1887

Abstract

In enterobacteria, the CsgD protein activates production of two extracellular structures: thin aggregative fimbriae (curli) and cellulose. While curli fibres promote biofilm formation and cell aggregation, the evidence for a direct role of cellulose as an additional determinant for biofilm formation is not as straightforward. The MG1655 laboratory strain of only produces limited amounts of curli and cellulose; however, ectopic expression results in strong stimulation of curli and cellulose production. We show that, in a -overexpressing derivative of MG1655, cellulose production negatively affects curli-mediated surface adhesion and cell aggregation, thus acting as a negative determinant for biofilm formation. Consistent with this observation, deletion of the gene, necessary for cellulose production, resulted in a significant increase in curli-dependent adhesion. We found that cellulose production increased tolerance to desiccation, suggesting that the function of cellulose might be related to resistance to environmental stresses rather than to biofilm formation. Production of the curli/cellulose network in enterobacteria typically takes place at low growth temperature (<32 °C), but not at 37 °C. We show that CsgD overexpression can overcome temperature-dependent control of the curli-encoding operon, but not of the cellulose-related gene, suggesting very tight temperature control of cellulose production in MG1655.

Keyword(s): CV, crystal violet
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2008-07-01
2024-04-23
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References

  1. 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]
  2. Ben Nasr A., Olsen A., Sjobring U., Muller-Esterl W., Bjorck L. 1996; Assembly of human contact phase proteins and release of bradykinin at the surface of curli-expressing Escherichia coli. Mol Microbiol 20:927–935
    [Google Scholar]
  3. 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]
  4. Bokranz W., Wang X., Tschape H., Romling U. 2005; Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract. J Med Microbiol 54:1171–1182
    [Google Scholar]
  5. 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]
  6. 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]
  7. Brown W. C., Campbell J. L. 1993; A new cloning vector and expression strategy for genes encoding proteins toxic to Escherichia coli. Gene 127:99–103
    [Google Scholar]
  8. Castonguay M. H., van der Schaaf S., Koester W., Krooneman J., van der Meer W., Harmsen H., Landini P. 2006; Biofilm formation by Escherichia coli is stimulated by synergistic interactions and co-adhesion mechanisms with adherence-proficient bacteria. Res Microbiol 157:471–478
    [Google Scholar]
  9. 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]
  10. Collinson S. K., Emödy L., Müller K.-H., Trust T. J., Kay W. W. 1991; Purification and characterization of thin, aggregative fimbriae from Salmonella enteritidis. J Bacteriol 173:4773–4781
    [Google Scholar]
  11. Doran J. L., Collinson K., Burian J., Sarlos G., Todd E. C. D., Munro C. K., Kay C. M., Banser P. A., Peterkin P. I., Kay W. W. 1993; DNA-based diagnostic tests for Salmonella species targeting agfA, the structural gene for thin, aggregative fimbriae. J Clin Microbiol 31:2263–2273
    [Google Scholar]
  12. 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 Lett 178:169–175
    [Google Scholar]
  13. Gerstel U., Park C., Romling U. 2003; Complex regulation of csgD promoter activity by global regulatory proteins. Mol Microbiol 49:639–654
    [Google Scholar]
  14. Gibson D. L., White A. P., Snyder S. D., Martin S., Heiss C., Azadi P., Surette M., Kay W. W. 2006; Salmonella produces an O-antigen capsule regulated by AgfD and important for environmental persistence. J Bacteriol 188:7722–7730
    [Google Scholar]
  15. 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]
  16. Gualdi L., Tagliabue L., Landini P. 2007; A biofilm formation–gene expression relay system in Escherichia coli: modulation of σS-dependent gene expression by the CsgD regulatory protein via σS protein stabilization. J Bacteriol 189:8034–8043
    [Google Scholar]
  17. 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 Bacteriol 185:5735–5746
    [Google Scholar]
  18. 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]
  19. Hickman J. W., Tifrea D. F., Harwood C. S. 2005; A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci U S A 102:14422–14427
    [Google Scholar]
  20. Kader A., Simm R., Gerstel U., Morr M., Romling U. 2006; Hierarchical involvement of various GGDEF domain proteins in rdar morphotype development of Salmonella enterica serovar Typhimurium. Mol Microbiol 60:602–616
    [Google Scholar]
  21. Latasa C., Roux A., Toledo-Arana A., Ghigo J. M., Gamazo C., Penades 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]
  22. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  23. Olsen A., Arnqvist A., Hammar M., Normark S. 1993; Environmental regulation of curli production in Escherichia coli. Infect Agents Dis 2:272–274
    [Google Scholar]
  24. Paul R., Weiser S., Amiot N. C., Chan C., Schirmer T., Giese B., Jenal U. 2004; Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev 18:715–727
    [Google Scholar]
  25. Persson K., Russell W., Morgelin M., Herwald H. 2003; The conversion of fibrinogen to fibrin at the surface of curliated Escherichia coli bacteria leads to the generation of proinflammatory fibrinopeptides. J Biol Chem 278:31884–31890
    [Google Scholar]
  26. Pratt L. A., Silhavy T. J. 1998; Crl stimulates RpoS activity during stationary phase. Mol Microbiol 29:1225–1236
    [Google Scholar]
  27. 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]
  28. Robbe-Saule V., Jaumouille V., Prevost M. C., Guadagnini 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]
  29. Romling U., Bian Z., Hammar M., Sierralta W. D., Normark S. 1998a; Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 180:722–731
    [Google Scholar]
  30. Romling U., Sierralta W. D., Eriksson K., Normark S. 1998b; Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol Microbiol 28:249–264
    [Google Scholar]
  31. 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]
  32. Sakellaris H., Hannink N. K., Rajakumar K., Bulach D., Hunt M., Sasakawa C., Adler B. 2000; Curli loci of Shigella spp. Infect Immun 68:3780–3783
    [Google Scholar]
  33. Schembri M. A., Dalsgaard D., Klemm P. 2004; Capsule shields the function of short bacterial adhesins. J Bacteriol 186:1249–1257
    [Google Scholar]
  34. Simm R., Morr M., Kader A., Nimtz M., Romling U. 2004; GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53:1123–1134
    [Google Scholar]
  35. Smith H. O., Levine M. 1964; Two sequential repressions of DNA synthesis in the establishment of lysogeny by phage P22 and its mutants. Proc Natl Acad Sci U S A 52:356–363
    [Google Scholar]
  36. Solano C., Garcia B., Valle J., Berasain C., Ghigo J. M., Gamazo C., Lasa I. 2002; Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol Microbiol 43:793–808
    [Google Scholar]
  37. Somogyi M. 1952; Notes on sugar determination. J Biol Chem 195:19–23
    [Google Scholar]
  38. Tischler A. D., Camilli A. 2005; Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect Immun 73:5873–5882
    [Google Scholar]
  39. Uhlich G. A., Keen J. E., Elder R. O. 2001; Mutations in the csgD promoter associated with variations in curli expression in certain strains of Escherichia coli O157 : H7. Appl Environ Microbiol 67:2367–2370
    [Google Scholar]
  40. Uhlich G. A., Cooke P. H., Solomon E. B. 2006; Analyses of the red-dry-rough phenotype of an Escherichia coli O157 : H7 strain and its role in biofilm formation and resistance to antibacterial agents. Appl Environ Microbiol 72:2564–2572
    [Google Scholar]
  41. 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 Bacteriol 180:2442–2449
    [Google Scholar]
  42. Wang X., Rochon M., Lamprokostopoulou A., Lunsdorf H., Nimitz M., Romling U. 2006; Impact of biofilm matrix components on interaction of commensal Escherichia coli with the gastrointestinal cell line HT-29. Cell Mol Life Sci 63:2352–2363
    [Google Scholar]
  43. White A. P., Gibson D. L., Kim W., Kay W. W., Surette M. G. 2006; Thin aggregative fimbriae and cellulose enhance long-term survival and persistence of Salmonella. J Bacteriol 188:3219–3227
    [Google Scholar]
  44. Zogaj X., Nimtz M., Rohde M., Bokranz W., Romling U. 2001; The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 39:1452–1463
    [Google Scholar]
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