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.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-147-5-1115
2001-05-01
2019-08-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/147/5/1471115a.html?itemId=/content/journal/micro/10.1099/00221287-147-5-1115&mimeType=html&fmt=ahah

References

  1. Bäumler, A. J. & Hantke, K. ( 1992; ). Ferrioxamine uptake in Yersinia enterocolitica: characterization of the receptor protein FoxA. Mol Microbiol 6, 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 Immun 65, 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 Bacteriol 180, 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. Microbiology 144, 1517-1526.[CrossRef]
    [Google Scholar]
  5. Boos, W. & Lucht, J. M. (1996). Periplasmic binding protein-dependent ABC transporters. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn, pp. 1175–1209. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
  6. Braun, V., Hantke, K. & Koster, W. ( 1998; ). Bacterial iron transport: mechanisms, genetics, and regulation. Metal Ions Biol Syst 35, 67-145.
    [Google Scholar]
  7. Brubaker, R. R. ( 1991; ). Factors promoting acute and chronic diseases caused by yersiniae. Clin Microbiol Rev 4, 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 Immun 67, 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 Microbiol 6, 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 Bacteriol 178, 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 Bacteriol 134, 1141-1156.
    [Google Scholar]
  12. Earhart, C. F. (1996). Uptake and metabolism of iron and molybdenum. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn, pp. 1075–1090. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
  13. Fetherston, J. D., Bearden, S. W. & Perry, R. D. ( 1996; ). YbtA, an AraC-type regulator of the Yersinia pestis pesticin/yersiniabactin receptor. Mol Microbiol 22, 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 Microbiol 32, 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 Microbiol 25, 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. Gene 18, 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 Bacteriol 17, 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 Biol 5, 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 Bacteriol 177, 4121-4130.
    [Google Scholar]
  20. Hanahan, D. ( 1983; ). Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166, 557-580.[CrossRef]
    [Google Scholar]
  21. Heesemann, J. ( 1987; ). Chromosomal-encoded siderophores are required for mouse virulence of enteropathogenic Yersinia species. FEMS Microbiol Lett 48, 229-233.[CrossRef]
    [Google Scholar]
  22. Heesemann, J. & Laufs, R. ( 1983; ). Construction of a mobilizable Yersinia enterocolitica virulence plasmid. J Bacteriol 155, 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 Immun 54, 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 Microbiol 8, 397-408.[CrossRef]
    [Google Scholar]
  25. Hu, P. C., Yang, G. C. & Brubaker, R. R. ( 1972; ). Specificity, induction, and absorption of pesticin. J Bacteriol 112, 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.
  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 Microbiol 30, 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. Cell 88, 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. Gene 109, 137-141.[CrossRef]
    [Google Scholar]
  30. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 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 Microbiol 9, 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 Bacteriol 170, 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 Bacteriol 180, 538-546.
    [Google Scholar]
  34. Perry, R. D. & Fetherston, J. D. ( 1997; ). Yersinia pestis – etiologic agent of plague. Clin Microbiol Rev 10, 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. Microbiology 145, 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.
    [Google Scholar]
  37. Rakin, A., Saken, E., Harmsen, D. & Heesemann, J. ( 1994; ). The pesticin receptor of Yersinia enterocolitica: a novel virulence factor with dual function. Mol Microbiol 13, 253-263.[CrossRef]
    [Google Scholar]
  38. Rakin, A., Urbitsch, P. & Heesemann, J. ( 1995; ). Evidence for two evolutionary lineages of highly pathogenic Yersinia species. J Bacteriol 177, 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 Immun 67, 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 , pp. 77-90. Edited by J. B. Kaper & J. Hacker. Washington, DC: American Society for Microbiology.
  41. Saken, E., Rakin, A. & Heesemann, J. ( 2000; ). Molecular characterization of a novel siderophore-independent iron transport system in Yersinia. Int J Med Microbiol 290, 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 Microbiol 4, 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 Immun 66, 480-485.
    [Google Scholar]
  44. Schubert, S., Fischer, D. & Heesemann, J. ( 1999; ). Ferric enterochelin transport in Yersinia enterocolitica: molecular and evolutionary aspects. J Bacteriol 181, 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 Dis 182, 1268-1271.[CrossRef]
    [Google Scholar]
  46. Schwyn, B. & Neilands, J. B. ( 1987; ). Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160, 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. Biotechnology 1, 784-785.
    [Google Scholar]
  48. Skorupski, K. & Taylor, R. K. ( 1996; ). Positive selection vectors for allelic exchange. Gene 169, 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 Bacteriol 176, 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 USA 82, 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 Immun 43, 895-900.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-147-5-1115
Loading
/content/journal/micro/10.1099/00221287-147-5-1115
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