1887

Abstract

The RcsCDB signal transduction system is an atypical His–Asp phosphorelay. Notably, the response regulator RcsB can be activated either by phosphorylation through the RcsCD pathway or by an accessory cofactor RcsA. Although conserved in , the role of this system in adaptation to environmental stress conditions is largely unknown. This study reveals that the response regulator RcsB is essential to glutamate-dependent acid resistance, a condition pertinent to the lifestyle of . The requirement for RcsB is independent of its activation by either the RcsCD or the RcsA pathway. The basal activity of RcsB appears to be necessary and sufficient for acid resistance. The sensitivity of the strain to low pH is correlated to a strong reduction of the expression of the glutamate decarboxylase genes, and , during the stationary phase of growth. This effect on expression is not mediated by the general stress sigma factor RpoS, but does require a functional allele and the previously identified GadE box. Therefore activation of expression and acid resistance absolutely requires both GadE and RcsB. In contrast, an increase in RcsB activity through the activation of the RcsCD phosphorelay or the RcsA pathway or through overproduction of the protein leads to general repression of the expression of the genes and a corresponding reduction in acid resistance.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.29278-0
2007-01-01
2019-11-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/1/238.html?itemId=/content/journal/micro/10.1099/mic.0.29278-0&mimeType=html&fmt=ahah

References

  1. Bachmann, B. J. ( 1996; ). Derivations and genotypes of some mutant derivatives of Escherichia coli K-12. In Escherichia coli and Salmonella: Cellular and Molecular Biology, pp. 2460–2488. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
  2. Bang, I. S., Kim, B. H., Foster, J. W. & Park, Y. K. ( 2000; ). OmpR regulates the stationary-phase acid resistance response of Salmonella enterica serovar Typhimurium. J Bacteriol 182, 2245–2252.[CrossRef]
    [Google Scholar]
  3. Bereswill, S. & Geider, K. ( 1997; ). Characterization of the rcsB gene from Erwinia amylovora and its influence on exopolysaccharide synthesis and virulence of the fire blight pathogen. J Bacteriol 179, 1354–1361.
    [Google Scholar]
  4. Bordi, C., Theraulaz, L., Mejean, V. & Jourlin-Castelli, C. ( 2003; ). Anticipating an alkaline stress through the Tor phosphorelay system in Escherichia coli. Mol Microbiol 48, 211–223.[CrossRef]
    [Google Scholar]
  5. Carballes, F., Bertrand, C., Bouché, J. P. & Cam, K. ( 1999; ). Regulation of E. coli cell division genes ftsA and ftsZ by the two-component system rcsC-rcsB. Mol Microbiol 34, 442–450.[CrossRef]
    [Google Scholar]
  6. Castanié-Cornet, M. P. & Foster, J. W. ( 2001; ). Escherichia coli acid resistance: cAMP receptor protein and a 20 bp cis-acting sequence control pH and stationary phase expression of the gadA and gadBC glutamate decarboxylase genes. Microbiology 147, 709–715.
    [Google Scholar]
  7. Castanié-Cornet, M. P., Penfound, T. A., Smith, D., Elliott, J. F. & Foster, J. W. ( 1999; ). Control of acid resistance in Escherichia coli. J Bacteriol 181, 3525–3535.
    [Google Scholar]
  8. Castanié-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 Bacteriol 188, 4264–4270.[CrossRef]
    [Google Scholar]
  9. Clarke, D. J., Holland, I. B. & Jacq, A. ( 1997; ). Point mutations in the transmembrane domain of DjlA, a membrane-linked DnaJ-like protein, abolish its function in promoting colanic acid production via the Rcs signal transduction pathway. Mol Microbiol 25, 933–944.[CrossRef]
    [Google Scholar]
  10. 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 Bacteriol 184, 2850–2853.[CrossRef]
    [Google Scholar]
  11. 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 A 97, 6640–6645.[CrossRef]
    [Google Scholar]
  12. 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 Bacteriol 183, 5870–5876.[CrossRef]
    [Google Scholar]
  13. De Biase, D., Tramonti, A., Bossa, F. & Visca, P. ( 1999; ). The response to stationary-phase stress conditions in Escherichia coli: role and regulation of the glutamic acid decarboxylase system. Mol Microbiol 32, 1198–1211.[CrossRef]
    [Google Scholar]
  14. Detweiler, C. S., Monack, D. M., Brodsky, I. E., Mathew, H. & Falkow, S. ( 2003; ). virK, somA and rcsC are important for systemic Salmonella enterica Serovar Typhimurium infection and cationic peptide resistance. Mol Microbiol 48, 385–400.[CrossRef]
    [Google Scholar]
  15. 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 Microbiol 53, 1437–1449.[CrossRef]
    [Google Scholar]
  16. 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 Microbiol 50, 1665–1682.[CrossRef]
    [Google Scholar]
  17. Foster, J. W. ( 2004; ). Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol 2, 898–907.[CrossRef]
    [Google Scholar]
  18. Francez-Charlot, A., Filée, J., Castanié-Cornet, M. P. & Cam, K. ( 2005a; ). Regulation of flhDC by the His-Asp phosphorelay RcsCDB. In Global Regulatory Networks in Enteric Bacteria, pp. 93–106. Edited by Birgit M. Prüß. Trivandrum: Research Signpost.
  19. Francez-Charlot, A., Castanié-Cornet, M. P., Gutierrez, C. & Cam, K. ( 2005b; ). Osmotic regulation of the Escherichia coli bdm (biofilm dependent modulation) gene by the RcsCDB His-Asp phosphorelay. J Bacteriol 187, 3873–3877.[CrossRef]
    [Google Scholar]
  20. Fredericks, C. E., Shibata, S., Aizawa, S., Reimann, S. A. & Wolfe, A. J. ( 2006; ). Acetyl phosphate-sensitive regulation of flagellar biogenesis and capsular biosynthesis depends on the Rcs phosphorelay. Mol Microbiol 61, 734–747.[CrossRef]
    [Google Scholar]
  21. 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. Microbiology 151, 579–588.[CrossRef]
    [Google Scholar]
  22. Gong, S., Ma, Z. & Foster, J. W. ( 2004; ). The Era-like GTPase TrmE conditionally activates gadE and glutamate-dependent acid resistance in Escherichia coli. Mol Microbiol 54, 948–961.[CrossRef]
    [Google Scholar]
  23. 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.[CrossRef]
    [Google Scholar]
  24. Hommais, F., Krin, E., Laurent-Winter, C., Soutourina, O., Malpertuy, A., Le Caer, J. P., Danchin, A. & Bertin, P. ( 2001; ). Large-scale monitoring of pleiotropic regulation of gene expression by the prokaryotic nucleoid-associated protein, H-NS. Mol Microbiol 40, 20–36.[CrossRef]
    [Google Scholar]
  25. Hommais, F., Krin, E., Coppee, J. Y., Lacroix, C., Yeramian, E., Danchin, A. & Bertin, P. ( 2004; ). GadE (YhiE): a novel activator involved in the response to acid environment in Escherichia coli. Microbiology 150, 61–72.[CrossRef]
    [Google Scholar]
  26. Huang, Y.-H., Ferrières, L. & Clarke, D. J. ( 2006; ). The role of the Rcs phosphorelay in Enterobacteriaceae. Res Microbiol 157, 206–212.[CrossRef]
    [Google Scholar]
  27. Lange, R. & Hengge-Aronis, R. ( 1991; ). Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol 5, 49–59.[CrossRef]
    [Google Scholar]
  28. Ma, Z., Richard, H., Tucker, D. L., Conway, T. & Foster, J. W. ( 2002; ). Collaborative regulation of Escherichia coli glutamate-dependent acid resistance by two AraC-like regulators, GadX and GadW (YhiW). J Bacteriol 184, 7001–7012.[CrossRef]
    [Google Scholar]
  29. Ma, Z., Gong, S., Richard, H., Tucker, D. L., Conway, T. & Foster, J. W. ( 2003; ). GadE (YhiE) activates glutamate decarboxylase-dependent acid resistance in Escherichia coli K-12. Mol Microbiol 49, 1309–1320.[CrossRef]
    [Google Scholar]
  30. Ma, Z., Masuda, N. & Foster, J. W. ( 2004; ). Characterization of EvgAS-YdeO-GadE branched regulatory circuit governing glutamate-dependent acid resistance in Escherichia coli. J Bacteriol 186, 7378–7389.[CrossRef]
    [Google Scholar]
  31. Majdalani, N. & Gottesman, S. ( 2005; ). The Rcs phosphorelay: a complex signal transduction system. Annu Rev Microbiol 59, 379–405.[CrossRef]
    [Google Scholar]
  32. Majdalani, N., Hernandez, D. & Gottesman, S. ( 2002; ). Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 46, 813–826.[CrossRef]
    [Google Scholar]
  33. Masuda, N. & Church, G. M. ( 2002; ). Escherichia coli gene expression responsive to levels of the response regulator EvgA. J Bacteriol 184, 6225–6234.[CrossRef]
    [Google Scholar]
  34. Masuda, N. & Church, G. M. ( 2003; ). Regulatory network of acid resistance genes in Escherichia coli. Mol Microbiol 48, 699–712.[CrossRef]
    [Google Scholar]
  35. Miller, J. H. ( 1992; ). A Short Course In Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  36. Mouslim, C., Delgado, M. & Groisman, E. A. ( 2004; ). Activation of the RcsC/YojN/RcsB phosphorelay system attenuates Salmonella virulence. Mol Microbiol 54, 386–395.[CrossRef]
    [Google Scholar]
  37. Shin, S., Castanié-Cornet, M. P., Foster, J. W., Crawford, J. A., Brinkley, C. & Kaper, J. B. ( 2001; ). An activator of glutamate decarboxylase genes regulates the expression of enteropathogenic Escherichia coli virulence genes through control of the plasmid-encoded regulator, Per. Mol Microbiol 41, 1133–1150.
    [Google Scholar]
  38. Simons, R. W., Houman, F. & Kleckner, N. ( 1987; ). Improved single and multicopy lac-based cloning vectors for protein and gene fusions. Gene 53, 85–96.[CrossRef]
    [Google Scholar]
  39. Stout, V., Torres-Cabassa, A., Maurizi, M. R., Gutnick, D. & Gottesman, S. ( 1991; ). RcsA, an unstable positive regulator of capsular polysaccharide synthesis. J Bacteriol 173, 1738–1747.
    [Google Scholar]
  40. Takeda, S. I., 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 Microbiol 40, 440–450.[CrossRef]
    [Google Scholar]
  41. Tobe, T., Ando, H., Ishikawa, H., Abe, H., Tashiro, K., Hayashi, T., Kuhara, S. & Sugimoto, N. ( 2005; ). Dual regulatory pathways integrating the RcsC-RcsD-RcsB signalling system control enterohaemorrhagic Escherichia coli pathogenicity. Mol Microbiol 58, 320–333.[CrossRef]
    [Google Scholar]
  42. Tucker, D. L., Tucker, N., Ma, Z., Foster, J. W., Miranda, R. L., Cohen, P. S. & Conway, T. ( 2003; ). Genes of the GadX-GadW regulon in Escherichia coli. J Bacteriol 185, 3190–3201.[CrossRef]
    [Google Scholar]
  43. Weber, H., Polen, T., Heuveling, J., Wendisch, V. F. & Hengge, R. ( 2005; ). Genome-wide analysis of the general stress response network in Escherichia coli: σ S-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187, 1591–1603.[CrossRef]
    [Google Scholar]
  44. 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 Chem 275, 7013–7020.[CrossRef]
    [Google Scholar]
  45. Zhang, W. & Shi, L. ( 2005; ). Distribution and evolution of multiple-step phosphorelay in prokaryotes: lateral domain recruitment involved in the formation of hybrid-type histidine kinases. Microbiology 151, 2159–2173.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.29278-0
Loading
/content/journal/micro/10.1099/mic.0.29278-0
Loading

Data & Media loading...

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