proteins repressed through a dominant effect on the activator protein CsgD, thus affecting curli synthesis. The results demonstrate that the Rcs system, previously known to control the synthesis of the capsule and the flagella, is an additional component involved in the regulation of curli. Furthermore, it is shown that the defect in cell motility observed in the mutants depends on RcsB and RcsA.

Keyword(s): A, enzyme activity
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2005-07-01
2020-07-03
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References

  1. Allen-Vercoe E., Dibb-Fuller M., Thorns C. J., Woodward M. J. 1997; SEF17 fimbriae are essential for the convoluted colonial morphology of Salmonella enteritidis . FEMS Microbiol Lett153:33–42[CrossRef]
    [Google Scholar]
  2. Arnqvist A., Olsen A., Pfeifer J., Russell D. G., Normark S. 1992; The Crl protein activates cryptic genes for curli formation and fibronectin binding in Escherichia coli HB101. Mol Microbiol6:2443–2452
    [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 Microbiol13:1021–1032[CrossRef]
    [Google Scholar]
  4. Bernadac A., Gavioli M., Lazzaroni J. C., Raina S., Lloubes R. 1998; Escherichia coli tol-pal mutants form outer membrane vesicles. J Bacteriol180:4872–4878
    [Google Scholar]
  5. Bian Z., Normark S. 1997; Nucleator function of CsgB for the assembly of adhesive surface organelles in Escherichia coli . EMBO J16:5827–5836[CrossRef]
    [Google Scholar]
  6. 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 Chem279:19540–19550[CrossRef]
    [Google Scholar]
  7. Brill J. A., Quinlan-Walshe C., Gottesman S. 1988; Fine-structure mapping and identification of two regulators of capsule synthesis in Escherichia coli K-12. J Bacteriol170:2599–2611
    [Google Scholar]
  8. Brown P. K., Dozois C. M., Nickerson C. A., Zuppardo A., Terlonge J., Curtiss R.. 3rd (2001; MlrA, a novel regulator of curli (AgF) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium. Mol Microbiol41:349–363[CrossRef]
    [Google Scholar]
  9. Cai S. J., Inouye M. 2002; EnvZ-OmpR interaction and osmoregulation in Escherichia coli . J Biol Chem277:24155–24161[CrossRef]
    [Google Scholar]
  10. Carballes F., Bertrand C., Bouche J. P., Cam K. 1999; Regulation of Escherichia coli cell division genes ftsA and ftsZ by the two-component system rcsC-rcsB. Mol Microbiol34:442–450[CrossRef]
    [Google Scholar]
  11. 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. Science295:851–855[CrossRef]
    [Google Scholar]
  12. Chen M. H., Takeda S., Yamada H., Ishii Y., Yamashino T., Mizuno T. 2001; Characterization of the RcsC→YojN→RcsB phosphorelay signaling pathway involved in capsular synthesis in Escherichia coli . Biosci Biotechnol Biochem65:2364–2367[CrossRef]
    [Google Scholar]
  13. Clavel T., Lazzaroni J. C., Vianney A., Portalier R. 1996; Expression of the tolQRA genes of Escherichia coli K-12 is controlled by the RcsC sensor protein involved in capsule synthesis. Mol Microbiol19:19–25[CrossRef]
    [Google Scholar]
  14. Collinson S. K., Emody L., Muller K. H., Trust T. J., Kay W. W. 1991; Purification and characterization of thin, aggregative fimbriae from Salmonella enteritidis . J Bacteriol173:4773–4781
    [Google Scholar]
  15. Davalos-Garcia M., Conter A., Toesca I., Gutierrez C., Cam K. 2001; Regulation of osmC gene expression by the two-component system rcsB-rcsC in Escherichia coli . J Bacteriol183:5870–5876[CrossRef]
    [Google Scholar]
  16. Dorel C., Vidal O., Prigent-Combaret C., Vallet I., Lejeune P. 1999; Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation. FEMS Microbiol Lett178:169–175[CrossRef]
    [Google Scholar]
  17. Ebel W., Vaughn G. J., Peters H. K. 3rd, Trempy J. E. 1997; Inactivation of mdoH leads to increased expression of colanic acid capsular polysaccharide in Escherichia coli . J Bacteriol179:6858–6861
    [Google Scholar]
  18. El-Kazzaz W., Morita T., Tagami H., Inada T., Aiba H. 2004; Metabolic block at early stages of the glycolytic pathway activates the Rcs phosphorelay system via increased synthesis of dTDP-glucose in Escherichia coli . Mol Microbiol51:1117–1128[CrossRef]
    [Google Scholar]
  19. Elliott T. 1992; A method for constructing single-copy lac fusions in Salmonella typhimurium and its application to the hemA-prfA operon. J Bacteriol174:245–253
    [Google Scholar]
  20. Evans D. G., Evans D. J. Jr, Tjoa W. 1977; Hemagglutination of human group A erythrocytes by enterotoxigenic Escherichia coli isolated from adults with diarrhea: correlation with colonization factor. Infect Immun18:330–337
    [Google Scholar]
  21. 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 Microbiol50:1665–1682[CrossRef]
    [Google Scholar]
  22. Francez-Charlot A., Laugel B., Van Gemert A., Dubarry N., Wiorowski F., Castanie-Cornet M. P., Gutierrez C., Cam K. 2003; RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli . Mol Microbiol49:823–832
    [Google Scholar]
  23. Germon P., Clavel T., Vianney A., Portalier R., Lazzaroni J. C. 1998; Mutational analysis of the Escherichia coli K-12 TolA N-terminal region and characterization of its TolQ-interacting domain by genetic suppression. J Bacteriol180:6433–6439
    [Google Scholar]
  24. Gerstel U., Park C., Romling U. 2003; Complex regulation of csgD promoter activity by global regulatory proteins. Mol Microbiol49:639–654
    [Google Scholar]
  25. Gervais F. G., Drapeau G. R. 1992; Identification, cloning, and characterization of rcsF , a new regulator gene for exopolysaccharide synthesis that suppresses the division mutation ftsZ84 in Escherichia coli K-12. J Bacteriol174:8016–8022
    [Google Scholar]
  26. Gottesman S., Stout V. 1991; Regulation of capsular polysaccharide synthesis in Escherichia coli K12. Mol Microbiol5:1599–1606[CrossRef]
    [Google Scholar]
  27. Hagiwara D., Sugiura M., Oshima T., Mori H., Aiba H., Yamashino T., Mizuno T. 2003; Genome-wide analyses revealing a signaling network of the RcsC-YojN-RcsB phosphorelay system in Escherichia coli . J Bacteriol185:5735–5746[CrossRef]
    [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 Microbiol18:661–670[CrossRef]
    [Google Scholar]
  29. Hedblom M. L., Adler J. 1980; Genetic and biochemical properties of Escherichia coli mutants with defects in serine chemotaxis. J Bacteriol144:1048–1060
    [Google Scholar]
  30. Kuo M. S., Chen K. P., Wu W. F. 2004; Regulation of RcsA by the ClpYQ (HslUV) protease in Escherichia coli . Microbiology150:437–446[CrossRef]
    [Google Scholar]
  31. Lazzaroni J. C., Fognini-Lefebvre N., Portalier R. 1986; Effects of lkyB mutations on the expression of ompF , ompC and lamB porin structural genes in E. coli K-12. FEMS Microbiol Lett33:235–239[CrossRef]
    [Google Scholar]
  32. Lazzaroni J. C., Germon P., Ray M. C., Vianney A. 1999; The Tol proteins of Escherichia coli and their involvement in the uptake of biomolecules and outer membrane stability. FEMS Microbiol Lett177:191–197[CrossRef]
    [Google Scholar]
  33. Lejeune P. 2003; Contamination of abiotic surfaces: what a colonizing bacterium sees and how to blur it. Trends Microbiol11:179–184[CrossRef]
    [Google Scholar]
  34. Loferer H., Hammar M., Normark S. 1997; Availability of the fibre subunit CsgA and the nucleator protein CsgB during assembly of fibronectin-binding curli is limited by the intracellular concentration of the novel lipoprotein CsgG. Mol Microbiol26:11–23[CrossRef]
    [Google Scholar]
  35. Majdalani N., Hernandez D., Gottesman S. 2002; Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol46:813–826[CrossRef]
    [Google Scholar]
  36. Miller J. H. 1992; A Short Course in Bacterial Genetics: a Laboratory Manual and Handbook for Escherichia coli and Related Bacteria Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  37. Mouslim C., Groisman E. A. 2003; Control of the Salmonella ugd gene by three two-component regulatory systems. Mol Microbiol47:335–344[CrossRef]
    [Google Scholar]
  38. Olsen A., Arnqvist A., Hammar M., 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 Microbiol7:523–536[CrossRef]
    [Google Scholar]
  39. Ophir T., Gutnick D. L. 1994; A role for exopolysaccharides in the protection of microorganisms from dessication. Appl Environ Microbiol60:740–745
    [Google Scholar]
  40. 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 A99:2287–2292[CrossRef]
    [Google Scholar]
  41. Parker C. T., Kloser A. W., Schnaitman C. A., Stein M. A., Gottesman S., Gibson B. W. 1992; Role of the rfaG and rfaP genes in determining the lipopolysaccharide core structure and cell surface properties of Escherichia coli K-12. J Bacteriol174:2525–2538
    [Google Scholar]
  42. Prigent-Combaret C., Prensier G., Le Thi T. T., Vidal O., Lejeune P., Dorel C. 2000; Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ Microbiol2:450–464[CrossRef]
    [Google Scholar]
  43. 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 Bacteriol183:7213–7223[CrossRef]
    [Google Scholar]
  44. Romling U., Bian Z., Hammar M., Sierralta W. D., Normark S. 1998; Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol180:722–731
    [Google Scholar]
  45. Simons R. W., Houman F., Kleckner N. 1987; Improved single and multicopy lac -based cloning vectors for protein and operon fusions. Gene53:85–96[CrossRef]
    [Google Scholar]
  46. Sledjeski D., Gottesman S. 1995; A small RNA acts as an antisilencer of the H-NS-silenced rcsA gene of Escherichia coli . Proc Natl Acad Sci U S A92:2003–2007[CrossRef]
    [Google Scholar]
  47. Sledjeski D. D., Gottesman S. 1996; Osmotic shock induction of capsule synthesis in Escherichia coli K-12. J Bacteriol178:1204–1206
    [Google Scholar]
  48. Stout V. 1994; Regulation of capsule synthesis includes interactions of the RcsC/RcsB regulatory pair. Res Microbiol145:389–392[CrossRef]
    [Google Scholar]
  49. Stout V., Torres-Cabassa A., Maurizi M. R., Gutnick D., Gottesman S. 1991; RcsA, an unstable positive regulator of capsular polysaccharide synthesis. J Bacteriol173:1738–1747
    [Google Scholar]
  50. Toutain C. M., Clarke D. J., Leeds J. A., Kuhn J., Beckwith J., Holland I. B., Jacq A. 2003; The transmembrane domain of the DnaJ-like protein DjlA is a dimerisation domain. Mol Genet Genomics268:761–770
    [Google Scholar]
  51. Vidal O., Longin 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 Bacteriol180:2442–2449
    [Google Scholar]
  52. Wehland M., Bernhard F. 2000; The RcsAB box. Characterization of a new operator essential for the regulation of exopolysaccharide biosynthesis in enteric bacteria. J Biol Chem275:7013–7020[CrossRef]
    [Google Scholar]
  53. Whiteley M., Bangera M. G., Bumgarner R. E., Parsek M. R., Teitzel G. M., Lory S., Greenberg E. P. 2001; Gene expression in Pseudomonas aeruginosa biofilms. Nature413:860–864[CrossRef]
    [Google Scholar]
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