1887

Abstract

IgaA is a membrane protein that attenuates the response of the RcsCDB signalling system to envelope stress. This protein is essential unless the RcsCDB system is inactivated, suggesting that IgaA may constantly adjust the magnitude of the response. Such a functional link is also supported by the concurrence of the and loci in genomes of enteric bacteria and the selection of spontaneous mutations in the RcsCDB system following IgaA deprivation. However, the exact nature of the spontaneous mutations rendering IgaA dispensable remains undefined. In this work, we examined how the transduction of an null allele affects the status of the RcsCDB system. Loss of RcsCDB response was registered in ∼90 % of the IgaA-defective clones, which failed to produce the capsule material positively regulated by this system. About half of these non-mucoid clones suppressed the loss of IgaA with large deletions encompassing variable regions of the locus. Unexpectedly, mucoid transductants were also reproducibly obtained and indicated the capacity of to retain a functional RcsCDB system in the absence of IgaA. Decreased levels of either RcsC or RcsD were shown in ‘mucoid’ clones lacking IgaA and displaying low responsiveness to stimuli. Taken together, these data demonstrate that the stability and responsiveness of the RcsCDB system relies on its attenuator IgaA. The type of suppressions found also support a model with IgaA controlling the level of signal flowing through RcsC and RcsD.

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2008-05-01
2020-08-14
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References

  1. Arricau N., Hermant D., Waxin H., Ecobichon C., Duffey P. S., Popoff M. Y.. 1998; The RcsB-RcsC regulatory system of Salmonella typhi differentially modulates the expression of invasion proteins, flagellin and Vi antigen in response to osmolarity. Mol Microbiol29:835–850
    [Google Scholar]
  2. Batchelor E., Goulian M.. 2003; Robustness and the cycle of phosphorylation and dephosphorylation in a two-component regulatory system. Proc Natl Acad Sci U S A100:691–696
    [Google Scholar]
  3. Beier D., Gross R.. 2006; Regulation of bacterial virulence by two-component systems. Curr Opin Microbiol9:143–152
    [Google Scholar]
  4. Bzymek M., Lovett S. T.. 2001; Evidence for two mechanisms of palindrome-stimulated deletion in Escherichia coli : single-strand annealing and replication slipped mispairing. Genetics158:527–540
    [Google Scholar]
  5. Calva E., Oropeza R.. 2006; Two-component signal transduction systems, environmental signals, and virulence. Microb Ecol51:166–176
    [Google Scholar]
  6. Cano D. A., Martinez-Moya M., Pucciarelli M. G., Groisman E. A., Casadesus J., Garcia-Del Portillo F.. 2001; Salmonella enterica serovar Typhimurium response involved in attenuation of pathogen intracellular proliferation. Infect Immun69:6463–6474
    [Google Scholar]
  7. Cano D. A., Dominguez-Bernal G., Tierrez A., Garcia-Del Portillo F., Casadesus J.. 2002; Regulation of capsule synthesis and cell motility in Salmonella enterica by the essential gene igaA . Genetics162:1513–1523
    [Google Scholar]
  8. 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
    [Google Scholar]
  9. Castanie-Cornet M. P., Cam K., Jacq A.. 2006; RcsF is an outer membrane lipoprotein involved in the RcsCDB phosphorelay signaling pathway in Escherichia coli . J Bacteriol188:4264–4270
    [Google Scholar]
  10. Chan R. K., Botstein D., Watanabe T., Ogata Y.. 1972; Specialized transduction of tetracycline resistance by phage P22 in Salmonella typhimurium . II. Properties of a high-frequency-transducing lysate. Virology50:883–898
    [Google Scholar]
  11. 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]
  12. 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
    [Google Scholar]
  13. Collins J., Volckaert G., Nevers P.. 1982; Precise and nearly-precise excision of the symmetrical inverted repeats of Tn5; common features of recA -independent deletion events in Escherichia coli . Gene19:139–146
    [Google Scholar]
  14. Conter A., Sturny R., Gutierrez C., Cam K.. 2002; The RcsCB His-Asp phosphorelay system is essential to overcome chlorpromazine-induced stress in Escherichia coli . J Bacteriol184:2850–2853
    [Google Scholar]
  15. Costa C. S., Pettinari M. J., Mendez B. S., Anton D. N.. 2003; Null mutations in the essential gene yrfF ( mucM ) are not lethal in rcsB , yojN or rcsC strains of Salmonella enterica serovar Typhimurium. FEMS Microbiol Lett222:25–32
    [Google Scholar]
  16. DiGiuseppe P. A., Silhavy T. J.. 2003; Signal detection and target gene induction by the CpxRA two-component system. J Bacteriol185:2432–2440
    [Google Scholar]
  17. Dominguez-Bernal G., Pucciarelli M. G., Ramos-Morales F., Garcia-Quintanilla M., Cano D. A., Casadesus J., Garcia-del Portillo F.. 2004; Repression of the RcsC-YojN-RcsB phosphorelay by the IgaA protein is a requisite for Salmonella virulence. Mol Microbiol53:1437–1449
    [Google Scholar]
  18. Ebel W., Vaughn G. J., Peters H. K. III, 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]
  19. 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
    [Google Scholar]
  20. Erickson K. D., Detweiler C. S.. 2006; The Rcs phosphorelay system is specific to enteric pathogens/commensals and activates ydeI , a gene important for persistent Salmonella infection of mice. Mol Microbiol62:883–894
    [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
    [Google Scholar]
  22. Francez-Charlot A., Castanie-Cornet M. P., Gutierrez C., Cam K.. 2005; Osmotic regulation of the Escherichia coli bdm (biofilm-dependent modulation) gene by the RcsCDB His-Asp phosphorelay. J Bacteriol187:3873–3877
    [Google Scholar]
  23. Garcia-Calderon C. B., Garcia-Quintanilla M., Casadesus J., Ramos-Morales F.. 2005; Virulence attenuation in Salmonella enterica rcsC mutants with constitutive activation of the Rcs system. Microbiology151:579–588
    [Google Scholar]
  24. Hoiseth S. K., Stocker B. A.. 1981; Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature291:238–239
    [Google Scholar]
  25. Huang Y. H., Ferrieres L., Clarke D. J.. 2006; The role of the Rcs phosphorelay in Enterobacteriaceae. Res Microbiol157:206–212
    [Google Scholar]
  26. Ize B., Porcelli I., Lucchini S., Hinton J. C., Berks B. C., Palmer T.. 2004; Novel phenotypes of Escherichia coli tat mutants revealed by global gene expression and phenotypic analysis. J Biol Chem279:47543–47554
    [Google Scholar]
  27. Kaldalu N., Mei R., Lewis K.. 2004; Killing by ampicillin and ofloxacin induces overlapping changes in Escherichia coli transcription profile. Antimicrob Agents Chemother48:890–896
    [Google Scholar]
  28. Kanie S., Horibata K., Kawano M., Isogawa A., Sakai A., Matsuo N., Nakanishi M., Hasegawa K., Yoshiyama K., Maki H.. 2007; Roles of RecA protein in spontaneous mutagenesis in Escherichia col i. Genes Genet Syst82:99–108
    [Google Scholar]
  29. Kelley W. L., Georgopoulos C.. 1997; Positive control of the two-component RcsC/B signal transduction network by DjlA: a member of the DnaJ family of molecular chaperones in Escherichia coli . Mol Microbiol25:913–931
    [Google Scholar]
  30. Majdalani N., Gottesman S.. 2005; The Rcs phosphorelay: a complex signal transduction system. Annu Rev Microbiol59:379–405
    [Google Scholar]
  31. Majdalani N., Gottesman S.. 2007; Genetic dissection of signaling through the Rcs phosphorelay. Methods Enzymol423:349–362
    [Google Scholar]
  32. 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]
  33. Maloy S. R.. 1990; Experimental Techniques in Bacterial Genetics Boston, MA: Jones & Barlett;
    [Google Scholar]
  34. Mascher T., Helmann J. D., Unden G.. 2006; Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev70:910–938
    [Google Scholar]
  35. Miller J. H.. 1972; Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  36. Mouslim C., Delgado M., Groisman E. A.. 2004; Activation of the RcsC/YojN/RcsB phosphorelay system attenuates Salmonella virulence. Mol Microbiol54:386–395
    [Google Scholar]
  37. Page F., Altabe S., Hugouvieux-Cotte-Pattat N., Lacroix J. M., Robert-Baudouy J., Bohin J. P.. 2001; Osmoregulated periplasmic glucan synthesis is required for Erwinia chrysanthemi pathogenicity. J Bacteriol183:3134–3141
    [Google Scholar]
  38. 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]
  39. Pucciarelli M. G., Prieto A. I., Casadesus J., Garcia-del Portillo F.. 2002; Envelope instability in DNA adenine methylase mutants of Salmonella enterica . Microbiology148:1171–1182
    [Google Scholar]
  40. Sailer F. C., Meberg B. M., Young K. D.. 2003; β -Lactam induction of colanic acid gene expression in Escherichia coli . FEMS Microbiol Lett226:245–249
    [Google Scholar]
  41. Schagger H., von Jagow G.. 1987; Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem166:368–379
    [Google Scholar]
  42. Schmieger H.. 1972; Phage P22-mutants with increased or decreased transduction abilities. Mol Gen Genet119:75–88
    [Google Scholar]
  43. Shiba Y., Yokoyama Y., Aono Y., Kiuchi T., Kusaka J., Matsumoto K., Hara H.. 2004; Activation of the Rcs signal transduction system is responsible for the thermosensitive growth defect of an Escherichia coli mutant lacking phosphatidylglycerol and cardiolipin. J Bacteriol186:6526–6535
    [Google Scholar]
  44. Stock A. M., Robinson V. L., Goudreau P. N.. 2000; Two-component signal transduction. Annu Rev Biochem69:183–215
    [Google Scholar]
  45. Stout V., Gottesman S.. 1990; RcsB and RcsC: a two-component regulator of capsule synthesis in Escherichia coli . J Bacteriol172:659–669
    [Google Scholar]
  46. 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]
  47. West A. H., Stock A. M.. 2001; Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci26:369–376
    [Google Scholar]
  48. Wilson J. A., Doyle T. J., Gulig P. A.. 1997; Exponential-phase expression of spvA of the Salmonella typhimurium virulence plasmid: induction in intracellular salts medium and intracellularly in mice and cultured mammalian cells. Microbiology143:3827–3839
    [Google Scholar]
  49. Zhou L., Lei X. H., Bochner B. R., Wanner B. L.. 2003; Phenotype microarray analysis of Escherichia coli K-12 mutants with deletions of all two-component systems. J Bacteriol185:4956–4972
    [Google Scholar]
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