1887

Abstract

O:8, biogroup (BG) IB, strain WA-C carries a high-pathogenicity island (HPI) including iron-repressible genes (, ) for biosynthesis and uptake of the siderophore yersiniabactin (Ybt). The authors report the functional analysis of ,,, which show 98–99% similarity to the corresponding genes ,, on the HPI of . It was demonstrated that , are involved in ferric (Fe)-Ybt utilization and mouse virulence of , thus confirming corresponding results for . Additionally it was shown that inactivation of the like gene did not affect either Fe-Ybt utilization or mouse virulence. To determine whether , and (encoding the outer-membrane Fe-Ybt/pesticin receptor FyuA) are sufficient to mediate Fe-Ybt transport/utilization, these genes were transferred into , and into non-pathogenic , BG IA, strain NF-O. Surprisingly, , but not NF-O gained the capability to utilize exogenous Fe-Ybt as a result of this gene transfer, although both strains expressed functional FyuA (pesticin sensitivity). These results suggest that besides , and , additional genes are required for sufficient Fe-Ybt transport/utilization. Finally, it was shown that , and but not are involved in controlling Ybt biosynthesis and gene expression: and/or mutation leads to upregulation whereas mutation leads to downregulation. However, -dependent control of Ybt biosynthesis could be bypassed in a mutant by ingredients of chrome azurol S (CAS) siderophore indicator agar.

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2001-05-01
2020-09-21
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References

  1. Bäumler A. J.. Hantke K. 1992; Ferrioxamine uptake in Yersinia enterocolitica : characterization of the receptor protein FoxA. Mol Microbiol6:1309–1321[CrossRef]
    [Google Scholar]
  2. Bearden S. W., Fetherston J. D., Perry R. D. 1997; Genetic organization of the yersiniabactin biosynthetic region and construction of avirulent mutants in Yersinia pestis . Infect Immun65:1659–1668
    [Google Scholar]
  3. Bearden S. W., Staggs T. M., Perry R. D. 1998; An ABC transporter system of Yersinia pestis allows utilization of chelated iron by Escherichia coli SAB11. J Bacteriol180:1135–1147
    [Google Scholar]
  4. Bengoechea J. A., Brandenburg K., Seydel U., Diaz R., Moriyon I. 1998; Yersinia pseudotuberculosis and Yersinia pestis show increased outer membrane permeability to hydrophobic agents which correlates with lipopolysaccharide acyl-chain fluidity. Microbiology144:1517–1526[CrossRef]
    [Google Scholar]
  5. Boos W., Lucht J. M. others 1996; Periplasmic binding protein-dependent ABC transporters. In Escherichia coli and Salmonella: Cellular and Molecular Biology , 2nd edn. pp1175–1209 Edited by Neidhardt F. C.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  6. Braun V., Hantke K., Koster W. 1998; Bacterial iron transport: mechanisms, genetics, and regulation. Metal Ions Biol Syst35:67–145
    [Google Scholar]
  7. Brubaker R. R. 1991; Factors promoting acute and chronic diseases caused by yersiniae. Clin Microbiol Rev4:309–324
    [Google Scholar]
  8. Buchrieser C., Rusniok C., Frangeul L., Couve E., Billault A., Kunst F. 1999; The 102-kilobase pgm locus of Yersinia pestis : sequence analysis and comparison of selected regions among different Yersinia pestis and Yersinia pseudotuberculosis strains. Infect Immun67:4851–4861
    [Google Scholar]
  9. Carniel E., Guiyoule A., Guilvout I., Mercereau Puijalon O. 1992; Molecular cloning, iron-regulation and mutagenesis of the irp2 gene encoding HMWP2, a protein specific for the highly pathogenic Yersinia . Mol Microbiol6:379–388[CrossRef]
    [Google Scholar]
  10. Carniel E., Guilvout I., Prentice M. 1996; Characterization of a large chromosomal high-pathogenicity island in biotype 1B Yersinia enterocolitica . J Bacteriol178:6743–6751
    [Google Scholar]
  11. Chang A. C., Cohen S. N. 1978; Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol134:1141–1156
    [Google Scholar]
  12. Earhart C. F. others 1996; Uptake and metabolism of iron and molybdenum. In Escherichia coli and Salmonella: Cellular and Molecular Biology , 2nd edn. pp1075–1090 Edited by Neidhardt F. C.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  13. Fetherston J. D., Bearden S. W., Perry R. D. 1996; YbtA, an AraC-type regulator of the Yersinia pestis pesticin/yersiniabactin receptor. Mol Microbiol22:315–325[CrossRef]
    [Google Scholar]
  14. Fetherston J. D., Bertolino V. J., Perry R. D. 1999; YbtP and YbtQ: two ABC transporters required for iron uptake in Yersinia pestis . Mol Microbiol32:289–299[CrossRef]
    [Google Scholar]
  15. Flossmann K. D., Grajetzki C., Rosner H. 1985; Nachweis von Eisen-Transport-Aktivität in Pasteurella multocida -Kulturen. J Basic Microbiol25:559–567[CrossRef]
    [Google Scholar]
  16. Friedmann A. M., Long S. R., Brown S. E., Buikema W. J., Ausubel F. M. 1982; Construction of a broad-host-range cosmid cloning vector and its use in the genetic analysis of Rhizobium mutants. Gene18:289–296[CrossRef]
    [Google Scholar]
  17. Galan J. E., Ginocchio C., Costeas P. 1992; Molecular and functional characterization of the Salmonella typhimurium invasion gene invA : homology of InvA to members of a new protein family. J Bacteriol17:4338–4349
    [Google Scholar]
  18. Gehring A. M., DeMoll E., Fetherston J. D., Mori I., Mayhew G. F., Blattner F. R. 1998; Iron acquisition in plague: modular logic in enzymic biogenesis of yersiniabactin by Yersinia pestis . Chem Biol5:573–586[CrossRef]
    [Google Scholar]
  19. 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]
  20. Hanahan D. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol166:557–580[CrossRef]
    [Google Scholar]
  21. Heesemann J. 1987; Chromosomal-encoded siderophores are required for mouse virulence of enteropathogenic Yersinia species. FEMS Microbiol Lett48:229–233[CrossRef]
    [Google Scholar]
  22. Heesemann J., Laufs R. 1983; Construction of a mobilizable Yersinia enterocolitica virulence plasmid. J Bacteriol155:761–767
    [Google Scholar]
  23. Heesemann J., Gross U., Schmidt N., Laufs R. 1986; Immunochemical analysis of plasmid-encoded proteins released by enteropathogenic Yersinia sp. grown in calcium-deficient media. Infect Immun54:561–567
    [Google Scholar]
  24. Heesemann J., Hantke K., Vocke T., Saken E., Rakin A., Stojiljkovic I., Berner R. 1993; Virulence of Yersinia enterocolitica is closely associated with siderophore production, expression of an iron-repressible outer membrane polypeptide of 65000 Da and pesticin sensitivity. Mol Microbiol8:397–408[CrossRef]
    [Google Scholar]
  25. Hu P. C., Yang G. C., Brubaker R. R. 1972; Specificity, induction, and absorption of pesticin. J Bacteriol112:212–219
    [Google Scholar]
  26. Jacobi C. A. 1999; Analyse von Pathogenitätsfaktoren von Yersinia enterocolitica mit den Reportergenen GFP und Luziferase PhD thesis Universität Würzburg; Germany:
    [Google Scholar]
  27. Jacobi C. A., Roggenkamp A., Rakin A., Zumbihl R., Leitritz L., Heesemann J. 1998; In vitro and in vivo expression studies of yopE from Yersinia enterocolitica using the gfp reporter gene. Mol Microbiol30:865–882[CrossRef]
    [Google Scholar]
  28. Jacobs C., Frere J. M., Normark S. 1997; Cytosolic intermediates for cell wall biosynthesis and degradation control inducible beta-lactam resistance in Gram-negative bacteria. Cell88:823–832[CrossRef]
    [Google Scholar]
  29. Kaniga K., Delor I., Cornelis G. R. 1991; A wide-host-range suicide vector for improving reverse genetics in Gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica . Gene109:137–141[CrossRef]
    [Google Scholar]
  30. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685[CrossRef]
    [Google Scholar]
  31. Lindquist S., Weston-Hafer K., Schmidt H., Pul C., Korfmann G., Erickson J., Sanders C., Martin H. H., Normark S. 1993; AmpG, a signal transducer in chromosomal β-lactamase induction. Mol Microbiol9:703–715[CrossRef]
    [Google Scholar]
  32. Miller V. L., Mekalanos J. J. 1988; A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer-membrane proteins and virulence determinants in Vibrio cholerae requires toxR . J Bacteriol170:2575–2583
    [Google Scholar]
  33. Pelludat C., Rakin A., Jacobi C. A., Schubert S., Heesemann J. 1998; The yersiniabactin biosynthetic gene cluster of Yersinia enterocolitica : organization and siderophore-dependent regulation. J Bacteriol180:538–546
    [Google Scholar]
  34. Perry R. D., Fetherston J. D. 1997; Yersinia pestis – etiologic agent of plague. Clin Microbiol Rev10:35–66
    [Google Scholar]
  35. Perry R. D., Balbo P. B., Jones H. A., Fetherston J. D., DeMoll E. 1999; Yersiniabactin from Yersinia pestis : biochemical characterization of the siderophore and its role in iron transport and regulation. Microbiology145:1181–1190[CrossRef]
    [Google Scholar]
  36. Rakin A., Heesemann J. 1995; Yersiniabactin/pesticin receptor: a component of an iron uptake system of highly pathogenic Yersinia. Contrib Microbiol Immunol 13. 244–247
  37. Rakin A., Saken E., Harmsen D., Heesemann J. 1994; The pesticin receptor of Yersinia enterocolitica : a novel virulence factor with dual function. Mol Microbiol13:253–263[CrossRef]
    [Google Scholar]
  38. Rakin A., Urbitsch P., Heesemann J. 1995; Evidence for two evolutionary lineages of highly pathogenic Yersinia species. J Bacteriol177:2292–2298
    [Google Scholar]
  39. Rakin A., Noelting C., Schubert S., Heesemann J. 1999a; Common and specific characteristics of the high-pathogenicity island of Yersinia enterocolitica . Infect Immun67:5265–5274
    [Google Scholar]
  40. Rakin A., Schubert S., Pelludat C., Brem D., Heesemann J. 1999b; The high-pathogenicity island of yersiniae. In Pathogenicity Islands and Other Mobile Virulence Elements pp77–90 Edited by Kaper J. B., Hacker J.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  41. Saken E., Rakin A., Heesemann J. 2000; Molecular characterization of a novel siderophore-independent iron transport system in Yersinia . Int J Med Microbiol290:51–60[CrossRef]
    [Google Scholar]
  42. Sauer M., Hantke K., Braun V. 1990; Sequence of the fhuE outer-membrane receptor gene of Escherichia coli K-12 and properties of mutants. Mol Microbiol4:427–437[CrossRef]
    [Google Scholar]
  43. Schubert S., Rakin A., Karch H., Carniel E., Heesemann J. 1998; Prevalence of the ‘‘high-pathogenicity island’’ of Yersinia species among Escherichia coli strains that are pathogenic to humans. Infect Immun66:480–485
    [Google Scholar]
  44. Schubert S., Fischer D., Heesemann J. 1999; Ferric enterochelin transport in Yersinia enterocolitica : molecular and evolutionary aspects. J Bacteriol181:6387–6395
    [Google Scholar]
  45. Schubert S., Cuenca S., Fischer D., Heesemann J. 2000; High-pathogenicity island of Yersinia pestis in Enterobacteriaceae isolated from blood cultures and urine samples: prevalence and functional expression. J Infect Dis182:1268–1271[CrossRef]
    [Google Scholar]
  46. Schwyn B., Neilands J. B. 1987; Universal chemical assay for the detection and determination of siderophores. Anal Biochem160:47–56[CrossRef]
    [Google Scholar]
  47. Simon R., Priefer U., Pühler A. 1988; A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Biotechnology1:784–785
    [Google Scholar]
  48. Skorupski K., Taylor R. K. 1996; Positive selection vectors for allelic exchange. Gene169:47–52[CrossRef]
    [Google Scholar]
  49. Staggs T. M., Fetherston J. D., Perry R. D. 1994; Pleiotropic effects of a Yersinia pestis fur mutation. J Bacteriol176:7614–7624
    [Google Scholar]
  50. Tabor S., Richardson C. C. 1985; A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci USA82:1074–1078[CrossRef]
    [Google Scholar]
  51. Une T., Brubaker R. R. 1984; In vivo comparison of avirulent Vwa and Pgm or Pstr phenotypes of yersiniae. Infect Immun43:895–900
    [Google Scholar]
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