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Journal of Medical Microbiology logo Journal of Medical Microbiology

Volume 52, Issue 4

Expression of heterologous O-antigen in KIM does not affect virulence by the intravenous route No Access

Abstract

All strains of examined have been found to lack an O-antigen. In other members of the , the rough phenotype often results in attenuation. However, is the aetiological agent of bubonic plague. In evolving from the ancestral enteropathogenic , and with the development of an arthropod-vectored systemic pathogenesis, smooth LPS production is not necessary for virulence and the metabolic burden has been alleviated by inactivation of the O-antigen biosynthetic operon. To investigate this, strain KIM D27 was transformed with a plasmid carrying the operon encoding the O-antigen of O : 3. Expression of the O-antigen could be detected in silver-stained gels. The receptor for bacteriophage ϕYeO3-12 has been shown to be O-antigen, and infection by this bacteriophage results in lysis of O : 3. Expression of the O-antigen in conferred sensitivity to lysis by ϕYeO3-12. The O-antigen-expressing clone was shown to be as virulent in mice by the intravenous route of challenge as the rough wild-type. Assays showed no alteration in the ability of to resist lysis by cationic antimicrobial peptides, serum or polymyxin.

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© 2003 Society for General Microbiology
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2003-04-01
2025-06-24
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References

  1. Achtman M, Zurth K, Morelli C, 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 A 96:14043–14048 [CrossRef]
     [Google Scholar]
  2. al-Hendy A, Toivanen P, Skurnik M. 1991; Expression cloning of Yersinia enterocolitica O : 3 rfb gene cluster in Escherichia coli K12. Microb Pathog 10:47–59 [CrossRef]
     [Google Scholar]
  3. al-Hendy A, Toivanen P, Skurnik M. 1992; Lipopolysaccharide O side chain of Yersinia enterocolitica O : 3 is an essential virulence factor in an orally infected murine model. Infect Immun 60:870–875
     [Google Scholar]
  4. Baker E. E, Sommer H, Foster L. E, Meyer E, Meyer K. F. 1952; Studies on immunization against plague. I. The isolation and characterization of the soluble antigen of Pasteurella pestis . J Immunol 68:131–145
     [Google Scholar]
  5. Bayston K. F, Cohen J. 1990; Bacterial endotoxin and current concepts in the diagnosis and treatment of endotoxaemia. J Med Microbiol 31:73–83 [CrossRef]
     [Google Scholar]
  6. Bengoechea J.-A, Lindner B, Seydel U, Díaz R, Moriyón I. 1998; Yersinia pseudotuberculosis and Yersinia pestis are more resistant to bactericidal cationic peptides than Yersinia enterocolitica . Microbiology 144:1509–1515 [CrossRef]
     [Google Scholar]
  7. Bennett L. G, Tornabene T. G. 1974; Characterization of the antigenic subunits of the envelope protein of Yersinia pestis . J Bacteriol 117:48–55
     [Google Scholar]
  8. Bolivar F, Rodriguez R. L, Greene P. J, Betlach M. C, Heyneker H. L, Boyer H. W, Crosa J. H, Falkow S. 1977; Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene 2:95–113 [CrossRef]
     [Google Scholar]
  9. Brubaker R. R. 1991; Factors promoting acute and chronic diseases caused by yersiniae. Clin Microbiol Rev 4:309–324
     [Google Scholar]
  10. Butler T, Fu Y.-S, Furman L, Almeida C, Almeida A. 1982; Experimental Yersinia pestis infection in rodents after intragastric inoculation and ingestion of bacteria. Infect Immun 36:1160–1167
     [Google Scholar]
  11. Chart H. 1994; Lipopolysaccharide: isolation and characterization. In Methods in Practical Laboratory Bacteriology pp 11–20 Edited by Chart H. Boca Raton, FL: CRC Press;
     [Google Scholar]
  12. Christie A. B, Chen T. H, Elberg S. S. 1980; Plague in camels and goats: their role in human epidemics. J Infect Dis 141:724–726 [CrossRef]
     [Google Scholar]
  13. Cortes G, Borrell N, de Astorza B, Gomez C, Sauleda J, Alberti S. 2002; Molecular analysis of the contribution of the capsular polysaccharide and the lipopolysaccharide O side chain to the virulence of Klebsiella pneumoniae in a murine model of pneumonia. Infect Immun 70:2583–2590 [CrossRef]
     [Google Scholar]
  14. Ellwood D. C. 1968; The 3-deoxy-d-manno-octulosonic acid found in the lipopolysaccharide of Pasteurella species. Biochem J 106:47–48
     [Google Scholar]
  15. Estabrook M. M, Griffiss J. M, Jarvis G. A. 1997; Sialylation of Neisseria meningitidis lipooligosaccharide inhibits serum bactericidal activity by masking lacto- N -neotetraose. Infect Immun 65:4436–4444
     [Google Scholar]
  16. Garcia E, Nedialkov Y. A, Elliott J, Motin V. L, Brubaker R. R. 1999; Molecular characterization of KatY (antigen 5), a thermoregulated chromosomally encoded catalase-peroxidase of Yersinia pestis . J Bacteriol 181:3114–3122
     [Google Scholar]
  17. Groisman E. A. 1994; How bacteria resist killing by host-defense peptides. Trends Microbiol 2:444–449 [CrossRef]
     [Google Scholar]
  18. Hartley J. L, Adams G. A, Tornabene T. G. 1974; Chemical and physical properties of lipopolysaccharide of Yersinia pestis . J Bacteriol 118:848–854
     [Google Scholar]
  19. Hitchen P. G, Prior J. L, Oyston P. C. F, Panico M, Wren B. W, Titball R. W, Morris H. R, Dell A. 2002; Structural characterization of lipo-oligosaccharide (LOS) from Yersinia pestis : regulation of LOS structure by the PhoPQ system. Mol Microbiol 44:1637–1650 [CrossRef]
     [Google Scholar]
  20. Joiner K. A, Warren K. A, Brown E. J, Swanson J, Frank M. M. 1983; Studies on the mechanism of bacterial resistance to complement-mediated killing. IV C5b-9 forms high molecular weight complexes with bacterial outer membrane constituents on serum-resistant but not on serum-sensitive Neisseria gonorrhoeae . J Immunol 131:1443–1451
     [Google Scholar]
  21. Karlyshev A. V, Oyston P. C. F, Williams K, Clark G. C, Titball R. W, Winzeler E. A, Wren B. W. 2001; Application of high-density array-based signature-tagged mutagenesis to discover novel Yersinia virulence-associated genes. Infect Immun 69:7810–7819 [CrossRef]
     [Google Scholar]
  22. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [CrossRef]
     [Google Scholar]
  23. Makela P. H, Hovi M, Saxen H, Valtonen M, Valtonen V. 1988; Salmonella , complement and mouse macrophages. Immunol Lett 19:217–222 [CrossRef]
     [Google Scholar]
  24. Mandrell R. E, McLaughlin R, Aba Kwaik Y, Lesse A, Yamasaki R, Gibson B, Spinola S. M, Apicella M. A. 1992; Lipooligosaccharides (LOS) of some Haemophilus species mimic human glycosphingolipids, and some LOS are sialylated. Infect Immun 60:1322–1328
     [Google Scholar]
  25. McDonough K. A, Falkow S. 1989; A Yersinia pestis -specific DNA fragment encodes temperature-dependent coagulase and fibrinolysin-associated phenotypes. Mol Microbiol 3:767–775 [CrossRef]
     [Google Scholar]
  26. Mecsas J, Bilis I, Falkow S. 2001; Identification of attenuated Yersinia pseudotuberculosis strains and characterization of an orogastric infection in BALB/c mice on day 5 postinfection by signature-tagged mutagenesis. Infect Immun 69:2779–2787 [CrossRef]
     [Google Scholar]
  27. Nesper J, Lauriano C. M, Klose K. E, Kapfhammer D, Kraiss A, Reidl J. 2001; Characterization of Vibrio cholerae O1 El Tor galU and galE mutants: influence on lipopolysaccharide structure, colonization, and biofilm formation. Infect Immun 69:435–445 [CrossRef]
     [Google Scholar]
  28. Ogasawara M, Granfors K, Kono D. H, Hill J. L, Tak Yan Yu D. 1985; A Yersinia enterocolitica serotype O : 3 lipopolysaccharide-specific monoclonal antibody reacts more strongly with bacteria cultured at room temperature than those cultured at 37 °C. J Immunol 135:553–559
     [Google Scholar]
  29. Pajunen M, Kiljunen S, Skurnik M. 2000; Bacteriophage ϕYeO3-12, specific for Yersinia enterocolitica serotype O : 3, is related to coliphages T3 and T7. J Bacteriol 182:5114–5120 [CrossRef]
     [Google Scholar]
  30. Pajunen M. I, Kiljunen S. J, Soderholm M. E, Skurnik M. 2001; Complete genomic sequence of the lytic bacteriophage ϕYeO3-12 of Yersinia enterocolitica serotype O : 3. J Bacteriol 183:1928–1937 [CrossRef]
     [Google Scholar]
  31. Perry R. D, Fetherston J. D. 1997; Yersinia pestis – etiologic agent of plague. Clin Microbiol Rev 10:35–66
     [Google Scholar]
  32. Porat R, Johns M. A, McCabe W. R. 1987; Selective pressures and lipopolysaccharide subunits as determinants of resistance of clinical isolates of gram-negative bacilli to human serum. Infect Immun 55:320–328
     [Google Scholar]
  33. Porat R, McCabe W. R, Brubaker R. R. 1995; Lipopolysaccharide-associated resistance to killing of yersiniae by complement. J Endotoxin Res 2:91–97
     [Google Scholar]
  34. Prior J. L, Parkhill J, Hitchen P. G. 8 other authors 2001; The failure of different strains of Yersinia pestis to produce lipopolysaccharide O-antigen under different growth conditions is due to mutations in the O-antigen gene cluster. FEMS Microbiol Lett 197:229–233 [CrossRef]
     [Google Scholar]
  35. Reed L. J, Muench H. 1938; A simple method for estimating fifty percent endpoints. Am J Hyg 27:493–497
     [Google Scholar]
  36. Reeves P. 1994; Biosynthesis and assembly of lipopolysaccharide. In Bacterial Cell Wall pp 281–317 Edited by Hackenbeck R. Amsterdam: Elsevier;
     [Google Scholar]
  37. Sambrook J, Fritsch E. F, Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  38. Sebbane F, Devalckenaere A, Foulon J, Carniel E, Simonet M. 2001; Silencing and reactivation of urease in Yersinia pestis is determined by one G residue at a specific position in the ureD gene. Infect Immun 69:170–176 [CrossRef]
     [Google Scholar]
  39. Skurnik M. 1984; Lack of correlation between the presence of plasmids and fimbriae in Yersinia enterocolitica and Yersinia pseudotuberculosis . J Appl Bacteriol 56:355–363 [CrossRef]
     [Google Scholar]
  40. Skurnik M, Toivanen P. 1993; Yersinia enterocolitica lipopolysaccharide: genetics and virulence. Trends Microbiol 1:148–152 [CrossRef]
     [Google Scholar]
  41. Skurnik M, Venho R, Toivanen P, al-Hendy A. 1995; A novel locus of Yersinia enterocolitica serotype O : 3 involved in lipopolysaccharide outer core biosynthesis. Mol Microbiol 17:575–594 [CrossRef]
     [Google Scholar]
  42. Skurnik M, Venho R, Bengoechea J. A, Moriyon I. 1999; The lipopolysaccharide outer core of Yersinia enterocolitica serotype O : 3 is required for virulence and plays a role in outer membrane integrity. Mol Microbiol 31:1443–1462 [CrossRef]
     [Google Scholar]
  43. Skurnik M, Peippo A, Ervela E. 2000; Characterization of the O-antigen gene clusters of Yersinia pseudotuberculosis and the cryptic O-antigen gene cluster of Yersinia pestis shows that the plague bacillus is most closely related to and has evolved from Y. pseudotuberculosis serotype O : 1b. Mol Microbiol 37:316–330 [CrossRef]
     [Google Scholar]
  44. 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]
  45. Vinogradov E. V, Lindner B, Kocharova N. A. 7 other authors 2002; The core structure of the lipopolysaccharide from the causative agent of plague, Yersinia pestis . Carbohydr Res 337:775–777 [CrossRef]
     [Google Scholar]
  46. Vogel U, Claus H, Heinze G, Frosch M. 1999; Role of lipopolysaccharide sialylation in serum resistance of serogroup B and C meningococcal disease isolates. Infect Immun 67:954–957
     [Google Scholar]
  47. Wachter E, Brade V. 1989; Influence of surface modulations by enzymes and monoclonal antibodies on alternative complement pathway activation by Yersinia enterocolitica . Infect Immun 57:1984–1989
     [Google Scholar]
  48. Welkos S. L, Davis K. M, Pitt L. M, Worsham P. L, Friedlander A. M. 1995; Studies on the contribution of the F1 capsule-associated plasmid pFra to the virulence of Yersinia pestis . Contrib Microbiol Immunol 13:299–305
     [Google Scholar]
  49. Zhang L, Radziejewska-Lebrecht J, Krajewska-Pietrasik D, Toivanen P, Skurnik M. 1997; Molecular and chemical characterization of the lipopolysaccharide O-antigen and its role in the virulence of Yersinia enterocolitica serotype O : 8. Mol Microbiol 23:63–76 [CrossRef]
     [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.05044-0
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Expression of heterologous O-antigen in Yersinia pestis KIM does not affect virulence by the intravenous route
J. Med. Microbiol. 52, 289 (2003); https://doi.org/10.1099/jmm.0.05044-0
/content/journal/jmm/10.1099/jmm.0.05044-0
/content/journal/jmm/10.1099/jmm.0.05044-0
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