1887

Abstract

The Rcs phosphorelay is composed of RcsC, RcsD and the response regulator RcsB, and this signalling pathway has been implicated in virulence and biofilm formation in many enteric bacteria. It was previously shown that a mutation in resulted in defective biofilm formation in [ Ferrières, L. & Clarke, D. J. (2003) , 1665–1682 ]. To identify the molecular mechanisms underlying the observed biofilm defect we carried out a screen looking for suppressor mutants that restored biofilm formation in the mutant background. One of the mutants was identified to be in , a gene encoding a small RNA molecule that is involved in the post-transcriptional control of the alternative sigma factor, . The expression of is regulated by the Rcs phosphorelay, and there are elevated levels present in the mutant due to the overexpression of in this background. Using different approaches, we have established that the increase in levels is responsible for the biofilm defect. Therefore, the Rcs phosphorelay is involved in maintaining appropriate levels of during biofilm formation in .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.032722-0
2009-11-01
2020-08-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/11/3544.html?itemId=/content/journal/micro/10.1099/mic.0.032722-0&mimeType=html&fmt=ahah

References

  1. Adams J. L., McLean R. J.. 1999; Impact of rpoS deletion on Escherichia coli biofilms. Appl Environ Microbiol65:4285–4287
    [Google Scholar]
  2. Beloin C., Valle J., Latour-Lambert P., Faure P., Kzreminski M., Balestrino 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 Microbiol51:659–674
    [Google Scholar]
  3. Bohannon D. E., Connell N., Keener J., Tormo A., Espinosa-Urgel M., Zambrano M. M., Kolter R.. 1991; Stationary-phase-inducible “gearbox” promoters: differential effects of katF mutations and role of sigma 70. J Bacteriol173:4482–4492
    [Google Scholar]
  4. Bougdour A., Wickner S., Gottesman S.. 2006; Modulating RssB activity: IraP, a novel regulator of σ S stability in Escherichia coli. Genes Dev20:884–897
    [Google Scholar]
  5. Bougdour A., Cunning C., Baptiste P. J., Elliott T., Gottesman S.. 2008; Multiple pathways for regulation of σ S (RpoS) stability in Escherichia coli via the action of multiple anti-adaptors. Mol Microbiol68:298–313
    [Google Scholar]
  6. Bremer E., Silhavy T. J., Weinstock G. M.. 1985; Transposable lambda placMu bacteriophages for creating lacZ operon fusions and kanamycin resistance insertions in Escherichia coli. J Bacteriol162:1092–1099
    [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. 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
    [Google Scholar]
  9. Clarke D. J., Joyce S. A., Toutain C. M., Jacq A., Holland I. B.. 2002; Genetic analysis of the RcsC sensor kinase from Escherichia coli K-12. J Bacteriol184:1204–1208
    [Google Scholar]
  10. Collet A., Cosette P., Beloin C., Ghigo J. M., Rihouey C., Lerouge P., Junter G. A., Jouenne T.. 2008; Impact of rpoS deletion on the proteome of Escherichia coli grown planktonically and as biofilm. J Proteome Res7:4659–4669
    [Google Scholar]
  11. Corona-Izquierdo F. P., Membrillo-Hernandez J.. 2002; A mutation in rpoS enhances biofilm formation in Escherichia coli during exponential phase of growth. FEMS Microbiol Lett211:105–110
    [Google Scholar]
  12. Danese P. N., Pratt L. A., Dove S. L., Kolter R.. 2000a; The outer membrane protein, antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms. Mol Microbiol37:424–432
    [Google Scholar]
  13. Danese P. N., Pratt L. A., Kolter R.. 2000b; Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J Bacteriol182:3593–3596
    [Google Scholar]
  14. Datsenko K. A., Wanner B. L.. 2000; One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A97:6640–6645
    [Google Scholar]
  15. Domka J., Lee J., Bansal T., Wood T. K.. 2007; Temporal gene-expression in Escherichia coli K-12 biofilms. Environ Microbiol9:332–346
    [Google Scholar]
  16. Ferenci T.. 2005; Maintaining a healthy SPANC balance through regulatory and mutational adaptation. Mol Microbiol57:1–8
    [Google Scholar]
  17. Ferrières 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
    [Google Scholar]
  18. 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]
  19. Gottesman S., Trisler P., Torres-Cabassa A.. 1985; Regulation of capsular polysaccharide synthesis in Escherichia coli K-12: characterization of three regulatory genes. J Bacteriol162:1111–1119
    [Google Scholar]
  20. 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
    [Google Scholar]
  21. Hanna A., Berg M., Stout V., Razatos A.. 2003; Role of capsular colanic acid in adhesion of uropathogenic Escherichia coli. Appl Environ Microbiol69:4474–4481
    [Google Scholar]
  22. Hengge R.. 2008; The two-component network and the general stress sigma factor RpoS ( σ S) in Escherichia coli. Adv Exp Med Biol631:40–53
    [Google Scholar]
  23. Huang Y. H., Ferrières L., Clarke D. J.. 2006; The role of the Rcs phosphorelay in Enterobacteriaceae. Res Microbiol157:206–212
    [Google Scholar]
  24. Ito A., May T., Taniuchi A., Kawata K., Okabe S.. 2009; Localized expression profiles of rpoS in Escherichia coli biofilms. Biotechnol Bioeng103:975–983
    [Google Scholar]
  25. Magazin M., Howe M., Allet B.. 1977; Partial correlation of the genetic and physical maps of bacteriophage Mu. Virology77:677–688
    [Google Scholar]
  26. Majdalani N., Gottesman S.. 2005; The Rcs phosphorelay: a complex signal transduction system. Annu Rev Microbiol59:379–405
    [Google Scholar]
  27. Majdalani N., Chen S., Murrow J., St John K., Gottesman S.. 2001; Regulation of RpoS by a novel small RNA: the characterization of RprA. Mol Microbiol39:1382–1394
    [Google Scholar]
  28. 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
    [Google Scholar]
  29. Majdalani N., Heck M., Stout V., Gottesman S.. 2005; Role of RcsF in signaling to the Rcs phosphorelay pathway in Escherichia coli. J Bacteriol187:6770–6778
    [Google Scholar]
  30. Meberg B. M., Sailer F. C., Nelson D. E., Young K. D.. 2001; Reconstruction of Escherichia coli mrcA (PBP 1a) mutants lacking multiple combinations of penicillin binding proteins. J Bacteriol183:6148–6149
    [Google Scholar]
  31. Muffler A., Fischer D., Altuvia S., Storz G., Hengge-Aronis R.. 1996; The response regulator RssB controls stability of the sigma(S) subunit of RNA polymerase in Escherichia coli. EMBO J15:1333–1339
    [Google Scholar]
  32. Mukhopadhyay S., Audia J. P., Roy R. N., Schellhorn H. E.. 2000; Transcriptional induction of the conserved alternative sigma factor RpoS in Escherichia coli is dependent on BarA, a probable two-component regulator. Mol Microbiol37:371–381
    [Google Scholar]
  33. Nystrom T.. 2004; Growth versus maintenance: a trade-off dictated by RNA polymerase availability and sigma factor competition?. Mol Microbiol54:855–862
    [Google Scholar]
  34. O'Toole G. A., Kolter R.. 1998; Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol30:295–304
    [Google Scholar]
  35. O'Toole G., Kaplan H. B., Kolter R.. 2000; Biofilm formation as microbial development. Annu Rev Microbiol54:49–79
    [Google Scholar]
  36. Patten C. L., Kirchhof M. G., Schertzberg M. R., Morton R. A., Schellhorn H. E.. 2004; Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol Genet Genomics272:580–591
    [Google Scholar]
  37. Pratt L. A., Kolter R.. 1998; Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol30:285–293
    [Google Scholar]
  38. Pratt L. A., Silhavy T. J.. 1996; The response regulator SprE controls the stability of RpoS. Proc Natl Acad Sci U S A93:2488–2492
    [Google Scholar]
  39. 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
    [Google Scholar]
  40. Sahu S. N., Acharya S., Tuminaro H., Patel I., Dudley K., LeClerc J. E., Cebula T. A., Mukhopadhyay S.. 2003; The bacterial adaptive response gene, barA, encodes a novel conserved histidine kinase regulatory switch for adaptation and modulation of metabolism in Escherichia coli. Mol Cell Biochem253:167–177
    [Google Scholar]
  41. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  42. Sauer K., Camper A. K., Ehrlich G. D., Costerton J. W., Davies D. G.. 2002; Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol184:1140–1154
    [Google Scholar]
  43. Stoodley P., Sauer K., Davies D. G., Costerton J. W.. 2002; Biofilms as complex differentiated communities. Annu Rev Microbiol56:187–209
    [Google Scholar]
  44. 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]
  45. Takeda S., Fujisawa Y., Matsubara M., Aiba H., Mizuno T.. 2001; A novel feature of the multistep phosphorelay in Escherichia coli: a revised model of the RcsC→YojN→RcsB signalling pathway implicated in capsular synthesis and swarming behaviour. Mol Microbiol40:440–450
    [Google Scholar]
  46. Tierrez A., Garcia-del Portillo F.. 2004; The Salmonella membrane protein IgaA modulates the activity of the RcsC-YojN-RcsB and PhoP-PhoQ regulons. J Bacteriol186:7481–7489
    [Google Scholar]
  47. 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. Microbiology151:2487–2497
    [Google Scholar]
  48. Weber H., Polen T., Heuveling J., Wendisch V. F., Hengge R.. 2005; Genome-wide analyses of the general stress response network in Escherichia coli: σ S-dependent genes, promoters, and sigma factor selectivity. J Bacteriol187:1591–1603
    [Google Scholar]
  49. White-Ziegler C. A., Um S., Pérez N. M., Berns A. L., Malhowski A. J., Young S.. 2008; Low temperature (23 °C) increases expression of biofilm-, cold-shock- and RpoS-dependent genes in Escherichia coli K-12. Microbiology154:148–166
    [Google Scholar]
  50. Wood T. K., Gonzalez Barrios A. F., Herzberg M., Lee J.. 2006; Motility influences biofilm architecture in Escherichia coli. Appl Microbiol Biotechnol72:361–367
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.032722-0
Loading
/content/journal/micro/10.1099/mic.0.032722-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error