1887

Abstract

is an enteric bacterium which must overcome the acidic stress in host organs for successful colonization, but how this bacterium survives in acidic conditions remains largely unknown. In the present study, the importance of OmpR in acid survival of YpIII was confirmed by the fact that mutation of (strain Δ) greatly reduced cell survival at pH 4.5 or lower. To characterize the regulatory role of OmpR in this acid survival process, proteomic analysis was carried out to compare YpIII at pH 7.0 and pH 4.5 with Δ at pH 7.0, and urease components were revealed to be the main targets for OmpR regulation. Addition of urea to the culture medium also enhanced acid survival of YpIII but not Δ and urease activity was significantly induced by acid in YpIII but not in Δ. Each of the seven components of the YpIII urease gene cluster was fused to a reporter and their expression was dramatically decreased in a Δ background; this supports the notion that OmpR positively regulates urease expression. Furthermore, gel shift analysis revealed that OmpR binds to the deduced promoter regions of three polycistronic transcriptional units (, and ) in the urease cluster, suggesting that the regulation of OmpR to urease components is direct. Taken together, these data strongly suggest that OmpR activates urease expression to enhance acid survival in .

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2009-08-01
2024-04-16
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References

  1. Akada J. K., Shirai M., Takeuchi H., Tsuda M., Nakazawa T. 2000; Identification of the urease operon in Helicobacter pylori and its control by mRNA decay in response to pH. Mol Microbiol 36:1071–1084
    [Google Scholar]
  2. Allen K. J., Lepp D., McKellar R. C., Griffiths M. W. 2008; Examination of stress and virulence gene expression in Escherichia coli O157 : H7 using targeted microarray analysis. Foodborne Pathog Dis 5:437–447
    [Google Scholar]
  3. Atkinson S., Throup J. P., Stewart G. S., Williams P. 1999; A hierarchical quorum-sensing system in Yersinia pseudotuberculosis is involved in the regulation of motility and clumping. Mol Microbiol 33:1267–1277
    [Google Scholar]
  4. Bandara A. B., Contreras A., Contreras-Rodriguez A., Martins A. M., Dobrean V., Poff-Reichow S., Rajasekaran P., Sriranganathan N., Schurig G. G., Boyle S. M. 2007; Brucella suis urease encoded by ure1 but not ure2 is necessary for intestinal infection of BALB/c mice. BMC Microbiol 7:57
    [Google Scholar]
  5. Bang I. S., Kim B. H., Foster J. W., Park Y. K. 2000; OmpR regulates the stationary-phase acid tolerance response of Salmonella enterica serovar typhimurium. J Bacteriol 182:2245–2252
    [Google Scholar]
  6. Bearson S., Bearson B., Foster J. W. 1997; Acid stress responses in enterobacteria. FEMS Microbiol Lett 147:173–180
    [Google Scholar]
  7. Bearson B. L., Wilson L., Foster J. W. 1998; A low pH-inducible, PhoPQ-dependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress. J Bacteriol 180:2409–2417
    [Google Scholar]
  8. Berk P. A., Jonge R., Zwietering M. H., Abee T., Kieboom J. 2005; Acid resistance variability among isolates of Salmonella enterica serovar Typhimurium DT104. J Appl Microbiol 99:859–866
    [Google Scholar]
  9. Blankenhorn D., Phillips J., Slonczewski J. L. 1999; Acid- and base-induced proteins during aerobic and anaerobic growth of Escherichia coli revealed by two-dimensional gel electrophoresis. J Bacteriol 181:2209–2216
    [Google Scholar]
  10. Boot I. R., Cash P., O'Byrne C. 2002; Sensing and adapting to acid stress. Antonie Van Leeuwenhoek 81:33–42
    [Google Scholar]
  11. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
    [Google Scholar]
  12. Brzostek K., Brzostkowska M., Bukowska I., Karwicka E., Raczkowska A. 2007; OmpR negatively regulates expression of invasin in Yersinia enterocolitica . Microbiology 153:2416–2425
    [Google Scholar]
  13. Castanie-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]
  14. Castillo A., Lucia L. M., Goodson K. J., Savell J. W., Acuff G. R. 1999; Decontamination of beef carcass surface tissue by steam vacuuming alone and combined with hot water and lactic acid sprays. J Food Prot 62:146–151
    [Google Scholar]
  15. Coker C., Bakare O. O., Mobley H. L. 2000; H-NS is a repressor of the Proteus mirabilis urease transcriptional activator gene ureR . J Bacteriol 182:2649–2653
    [Google Scholar]
  16. Dattelbaum J. D., Lockatell C. V., Johnson D. E., Mobley H. L. 2003; UreR, the transcriptional activator of the Proteus mirabilis urease gene cluster, is required for urease activity and virulence in experimental urinary tract infections. Infect Immun 71:1026–1030
    [Google Scholar]
  17. De Koning-Ward T. F., Robins-Browne R. M. 1995; Contribution of urease to acid tolerance in Yersinia enterocolitica . Infect Immun 63:3790–3795
    [Google Scholar]
  18. De Koning-Ward T. F., Ward A. C., Robins-Browne R. M. 1994; Characterisation of the urease-encoding gene complex of Yersinia enterocolitica . Gene 145:25–32
    [Google Scholar]
  19. Delany I., Ieva R., Soragni A., Hilleringmann M., Rappuoli R., Scarlato V. 2005; In vitro analysis of protein-operator interactions of the NikR and Fur metal-responsive regulators of coregulated genes in Helicobacter pylori . J Bacteriol 187:7703–7715
    [Google Scholar]
  20. Flamez C., Ricard I., Arafah S., Simonet M., Marceau M. 2008; Phenotypic analysis of Yersinia pseudotuberculosis 32777 response regulator mutants: new insights into two-component system regulon plasticity in bacteria. Int J Med Microbiol 298:193–207
    [Google Scholar]
  21. Foster J. W. 2004; Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol 2:898–907
    [Google Scholar]
  22. Giannella R. A., Broitman S. A., Zamcheck N. 1972; Gastric acid barrier to ingested microorganisms in man: studies in vivo and in vitro. Gut 13:251–256
    [Google Scholar]
  23. Grabenstein J. P., Marceau M., Pujol C., Simonet M., Bliska J. B. 2004; The response regulator PhoP of Yersinia pseudotuberculosis is important for replication in macrophages and for virulence. Infect Immun 72:4973–4984
    [Google Scholar]
  24. Heuveling J., Possling A., Hengge R. 2008; A role for Lon protease in the control of the acid resistance genes of Escherichia coli . Mol Microbiol 69:534–547
    [Google Scholar]
  25. Huang Y. Y., Deng J. Y., Gu J., Zhang Z. P., Maxwell A., Bi L. J., Chen Y. Y., Zhou Y. F., Yu Z. N., Zhang X. E. 2006; The key DNA-binding residues in the C-terminal domain of Mycobacterium tuberculosis DNA gyrase A subunit (GyrA. Nucleic Acids Res 34:5650–5659
    [Google Scholar]
  26. Karimova G., Pidoux J., Ullmann A., Ladant D. 1998; A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci U S A 95:5752–5756
    [Google Scholar]
  27. Lee I. S., Slonczewski J. L., Foster J. W. 1994; A low-pH-inducible, stationary-phase acid tolerance response in Salmonella typhimurium . J Bacteriol 176:1422–1426
    [Google Scholar]
  28. Lee Y. H., Kim B. H., Kim J. H., Yoon W. S., Bang S. H., Park Y. K. 2007; CadC has a global translational effect during acid adaptation in Salmonella enterica serovar Typhimurium. J Bacteriol 189:2417–2425
    [Google Scholar]
  29. Lennox E. S. 1955; Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1:190–206
    [Google Scholar]
  30. Leyer G. J., Wang L. L., Johnson E. A. 1995; Acid adaptation of Escherichia coli O157 : H7 increases survival in acidic foods. Appl Environ Microbiol 61:3752–3755
    [Google Scholar]
  31. Lin J., Lee I. S., Frey J., Slonczewski J. L., Foster J. W. 1995; Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli . J Bacteriol 177:4097–4104
    [Google Scholar]
  32. Maroncle N., Rich C., Forestier C. 2006; The role of Klebsiella pneumoniae urease in intestinal colonization and resistance to gastrointestinal stress. Res Microbiol 157:184–193
    [Google Scholar]
  33. Marshall B. J., Barrett L. J., Prakash C., McCallum R. W., Guerrant R. L. 1990; Urea protects Helicobacter ( Campylobacter) pylori from the bactericidal effect of acid. Gastroenterology 99:697–702
    [Google Scholar]
  34. Masuda N., Church G. M. 2003; Regulatory network of acid resistance genes in Escherichia coli . Mol Microbiol 48:699–712
    [Google Scholar]
  35. Miller J. H. 1992 A Short Course in Bacterial Genetics: a Laboratory Manual and Handbook for Escherichia coli and Related Bacteria Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
    [Google Scholar]
  36. Mujacic M., Baneyx F. 2007; Chaperone Hsp31 contributes to acid resistance in stationary-phase Escherichia coli . Appl Environ Microbiol 73:1014–1018
    [Google Scholar]
  37. Nagano T., Kiyohara T., Suzuki K., Tsubokura M., Otsuki K. 1997; Identification of pathogenic strains within serogroups of Yersinia pseudotuberculosis and the presence of non-pathogenic strains isolated from animals and the environment. J Vet Med Sci 59:153–158
    [Google Scholar]
  38. O'Toole R., Milton D. L., Wolf-Watz H. 1996; Chemotactic motility is required for invasion of the host by the fish pathogen Vibrio anguillarum . Mol Microbiol 19:625–637
    [Google Scholar]
  39. Pflock M., Kennard S., Delany I., Scarlato V., Beier D. 2005; Acid-induced activation of the urease promoters is mediated directly by the ArsRS two-component system of Helicobacter pylori . Infect Immun 73:6437–6445
    [Google Scholar]
  40. Pflock M., Finsterer N., Joseph B., Mollenkopf H., Meyer T. F., Beier D. 2006a; Characterization of the ArsRS regulon of Helicobacter pylori, involved in acid adaptation. J Bacteriol 188:3449–3462
    [Google Scholar]
  41. Pflock M., Kennard S., Finsterer N., Beier D. 2006b; Acid-responsive gene regulation in the human pathogen Helicobacter pylori . J Biotechnol 126:52–60
    [Google Scholar]
  42. Richard H. T., Foster J. W. 2003; Acid resistance in Escherichia coli . Adv Appl Microbiol 52:167–186
    [Google Scholar]
  43. Rose R. E. 1988; The nucleotide sequence of pACYC184. Nucleic Acids Res 16:355
    [Google Scholar]
  44. Rosqvist R., Skurnik M., Wolf-Watz H. 1988; Increased virulence of Yersinia pseudotuberculosis by two independent mutations. Nature 334:522–524
    [Google Scholar]
  45. Ruiz C., McMurry L. M., Levy S. B. 2008; Role of the multidrug resistance regulator MarA in global regulation of the hdeAB acid resistance operon in Escherichia coli . J Bacteriol 190:1290–1297
    [Google Scholar]
  46. Sayed A. K., Odom C., Foster J. W. 2007; The Escherichia coli AraC-family regulators GadX and GadW activate gadE, the central activator of glutamate-dependent acid resistance. Microbiology 153:2584–2592
    [Google Scholar]
  47. Simon R., Priefer U., Pühler A. 1983; A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology 1:784–791
    [Google Scholar]
  48. Stingl K., De Reuse H. 2005; Staying alive overdosed: how does Helicobacter pylori control urease activity?. Int J Med Microbiol 295:307–315
    [Google Scholar]
  49. Takada A., Umitsuki G., Nagai K., Wachi M. 2007; RNase E is required for induction of the glutamate-dependent acid resistance system in Escherichia coli . Biosci Biotechnol Biochem 71:158–164
    [Google Scholar]
  50. Tramonti A., De Canio M., Delany I., Scarlato V., De Biase D. 2006; Mechanisms of transcription activation exerted by GadX and GadW at the gadA and gadBC gene promoters of the glutamate-based acid resistance system in Escherichia coli . J Bacteriol 188:8118–8127
    [Google Scholar]
  51. Tucker D. L., Tucker N., Conway T. 2002; Gene expression profiling of the pH response in Escherichia coli . J Bacteriol 184:6551–6558
    [Google Scholar]
  52. Yoshida T., Qin L., Egger L. A., Inouye M. 2006; Transcription regulation of ompF and ompC by a single transcription factor, OmpR. J Biol Chem 281:17114–17123
    [Google Scholar]
  53. Young G. M., Amid D., Miller V. L. 1996; A bifunctional urease enhances survival of pathogenic Yersinia enterocolitica and Morganella morganii at low pH. J Bacteriol 178:6487–6495
    [Google Scholar]
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