1887

Abstract

The human-pathogenic yersiniae represent an ideal species group to study the evolution of highly virulent bacteria, with having emerged from the enteropathogen an estimated 20 000 years ago. Sequence data reveal that the genome is in the early stages of decay and contains hundreds of non-functioning pseudogenes, some of which may be important in the enteric lifestyle of . Bioinformatic analysis of pseudogenes from seven genome sequences identified as a gene disrupted early in the evolution of this organism. This phosphotransfer protein is part the of the Rcs phosphorelay, a two-component system present in the which has been shown to regulate the expression of capsular polysaccharide and other virulence determinants in several species including and . Using microarray analysis, we determined that the Rcs phosphorelay regulates the expression of 136 coding sequences, of which 60 % are predicted to affect the cell envelope. Several putative virulence determinants were identified as being regulated by this phosphorelay, along with proteins involved in biofilm formation, motility, mammalian cell adhesion and stress survival. Phenotypic assays on defined mutants confirmed a role for the phosphorelay in these processes in both and .

Keyword(s): CDS, coding sequence
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2008-04-01
2020-04-08
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References

  1. Achtman M., Zurth K., Morelli G., Torrea G., Guiyoule A., Carniel E.. 1999; Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A96:14043–14048
    [Google Scholar]
  2. Amann E., Ochs B., Abel K. J.. 1988; Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene69:301–315
    [Google Scholar]
  3. 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]
  4. Belas R., Schneider R., Melch M.. 1998; Characterization of Proteus mirabilis precocious swarming mutants: identification of rsbA, encoding a regulator of swarming behavior. J Bacteriol180:6126–6139
    [Google Scholar]
  5. Bernstein C., Bernstein H., Payne C. M., Beard S. E., Schneider J.. 1999; Bile salt activation of stress response promoters in Escherichia coli. Curr Microbiol39:68–72
    [Google Scholar]
  6. Bowen D. J., Rocheleau T. A., Grutzmacher C. K., Meslet L., Valens M., Marble D., Dowling A., Ffrench-Constant R., Blight M. A.. 2003; Genetic and biochemical characterization of PrtA, an RTX-like metalloprotease from Photorhabdus. Microbiology149:1581–1591
    [Google Scholar]
  7. 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]
  8. Chain P. S., Carniel E., Larimer F. W., Lamerdin J., Stoutland P. O., Regala W. M., Georgescu A. M., Vergez L. M., Land M. L.. other authors 2004; Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A101:13826–13831
    [Google Scholar]
  9. Clarke D. J., Jacq A., Holland I. B.. 1996; A novel DnaJ-like protein in Escherichia coli inserts into the cytoplasmic membrane with a type III topology. Mol Microbiol20:1273–1286
    [Google Scholar]
  10. 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 Microbiol25:933–944
    [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 A97:6640–6645
    [Google Scholar]
  12. Dufour A., Furness R. B., Hughes C.. 1998; Novel genes that upregulate the Proteus mirabilis flhDC master operon controlling flagellar biogenesis and swarming. Mol Microbiol29:741–751
    [Google Scholar]
  13. 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]
  14. 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]
  15. Flamez C., Ricard I., Arafah S., Simonet M., Marceau M.. 2007; Two-component system regulon plasticity in bacteria: a concept emerging from phenotypic analysis of Yersinia pseudotuberculosis response regulator mutants. Adv Exp Med Biol603:145–155
    [Google Scholar]
  16. 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]
  17. Guzman L.-M., Belin D., Carson M. J., Beckwith J.. 1995; Tight regulation, modulation and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol177:4121–4130
    [Google Scholar]
  18. 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]
  19. Heeseman J.. 1987; Chromosomal-encoded siderophores are required for mouse virulence of enteropathogenic Yersinia species. FEMS Microbiol Lett48:229–233
    [Google Scholar]
  20. Hinchliffe S. J., Isherwood K. E., Stabler R. A., Prentice M. B., Rakin A., Nichols R. A., Oyston P. C. F., Hinds J., Titball R. W., Wren B. W.. 2003; Application of DNA microarrays to study the evolutionary genomics of Yersinia pestis and Yersinia pseudotuberculosis. Genome Res13:2018–2029
    [Google Scholar]
  21. Huang Y., Ferrières L., Clarke D. J.. 2006; The role of the Rcs phosphorelay in Enterobacteriaceae. Res Microbiol157:206–212
    [Google Scholar]
  22. Joshua G. W., Karlyshev A. V., Smith M. P., Isherwood K. E., Titball R. W., Wren B. W.. 2003; A Caenorhabditis elegans model of Yersinia infection: biofilm formation on a biotic surface. Microbiology149:3221–3229
    [Google Scholar]
  23. 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]
  24. Kim S. Y., Nishioka M., Hayashi S., Honda H., Kobayashi T., Taya M.. 2005; The gene yggE functions in restoring physiological defects of Escherichia coli cultivated under oxidative stress conditions. Appl Environ Microbiol71:2762–2765
    [Google Scholar]
  25. Kim C. M., Park R. Y., Chun H. J., Kim S. Y., Rhee J. H., Shin S. H.. 2007; Vibrio vulnificus metalloprotease VvpE is essentially required for swarming. FEMS Microbiol Lett269:170–179
    [Google Scholar]
  26. Kinder S. A., Badger J. L., Bryant G. O., Pepe J. C., Miller V. L.. 1993; Cloning of the YenI restriction endonuclease and methyltransferase from Yersinia enterocolitica serotype O8 and construction of a transformable RM+ mutant. Gene136:271–275
    [Google Scholar]
  27. Lerat E., Ochman H.. 2005; Recognizing the pseudogenes in bacterial genomes. Nucleic Acids Res33:3125–3132
    [Google Scholar]
  28. Majdalani N., Gottesman S.. 2005; The Rcs phosphorelay: a complex signal transduction system. Annu Rev Microbiol59:379–405
    [Google Scholar]
  29. 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]
  30. Majdalani N., Heck M., Stout V., Gottesman S.. 2005; Role of RcsF in signalling to the Rcs phosphorelay pathway in Escherichia coli. J Bacteriol187:6770–6778
    [Google Scholar]
  31. Maxson M. E., Darwin A. J.. 2004; Identification of inducers of the Yersinia enterocolitica phage shock protein system and comparison to the regulation of the RpoE and Cpx extracytoplasmic stress responses. J Bacteriol186:4199–4208
    [Google Scholar]
  32. Ophir T., Gutnick D. L.. 1994; A role for exopolysaccharides in the protection of microorganisms from desiccation. Appl Environ Microbiol60:740–745
    [Google Scholar]
  33. Parkhill J., Wren B. W., Thomson N. R., Titball R. W., Holden M. T., Prentice M. B., Sebaihia M., James K. D., Churcher C.. other authors 2001; Genome sequence of Yersinia pestis, the causative agent of plague. Nature413:523–527
    [Google Scholar]
  34. Pomposiello P. J., Koutsolioutsou A., Carrasco D., Demple B.. 2003; SoxRS-regulated expression and genetic analysis of the yggX gene of Escherichia coli. J Bacteriol185:6624–6632
    [Google Scholar]
  35. Potrykus J., Wegrzyn G.. 2004; The ypdI gene codes for a putative lipoprotein involved in the synthesis of colanic acid in Escherichia coli. FEMS Microbiol Lett235:265–271
    [Google Scholar]
  36. Ray M. C., Germon P., Vianney A., Portalier R., Lazzaroni J. C.. 2000; Identification by genetic suppression of Escherichia coli TolB residues important for TolB-Pal interaction. J Bacteriol182:821–824
    [Google Scholar]
  37. Riley G., Toma S.. 1989; Detection of pathogenic Yersinia enterocolitica by using Congo red-magnesium oxalate agar medium. J Clin Microbiol27:213–214
    [Google Scholar]
  38. Rogov V. V., Rogova N. Y., Bernhard F., Koglin A., Lohr F., Dotsch V.. 2006; A new structural domain in the Escherichia coli RcsC hybrid sensor kinase connects histidine kinase and phosphoreceiver domains. J Mol Biol364:68–79
    [Google Scholar]
  39. Santos J. M., Lobo M., Matos A. P., De Pedro M. A., Arraiano C. M.. 2002; The gene bolA regulatesdacA (PBP5), dacC (PBP6) and ampC(AmpC), promoting normal morphology in Escherichia coli. Mol Microbiol45:1729–1740
    [Google Scholar]
  40. Skovran E., Lauhon C. T., Downs D. M.. 2004; Lack of YggX results in chronic oxidative stress and uncovers subtle defects in Fe–S cluster metabolism in Salmonella enterica. J Bacteriol186:7626–7634
    [Google Scholar]
  41. Sledjeski D. D., Gottesman S.. 1996; Osmotic shock induction of capsule synthesis in Escherichia coli K-12. J Bacteriol178:1204–1206
    [Google Scholar]
  42. Song Y., Tong Z., Wang J., Wang L., Guo Z., Han Y., Zhang J., Pei D., Zhou D.. other authors 2004; Complete genome sequence of Yersinia pestis strain 91001, an isolate avirulent to humans. DNA Res11:179–197
    [Google Scholar]
  43. Stabler A., Hinds J., Witney A. A., Isherwood K., Oyston P., Titball R., Wren B. W., Hinchliffe S., Prentice M.. other authors 2003; Construction of a Yersinia pestis microarray. Adv Exp Med Biol529:47–51
    [Google Scholar]
  44. Stout V., Gottesman S.. 1990; RcsB and RcsC: a two-component regulator of capsule synthesis in Escherichia coli. J Bacteriol172:659–669
    [Google Scholar]
  45. Strong P. C. R., Hinchliffe S. J., Matthews S., Wren B. W.. 2006; A putative intimin-like adhesin in Y. pseudotuberculosis pathogenesis. Poster at the 9th International Symposium on Yersinia
    [Google Scholar]
  46. Sturny R., Cam K., Gutierrez C., Conter A.. 2003; NhaR and RcsB independently regulate the osmCp1 promoter of Escherichia coli at overlapping regulatory sites. J Bacteriol185:4298–4304
    [Google Scholar]
  47. Suzuki K., Wang X., Weilbacher T., Pernestig A. K., Melefors O., Georgellis D., Babitzke P., Romeo T.. 2002; Regulatory circuitry of the CsrA/CsrB and BarA/UvrY systems of Escherichia coli. J Bacteriol184:5130–5140
    [Google Scholar]
  48. 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]
  49. Taylor L. A., Rose R. E.. 1988; A correction in the nucleotide sequence of the Tn 903 kanamycin resistance determinant in pUC4K. Nucleic Acids Res16:358
    [Google Scholar]
  50. 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 Microbiol58:320–333
    [Google Scholar]
  51. Toguchi A., Siano M., Burkart M., Harshey R. M.. 2000; Genetics of swarming motility in Salmonella enterica serovar Typhimurium: critical role for lipopolysaccharide. J Bacteriol182:6308–6321
    [Google Scholar]
  52. 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]
  53. Vieira H. L., Freire P., Arraiano C. M.. 2004; Effect of Escherichia coli morphogene bolA on biofilms. Appl Environ Microbiol70:5682–5684
    [Google Scholar]
  54. 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
    [Google Scholar]
  55. 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]
  56. Zuber M., Hoover T. A., Court D. L.. 1995; Analysis of a Coxiella burnetti gene product that activates capsule synthesis in Escherichia coli: requirement for the heat shock chaperone DnaK and the two-component regulator RcsC. J Bacteriol177:4238–4244
    [Google Scholar]
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