1887

Abstract

is a zoonotic pathogen and a common cause of gastroenteritis in humans. The species is composed of six diverse phylogroups, of which strains of phylogroup 1 are considered non-pathogenic to mammals due to the lack of the major virulence plasmid pYV, and their lack of virulence in a mouse infection model. In the present report we present data examining the pathogenicity of strains of across all six phylogroups in a model. We have demonstrated that in this model strains of phylogroup 1 exhibit severe pathogenesis with a lethal dose of as low as 10 c.f.u., that this virulence is an active process and that flagella play a major role in the virulence phenotype. We have also demonstrated that the complete lack of virulence in of the mammalian pathogenic phylogroups is not due to carriage of the pYV virulence plasmid. Our data suggest that all can be pathogenic, which may be a reflection of the true natural habitat of the species, and that we may need to reconsider the eco-evo perspective of this important bacterial species.

Keyword(s): Galleria , virulence and Yersinia
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000311
2016-08-01
2019-12-05
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/8/1379.html?itemId=/content/journal/micro/10.1099/mic.0.000311&mimeType=html&fmt=ahah

References

  1. Autenrieth I. B., Beer M., Bohn E., Kaufmann S. H., Heesemann J.. 1994; Immune responses to Yersinia enterocolitica in susceptible BALB/c and resistant C57BL/6 mice: an essential role for gamma interferon. Infect Immun62:2590–2599[PubMed]
    [Google Scholar]
  2. Bottone E. J.. 1997; Yersinia enterocolitica: the charisma continues. Clin Microbiol Rev10:257–276[PubMed]
    [Google Scholar]
  3. Bottone E. J.. 1999; Yersinia enterocolitica: overview and epidemiologic correlates. Microbes Infect1:323–333 [CrossRef][PubMed]
    [Google Scholar]
  4. Cornelis G. R., Wolf-Watz H.. 1997; The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol Microbiol23:861–867 [CrossRef][PubMed]
    [Google Scholar]
  5. Drummond N., Murphy B. P., Ringwood T., Prentice M. B., Buckley J. F., Fanning S.. 2012; Yersinia enterocolitica: a brief review of the issues relating to the zoonotic pathogen, public health challenges, and the pork production chain. Foodborne Pathog Dis9:179–189[CrossRef]
    [Google Scholar]
  6. Farmer J. J., Carter G. P., Miller V. L., Falkow S., Wachsmuth I. K.. 1992; Pyrazinamidase, CR-MOX agar, salicin fermentation-esculin hydrolysis, and D-xylose fermentation for identifying pathogenic serotypes of Yersinia enterocolitica . J Clin Microbiol30:2589–2594[PubMed]
    [Google Scholar]
  7. Fredriksson-Ahomaa M., Korkeala H.. 2003; Low occurrence of pathogenic Yersinia enterocolitica in clinical, food, and environmental samples: a methodological problem. Clin Microbiol Rev16:220–229 [CrossRef][PubMed]
    [Google Scholar]
  8. Fuchs T. M., Bresolin G., Marcinowski L., Schachtner J., Scherer S.. 2008; Insecticidal genes of Yersinia spp.: taxonomical distribution, contribution to toxicity towards Manduca sexta and Galleria mellonella, and evolution. BMC Microbiol8:214 [CrossRef][PubMed]
    [Google Scholar]
  9. Gaspar F., Teixeira N., Rigottier-Gois L., Marujo P., Nielsen-LeRoux C., Crespo M. T., Lopes M. de F., Serror P.. 2009; Virulence of Enterococcus faecalis dairy strains in an insect model: the role of fsrB and gelE . Microbiology155:3564–3571 [CrossRef][PubMed]
    [Google Scholar]
  10. Gierczyñski R., Szych J., Rastawicki W., Wardak S., Jagielski M.. 2009; Molecular characterization of human clinical isolates of Yersinia enterocolitica bioserotype 1B/O8 in Poland: emergence and dissemination of three highly related clones. J Clin Microbiol47:1225–1228 [CrossRef][PubMed]
    [Google Scholar]
  11. Grant T., Bennett-Wood V., Robins-Browne R. M.. 1999; Characterization of the interaction between Yersinia enterocolitica biotype 1A and phagocytes and epithelial cells in vitro. Infect Immun67:4367–4375[PubMed]
    [Google Scholar]
  12. Hall M., Chattaway M. A., Reuter S., Savin C., Strauch E., Carniel E., Connor T., Van Damme I., Rajakaruna L. et al. 2015; Use of whole-genus genome sequence data to develop a multilocus sequence typing tool that accurately identifies Yersinia isolates to the species and subspecies levels. J Clin Microbiol53:35–42 [CrossRef][PubMed]
    [Google Scholar]
  13. Handley S. A., Dube P. H., Revell P. A., Miller V. L.. 2004; Characterization of oral Yersinia enterocolitica infection in three different strains of inbred mice. Infect Immun72:1645–1656 [CrossRef][PubMed]
    [Google Scholar]
  14. Kado C. I., Liu S. T.. 1981; Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol145:1365–1373[PubMed]
    [Google Scholar]
  15. 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][PubMed]
    [Google Scholar]
  16. Kapatral V., Minnich S. A.. 1995; Co-ordinate, temperature-sensitive regulation of the three Yersinia enterocolitica flagellin genes. Mol Microbiol17:49–56 [CrossRef][PubMed]
    [Google Scholar]
  17. Kapatral V., Olson J. W., Pepe J. C., Miller V. L., Minnich S. A.. 1996; Temperature-dependent regulation of Yersinia enterocolitica Class III flagellar genes. Mol Microbiol19:1061–1071 [CrossRef][PubMed]
    [Google Scholar]
  18. Kumar P., Virdi J. S.. 2012; Identification and distribution of putative virulence genes in clinical strains of Yersinia enterocolitica biovar 1A by suppression subtractive hybridization. J Appl Microbiol113:1263–1272 [CrossRef][PubMed]
    [Google Scholar]
  19. Mallik S., Virdi J. S.. 2010; Genetic relationships between clinical and non-clinical strains of Yersinia enterocolitica biovar 1A as revealed by multilocus enzyme electrophoresis and multilocus restriction typing. BMC Microbiol10:158 [CrossRef][PubMed]
    [Google Scholar]
  20. Martínez P. O., Fredriksson-Ahomaa M., Pallotti A., Rosmini R., Houf K., Korkeala H.. 2011; Variation in the prevalence of enteropathogenic Yersinia in slaughter pigs from Belgium, Italy, and Spain. Foodborne Pathog Dis8:445–450 [CrossRef][PubMed]
    [Google Scholar]
  21. McNally A., Cheasty T., Fearnley C., Dalziel R. W., Paiba G. A., Manning G., Newell D. G.. 2004; Comparison of the biotypes of Yersinia enterocolitica isolated from pigs, cattle and sheep at slaughter and from humans with yersiniosis in Great Britain during 1999–2000. Lett Appl Microbiol39:103–108[CrossRef]
    [Google Scholar]
  22. McNally A., Dalton T., La Ragione R. M., Stapleton K., Manning G., Newell D. G.. 2006; Yersinia enterocolitica isolates of differing biotypes from humans and animals are adherent, invasive and persist in macrophages, but differ in cytokine secretion profiles in vitro. J Med Microbiol55:1725–1734 [CrossRef][PubMed]
    [Google Scholar]
  23. McNally A., La Ragione R. M., Best A., Manning G., Newell D. G.. 2007; An aflagellate mutant Yersinia enterocolitica biotype 1A strain displays altered invasion of epithelial cells, persistence in macrophages, and cytokine secretion profiles in vitro. Microbiology153:1339–1349 [CrossRef][PubMed]
    [Google Scholar]
  24. Milnes A. S., Stewart I., Clifton-Hadley F. A., Davies R. H., Newell D. G., Sayers A. R., Cheasty T., Cassar C., Ridley A. et al. 2008; Intestinal carriage of verocytotoxigenic Escherichia coli O157, Salmonella, thermophilic Campylobacter and Yersinia enterocolitica, in cattle, sheep and pigs at slaughter in Great Britain during 2003. Epidemiol Infect136:739–751 [CrossRef][PubMed]
    [Google Scholar]
  25. Reuter S., Connor T. R., Barquist L., Walker D., Feltwell T., Harris S. R., Fookes M., Hall M. E., Petty N. K. et al. 2014; Parallel independent evolution of pathogenicity within the genus Yersinia . Proc Natl Acad Sci U S A111:6768–6773 [CrossRef][PubMed]
    [Google Scholar]
  26. Reuter S., Corander J., de Been M., Harris S., Cheng L., Hall M., Thomson N. R., McNally A.. 2015; Directional gene flow and ecological separation in Yersinia enterocolitica . Microb Genomhttp://irep.ntu.ac.uk/25773/1/221318_PubSub2875_McNally.pdf [CrossRef][PubMed]
    [Google Scholar]
  27. Rosner B. M., Stark K., Werber D.. 2010; Epidemiology of reported Yersinia enterocolitica infections in Germany, 2001–2008. BMC Public Health10:337 [CrossRef][PubMed]
    [Google Scholar]
  28. Schiemann D. A., Devenish J. A.. 1982; Relationship of HeLa cell infectivity to biochemical, serological, and virulence characteristics of Yersinia enterocolitica . Infect Immun35:497–506[PubMed]
    [Google Scholar]
  29. Schippers A., Mateika S., Prochnow B., Gruber A. D., Müller W., Frischmann U.. 2008; Susceptibility of four inbred mouse strains to a low-pathogenic isolate of Yersinia enterocolitica . Mamm Genome19:279–291 [CrossRef][PubMed]
    [Google Scholar]
  30. Schmiel D. H., Young G. M., Miller V. L.. 2000; The Yersinia enterocolitica phospholipase gene yplA is part of the flagellar regulon. J Bacteriol182:2314–2320 [CrossRef][PubMed]
    [Google Scholar]
  31. Senior N. J., Bagnall M. C., Champion O. L., Reynolds S. E., La Ragione R. M., Woodward M. J., Salguero F. J., Titball R. W.. 2011; Galleria mellonella as an infection model for Campylobacter jejuni virulence. J Med Microbiol60:661–669 [CrossRef][PubMed]
    [Google Scholar]
  32. Singh I., Virdi J. S.. 2004; Production of Yersinia stable toxin (YST) and distribution of yst genes in biotype 1A strains of Yersinia enterocolitica . J Med Microbiol53:1065–1068 [CrossRef][PubMed]
    [Google Scholar]
  33. Tennant S. M., Grant T. H., Robins-Browne R. M.. 2003; Pathogenicity of Yersinia enterocolitica biotype 1A. FEMS Immunol Med Microbiol38:127–137 [CrossRef][PubMed]
    [Google Scholar]
  34. Tennant S. M., Skinner N. A., Joe A., Robins-Browne R. M.. 2005; Homologues of insecticidal toxin complex genes in Yersinia enterocolitica biotype 1A and their contribution to virulence. Infect Immun73:6860–6867 [CrossRef][PubMed]
    [Google Scholar]
  35. Thomson N. R., Howard S., Wren B. W., Holden M. T., Crossman L., Challis G. L., Churcher C., Mungall K., Brooks K. et al. 2006; The complete genome sequence and comparative genome analysis of the high pathogenicity Yersinia enterocolitica strain 8081. PLoS Genet2:e206 [CrossRef][PubMed]
    [Google Scholar]
  36. Valentin-Weigand P., Heesemann J., Dersch P.. 2014; Unique virulence properties of Yersinia enterocolitica O:3 - An emerging zoonotic pathogen using pigs as preferred reservoir host. Int J Med Microbiol14:00090–00093
    [Google Scholar]
  37. van Pelt W., de Wit M. A., Wannet W. J., Ligtvoet E. J., Widdowson M. A., van Duynhoven Y. T.. 2003; Laboratory surveillance of bacterial gastroenteric pathogens in The Netherlands, 1991–2001. Epidemiol Infect130:431–441[PubMed]
    [Google Scholar]
  38. Wauters G., Kandolo K., Janssens M.. 1987; Revised biogrouping scheme of Yersinia enterocolitica . Contrib Microbiol Immunol9:14–21[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000311
Loading
/content/journal/micro/10.1099/mic.0.000311
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
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