1887

Abstract

Human illness due to infection is closely associated with consumption of poultry products. We previously demonstrated a 50 % shift in allele frequency (phase variation) in contingency gene () during passage of NCTC11168 populations through Ross 308 broiler chickens. We hypothesized that phase variation in contingency genes during chicken passage could promote subsequent colonization and disease in humans. To test this hypothesis, we passaged strains NCTC11168, 33292, 81-176, KanR4 and CamR2 through broiler chickens and analysed the ability of passaged and non-passaged populations to colonize C57BL6 IL-10-deficient mice, our model for human colonization and disease. We utilized fragment analysis and nucleotide sequence analysis to measure phase variation in contingency genes. Passage through the chicken reservoir promoted phase variation in five specific contingency genes, and these ‘successful’ populations colonized mice. When phase variation did not occur in these same five contingency genes during chicken passage, these ‘unsuccessful’ populations failed to colonize mice. Phase variation during chicken passage generated small insertions or deletions (indels) in the homopolymeric tract (HT) in contingency genes. Single-colony isolates of strain KanR4 carrying an allele of contingency gene with a10G HT colonized mice at high frequency and caused disease symptoms, whereas single-colony isolates carrying the 9G allele failed to colonize mice. Supporting results were observed for the successful 9G allele of in strain 33292. These data suggest that phase variation in and is strongly associated with mouse colonization and disease, and that the chicken reservoir can play an active role in natural selection, phase variation and disease.

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2012-05-01
2024-04-16
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References

  1. Ang C. W., Dijkstra J. R., de Klerk M. A., Endtz H. P., van Doorn P. A., Jacobs B. C., Jeurissen S. H. M., Wagenaar J. A. ( 2010). Host factors determine anti-GM1 response following oral challenge of chickens with Guillain-Barré syndrome derived Campylobacter jejuni strain GB11. PLoS ONE 5:e9820 [View Article][PubMed]
    [Google Scholar]
  2. Bacon D. J., Alm R. A., Burr D. H., Hu L., Kopecko D. J., Ewing C. P., Trust T. J., Guerry P. ( 2000). Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect Immun 68:4384–4390 [View Article][PubMed]
    [Google Scholar]
  3. Balbontín R., Rowley G., Pucciarelli M. G., López-Garrido J., Wormstone Y., Lucchini S., García-Del Portillo F., Hinton J. C., Casadesús J. ( 2006). DNA adenine methylation regulates virulence gene expression in Salmonella enterica serovar Typhimurium. J Bacteriol 188:8160–8168 [View Article][PubMed]
    [Google Scholar]
  4. Batz M. B., Hoffmann D., Morris J. G. ( 2011). Report. Ranking the Risks: the 10 Pathogen-Food Combinations with the Greatest Burden on Public Health Gainesville FL: University of Florida, Emerging Pathogens Institute;
    [Google Scholar]
  5. Bell J. A., St Charles J. L., Murphy A. J., Rathinam V. A., Plovanich-Jones A. E., Stanley E. L., Wolf J. E., Gettings J. R., Whittam T. S., Mansfield L. S. ( 2009). Multiple factors interact to produce responses resembling spectrum of human disease in Campylobacter jejuni infected C57BL/6 IL-10−/− mice. BMC Microbiol 9:57 [View Article][PubMed]
    [Google Scholar]
  6. Blaser M. J. ( 1997). Epidemiologic and clinical features of Campylobacter jejuni infections. J Infect Dis 176:Suppl. 2S103–S105 [View Article][PubMed]
    [Google Scholar]
  7. Dasti J. I., Tareen A. M., Lugert R., Zautner A. E., Groß U. ( 2010). Campylobacter jejuni: a brief overview on pathogenicity-associated factors and disease-mediating mechanisms. Int J Med Microbiol 300:205–211 [View Article][PubMed]
    [Google Scholar]
  8. Fälker S., Schmidt M. A., Heusipp G. ( 2005). DNA methylation in Yersinia enterocolitica: role of the DNA adenine methyltransferase in mismatch repair and regulation of virulence factors. Microbiology 151:2291–2299 [View Article][PubMed]
    [Google Scholar]
  9. French C. E., Bell J. M. L., Ward F. B. ( 2008). Diversity and distribution of hemerythrin-like proteins in prokaryotes. FEMS Microbiol Lett 279:131–145 [View Article][PubMed]
    [Google Scholar]
  10. Guerry P. ( 2007). Campylobacter flagella: not just for motility. Trends Microbiol 15:456–461 [View Article][PubMed]
    [Google Scholar]
  11. Guerry P., Szymanski C. M. ( 2008). Campylobacter sugars sticking out. Trends Microbiol 16:428–435 [View Article][PubMed]
    [Google Scholar]
  12. Guerry P., Szymanski C. M., Prendergast M. M., Hickey T. E., Ewing C. P., Pattarini D. L., Moran A. P. ( 2002). Phase variation of Campylobacter jejuni 81-176 lipooligosaccharide affects ganglioside mimicry and invasiveness in vitro . Infect Immun 70:787–793 [View Article][PubMed]
    [Google Scholar]
  13. Gundogdu O., Bentley S. D., Holden M. T., Parkhill J., Dorrell N., Wren B. W. ( 2007). Re-annotation and re-analysis of the Campylobacter jejuni NCTC11168 genome sequence. BMC Genomics 8:162 [View Article][PubMed]
    [Google Scholar]
  14. Humphrey T., O’Brien S., Madsen M. ( 2007). Campylobacters as zoonotic pathogens: a food production perspective. Int J Food Microbiol 117:237–257 [View Article][PubMed]
    [Google Scholar]
  15. Jerome J. P., Bell J. A., Plovanich-Jones A. E., Barrick J. E., Brown C. T., Mansfield L. S. ( 2011). Standing genetic variation in contingency loci drives the rapid adaptation of Campylobacter jejuni to a novel host. PLoS ONE 6:e16399 [View Article][PubMed]
    [Google Scholar]
  16. Jonsson M. E., Norström M., Sandberg M., Ersbøll A. K., Hofshagen M. ( 2010). Space–time patterns of Campylobacter spp. colonization in broiler flocks, 2002–2006. Epidemiol Infect 138:1336–1345 [View Article][PubMed]
    [Google Scholar]
  17. Karlyshev A. V., Linton D., Gregson N. A., Wren B. W. ( 2002). A novel paralogous gene family involved in phase-variable flagella-mediated motility in Campylobacter jejuni . Microbiology 148:473–480[PubMed]
    [Google Scholar]
  18. Karlyshev A. V., Champion O. L., Churcher C., Brisson J. R., Jarrell H. C., Gilbert M., Brochu D., St Michael F., Li J. & other authors ( 2005). Analysis of Campylobacter jejuni capsular loci reveals multiple mechanisms for the generation of structural diversity and the ability to form complex heptoses. Mol Microbiol 55:90–103 [View Article][PubMed]
    [Google Scholar]
  19. Linton D., Gilbert M., Hitchen P. G., Dell A., Morris H. R., Wakarchuk W. W., Gregson N. A., Wren B. W. ( 2000). Phase variation of a β-1,3 galactosyltransferase involved in generation of the ganglioside GM1-like lipo-oligosaccharide of Campylobacter jejuni . Mol Microbiol 37:501–514 [View Article][PubMed]
    [Google Scholar]
  20. Mansfield L. S., Gauthier D. T., Abner S. R., Jones K. M., Wilder S. R., Urban J. F. ( 2003). Enhancement of disease and pathology by synergy of Trichuris suis and Campylobacter jejuni in the colon of immunologically naïve swine. Am J Trop Med Hyg 68:70–80
    [Google Scholar]
  21. Mansfield L. S., Bell J. A., Wilson D. L., Murphy A. J., Elsheikha H. M., Rathinam V. A. K., Fierro B. R., Linz J. E., Young V. B. ( 2007). C57BL/6 and congenic interleukin-10-deficient mice can serve as models of Campylobacter jejuni colonization and enteritis. Infect Immun 75:1099–1115 [View Article][PubMed]
    [Google Scholar]
  22. Mansfield L. S., Patterson J. S., Fierro B. R., Murphy A. J., Rathinam V. A., Kopper J. J., Barbu N. I., Onifade T. J., Bell J. A. ( 2008). Genetic background of IL-10−/− mice alters host–pathogen interactions with Campylobacter jejuni and influences disease phenotype. Microb Pathog 45:241–257 [View Article][PubMed]
    [Google Scholar]
  23. McNally D. J., Lamoureux M. P., Karlyshev A. V., Fiori L. M., Li J. J., Thacker G., Coleman R. A., Khieu N. H., Wren B. W. & other authors ( 2007). Commonality and biosynthesis of the O-methyl phosphoramidate capsule modification in Campylobacter jejuni . J Biol Chem 282:28566–28576 [View Article][PubMed]
    [Google Scholar]
  24. Miller C. E., Williams P. H., Ketley J. M. ( 2009). Pumping iron: mechanisms for iron uptake by Campylobacter . Microbiology 155:3157–3165 [View Article][PubMed]
    [Google Scholar]
  25. Morooka T., Umeda A., Amako K. ( 1985). Motility as an intestinal colonization factor for Campylobacter jejuni . J Gen Microbiol 131:1973–1980[PubMed]
    [Google Scholar]
  26. Moxon R., Bayliss C., Hood D. ( 2006). Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu Rev Genet 40:307–333 [View Article][PubMed]
    [Google Scholar]
  27. Oshima T., Wada C., Kawagoe Y., Ara T., Maeda M., Masuda Y., Hiraga S., Mori H. ( 2002). Genome-wide analysis of deoxyadenosine methyltransferase-mediated control of gene expression in Escherichia coli . Mol Microbiol 45:673–695 [View Article][PubMed]
    [Google Scholar]
  28. Parkhill J., Wren B. W., Mungall K., Ketley J. M., Churcher C., Basham D., Chillingworth T., Davies R. M., Feltwell T. & other authors ( 2000). The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665–668 [View Article][PubMed]
    [Google Scholar]
  29. Rosqvist R., Skurnik M., Wolf-Watz H. ( 1988). Increased virulence of Yersinia pseudotuberculosis by two independent mutations. Nature 334:522–524 [View Article][PubMed]
    [Google Scholar]
  30. Sang F. C., Shane S. M., Yogasundram K., Hagstad H. V., Kearney M. T. ( 1989). Enhancement of Campylobacter jejuni virulence by serial passage in chicks. Avian Dis 33:425–430 [View Article][PubMed]
    [Google Scholar]
  31. Scallan E., Hoekstra R. M., Angulo F. J., Tauxe R. V., Widdowson M. A., Roy S. L., Jones J. L., Griffin P. M. ( 2011). Foodborne illness acquired in the United States–major pathogens. Emerg Infect Dis 17:7–15 [View Article][PubMed]
    [Google Scholar]
  32. Snelling W. J., Matsuda M., Moore J. E., Dooley J. S. G. ( 2005). Campylobacter jejuni . Lett Appl Microbiol 41:297–302 [View Article][PubMed]
    [Google Scholar]
  33. Srikhanta Y. N., Fox K. L., Jennings M. P. ( 2010). The phasevarion: phase variation of type III DNA methyltransferases controls coordinated switching in multiple genes. Nat Rev Microbiol 8:196–206 [View Article][PubMed]
    [Google Scholar]
  34. van der Woude M. W., Bäumler A. J. ( 2004). Phase and antigenic variation in bacteria. Clin Microbiol Rev 17:581–611 [View Article][PubMed]
    [Google Scholar]
  35. van Ham S. M., van Alphen L., Mooi F. R., van Putten J. P. ( 1993). Phase variation of H. influenzae fimbriae: transcriptional control of two divergent genes through a variable combined promoter region. Cell 73:1187–1196 [View Article][PubMed]
    [Google Scholar]
  36. Wassenaar T. M. ( 2011). Following an imaginary Campylobacter population from farm to fork and beyond: a bacterial perspective. Lett Appl Microbiol 53:253–263 [View Article][PubMed]
    [Google Scholar]
  37. Wassenaar T. M., Wagenaar J. A., Rigter A., Fearnley C., Newell D. G., Duim B. ( 2002). Homonucleotide stretches in chromosomal DNA of Campylobacter jejuni display high frequency polymorphism as detected by direct PCR analysis. FEMS Microbiol Lett 212:77–85 [View Article][PubMed]
    [Google Scholar]
  38. Willems R., Paul A., van der Heide H. G. J., ter Avest A. R., Mooi F. R. ( 1990). Fimbrial phase variation in Bordetella pertussis: a novel mechanism for transcriptional regulation. EMBO J 9:2803–2809[PubMed]
    [Google Scholar]
  39. Wilson D. L., Bell J. A., Young V. B., Wilder S. R., Mansfield L. S., Linz J. E. ( 2003). Variation of the natural transformation frequency of Campylobacter jejuni in liquid shake culture. Microbiology 149:3603–3615 [View Article][PubMed]
    [Google Scholar]
  40. Wilson D. L., Rathinam V. A. K., Qi W., Wick L. M., Landgraf J., Bell J. A., Plovanich-Jones A., Parrish J., Finley R. L. & other authors ( 2010). Genetic diversity in Campylobacter jejuni is associated with differential colonization of broiler chickens and C57BL/6J IL10-deficient mice. Microbiology 156:2046–2057 [View Article][PubMed]
    [Google Scholar]
  41. Yao R., Burr D. H., Guerry P. ( 1997). CheY-mediated modulation of Campylobacter jejuni virulence. Mol Microbiol 23:1021–1031 [View Article][PubMed]
    [Google Scholar]
  42. Young K. T., Davis L. M., Dirita V. J. ( 2007). Campylobacter jejuni: molecular biology and pathogenesis. Nat Rev Microbiol 5:665–679 [View Article][PubMed]
    [Google Scholar]
  43. Yuki N. ( 2010). Human gangliosides and bacterial lipo-oligosaccharides in the development of autoimmune neuropathies. Methods Mol Biol 600:51–65 [View Article][PubMed]
    [Google Scholar]
  44. Zhao S., Young S. R., Tong E., Abbott J. W., Womack N., Friedman S. L., McDermott P. F. ( 2010). Antimicrobial resistance of Campylobacter isolates from retail meat in the United States between 2002 and 2007. Appl Environ Microbiol 76:7949–7956 [View Article][PubMed]
    [Google Scholar]
  45. Zhu J. G., Hua X. G., Wu Z. L., Yi M. M. ( 2006). Molecular mechanisms of pathogenesis of Campylobacter jejuni . Rev Med Microbiol 17:39–43 [View Article]
    [Google Scholar]
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