1887

Abstract

The major outer-membrane protein (MOMP) of and , encoded by the gene, is extremely genetically diverse. Conformational MOMP epitopes are important in host immunity, and variation in surface-exposed regions probably occurs as a result of positive immune selection during infection. diversity has been exploited in genotyping studies using highly discriminatory nucleotide sequences to identify potentially epidemiologically linked cases of human campylobacteriosis. To understand the overall nature and extent of diversity and stability in and we investigated sequences in isolates (=584) obtained from a defined human population (approx. 600 000) over a defined time period (1 year). A total of 196 distinct variants were identified. Regions encoding putative extracellular loops were the most variable in both nucleotide sequence and length. Phylogenetic analysis identified three allele clusters that originated in (i) predominantly and a few , (ii) solely or (iii) predominantly and a few . The stability of within an individual human host was investigated using isolates cultured longitudinally from 64 sporadic cases, 27 of which had prolonged infection lasting between 5 and 98 days (the remainder having illness of normal duration, 0–4 days), and 20 cases from family outbreaks. Evidence of mutation was detected in two patients with prolonged illness. Despite demonstrable positive immune selection in these two unusual cases, the persistence of numerous variants within the population indicated that the allele is a valuable tool for use in extended typing schemes.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.031047-0
2009-12-01
2019-11-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/12/4145.html?itemId=/content/journal/micro/10.1099/mic.0.031047-0&mimeType=html&fmt=ahah

References

  1. Buchanan, S. K. ( 1999; ). Beta-barrel proteins from bacterial outer membranes: structure, function and refolding. Curr Opin Struct Biol 9, 455–461.[CrossRef]
    [Google Scholar]
  2. Cawthraw, S. A., Feldman, R. A., Sayers, A. R. & Newell, D. G. ( 2002; ). Long-term antibody responses following human infection with Campylobacter jejuni. Clin Exp Immunol 130, 101–106.[CrossRef]
    [Google Scholar]
  3. Clark, C. G., Beeston, A., Bryden, L., Wang, G., Barton, C., Cuff, W., Gilmour, M. W. & Ng, L. K. ( 2007; ). Phylogenetic relationships of Campylobacter jejuni based on porA sequences. Can J Microbiol 53, 27–38.[CrossRef]
    [Google Scholar]
  4. Corry, J. E. & Atabay, H. I. ( 2001; ). Poultry as a source of Campylobacter and related organisms. Symp Ser Soc Appl Microbiol 96S–114S.
    [Google Scholar]
  5. Cowan, S. W., Schirmer, T., Rummel, G., Steiert, M., Ghosh, R., Pauptit, R. A., Jansonius, J. N. & Rosenbusch, J. P. ( 1992; ). Crystal structures explain functional properties of two E. coli porins. Nature 358, 727–733.[CrossRef]
    [Google Scholar]
  6. Didelot, X. & Falush, D. ( 2007; ). Inference of bacterial microevolution using multilocus sequence data. Genetics 175, 1251–1266.
    [Google Scholar]
  7. Dingle, K. E., Colles, F. M., Wareing, D. R. A., Ure, R., Fox, A. J., Bolton, F. J., Bootsma, H. J., Willems, R. J. L., Urwin, R. & Maiden, M. C. J. ( 2001; ). Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol 39, 14–23.[CrossRef]
    [Google Scholar]
  8. Dingle, K. E., Colles, F. M., Ure, R., Wagenaar, J., Duim, B., Bolton, F. J., Fox, A. J., Wareing, D. R. A. & Maiden, M. C. J. ( 2002; ). Molecular characterisation of Campylobacter jejuni clones: a rational basis for epidemiological investigations. Emerg Infect Dis 8, 949–955.[CrossRef]
    [Google Scholar]
  9. Dingle, K. E., Colles, F. M., Falush, D. & Maiden, M. C. ( 2005; ). Sequence typing and comparison of population biology of Campylobacter coli and Campylobacter jejuni. J Clin Microbiol 43, 340–347.[CrossRef]
    [Google Scholar]
  10. Dingle, K. E., McCarthy, N. D., Cody, A. J., Peto, T. E. & Maiden, M. C. ( 2008; ). Extended sequence typing of Campylobacter spp., United Kingdom. Emerg Infect Dis 14, 1620–1622.[CrossRef]
    [Google Scholar]
  11. Embley, T. M. ( 1991; ). The linear PCR reaction: a simple and robust method for sequencing amplified rRNA genes. Lett Appl Microbiol 13, 171–174.[CrossRef]
    [Google Scholar]
  12. Forbes, K. J., Gormley, F. J., Dallas, J. F., Labovitiadi, O., MacRae, M., Owen, R. J., Richardson, J., Strachan, N. J., Cowden, J. M. & other authors ( 2009; ). Campylobacter immunity and coinfection following a large outbreak in a farming community. J Clin Microbiol 47, 111–116.[CrossRef]
    [Google Scholar]
  13. Friedman, C. R., Hoekstra, R. M., Samuel, M., Marcus, R., Bender, J., Shiferaw, B., Reddy, S., Ahuja, S. D., Helfrick, D. L. & other authors ( 2004; ). Risk factors for sporadic Campylobacter infection in the United States: a case-control study in FoodNet sites. Clin Infect Dis 38 (Suppl. 3), S285–S296.[CrossRef]
    [Google Scholar]
  14. Gelman, A. & Rubin, D. B. ( 1992; ). Inference from iterative simulation using mulitple sequences. Stat Sci 7, 457–472.[CrossRef]
    [Google Scholar]
  15. Harrington, C. S., Thomson Carter, F. M. & Carter, P. E. ( 1997; ). Evidence for recombination in the flagellin locus of Campylobacter jejuni: implications for the flagellin gene typing scheme. J Clin Microbiol 35, 2386–2392.
    [Google Scholar]
  16. Hopkins, R. S., Olmsted, R. & Istre, G. R. ( 1984; ). Endemic Campylobacter jejuni infection in Colorado: identified risk factors. Am J Public Health 74, 249–250.[CrossRef]
    [Google Scholar]
  17. Huang, S., Luangtongkum, T., Morishita, T. Y. & Zhang, Q. ( 2005; ). Molecular typing of Campylobacter strains using the cmp gene encoding the major outer membrane protein. Foodborne Pathog Dis 2, 12–23.[CrossRef]
    [Google Scholar]
  18. Huang, S., Sahin, O. & Zhang, Q. ( 2007; ). Infection-induced antibodies against the major outer membrane protein of Campylobacter jejuni mainly recognize conformational epitopes. FEMS Microbiol Lett 272, 137–143.[CrossRef]
    [Google Scholar]
  19. Jeanteur, D., Lakey, J. H. & Pattus, F. ( 1991; ). The bacterial porin superfamily: sequence alignment and structure prediction. Mol Microbiol 5, 2153–2164.[CrossRef]
    [Google Scholar]
  20. Jones, K. ( 2001; ). Campylobacters in water, sewage and the environment. Symp Ser Soc Appl Microbiol 68S–79S.
    [Google Scholar]
  21. Kapperud, G., Lassen, J., Ostroff, S. M. & Aasen, S. ( 1992; ). Clinical features of sporadic Campylobacter infections in Norway. Scand J Infect Dis 24, 741–749.[CrossRef]
    [Google Scholar]
  22. Kapperud, G., Espeland, G., Wahl, E., Walde, A., Herikstad, H., Gustavsen, S., Tveit, I., Natas, O., Bevanger, L. & Digranes, A. ( 2003; ). Factors associated with increased and decreased risk of Campylobacter infection: a prospective case-control study in Norway. Am J Epidemiol 158, 234–242.[CrossRef]
    [Google Scholar]
  23. Kervella, M., Fauchere, J. L., Fourel, D. & Pages, J. M. ( 1992; ). Immunological cross-reactivity between outer membrane pore proteins of Campylobacter jejuni and Escherichia coli. FEMS Microbiol Lett 78, 281–285.
    [Google Scholar]
  24. Kessel, A. S., Gillespie, I. A., O'Brien, S. J., Adak, G. K., Humphrey, T. J. & Ward, L. R. ( 2001; ). General outbreaks of infectious intestinal disease linked with poultry, England and Wales, 1992–1999. Commun Dis Public Health 4, 171–177.
    [Google Scholar]
  25. Konkel, M. E., Gray, S. A., Kim, B. J., Garvis, S. G. & Yoon, J. ( 1999; ). Identification of the enteropathogens Campylobacter jejuni and Campylobacter coli based on the cadF virulence gene and its product. J Clin Microbiol 37, 510–517.
    [Google Scholar]
  26. Korber, B. ( 2000; ). HIV signature and sequence variation analysis. In Computational Analysis of HIV Molecular Sequences, pp. 55–72. Edited by A. G. Rodrigo & G. H. Learn. Dordrecht, Netherlands: Kluwer.
  27. McCarthy, N. D., Colles, F. M., Dingle, K. E., Bagnall, M. C., Manning, G., Maiden, M. C. & Falush, D. ( 2007; ). Host-associated genetic import in Campylobacter jejuni. Emerg Infect Dis 13, 267–272.[CrossRef]
    [Google Scholar]
  28. Meinersmann, R. J., Helsel, L. O., Fields, P. I. & Hiett, K. L. ( 1997; ). Discrimination of Campylobacter jejuni isolates by fla gene sequencing. J Clin Microbiol 35, 2810–2814.
    [Google Scholar]
  29. Miller, W. G., On, S. L., Wang, G., Fontanoz, S., Lastovica, A. J. & Mandrell, R. E. ( 2005; ). Extended multilocus sequence typing system for Campylobacter coli, C. lari, C. upsaliensis, and C. helveticus. J Clin Microbiol 43, 2315–2329.[CrossRef]
    [Google Scholar]
  30. Moser, I., Schroeder, W. & Salnikow, J. ( 1997; ). Campylobacter jejuni major outer membrane protein and a 59-kDa protein are involved in binding to fibronectin and INT 407 cell membranes. FEMS Microbiol Lett 157, 233–238.[CrossRef]
    [Google Scholar]
  31. Nachamkin, I. & Yang, X. H. ( 1989; ). Human antibody response to Campylobacter jejuni flagellin protein and a synthetic N-terminal flagellin peptide. J Clin Microbiol 27, 2195–2198.
    [Google Scholar]
  32. Nachamkin, I. & Yang, X. H. ( 1992; ). Local immune responses to the Campylobacter flagellin in acute Campylobacter gastrointestinal infection. J Clin Microbiol 30, 509–511.
    [Google Scholar]
  33. Nei, M. & Gojobori, T. ( 1986; ). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3, 418–426.
    [Google Scholar]
  34. Newell, D. G. & Nachamkin, I. ( 1992; ). Immune responses directed against Campylobacter jejuni. In Campylobacter jejuni: Current Status and Future Trends, pp. 201–206. Edited by I. Nachamkin, M. J. Blaser & L. S. Tompkins. Washington, DC: American Society for Microbiology.
  35. Ota, T. & Nei, M. ( 1994; ). Variance and covariances of the numbers of synonymous and nonsynonymous substitutions per site. Mol Biol Evol 11, 613–619.
    [Google Scholar]
  36. Page, W. J., Huyer, G., Huyer, M. & Worobec, E. A. ( 1989; ). Characterization of the porins of Campylobacter jejuni and Campylobacter coli and implications for antibiotic susceptibility. Antimicrob Agents Chemother 33, 297–303.[CrossRef]
    [Google Scholar]
  37. Pebody, R. G., Ryan, M. J. & Wall, P. G. ( 1997; ). Outbreaks of Campylobacter infection: rare events for a common pathogen. Commun Dis Rep CDR Rev 7, R33–R37.
    [Google Scholar]
  38. Schroder, W. & Moser, I. ( 1997; ). Primary structure analysis and adhesion studies on the major outer membrane protein of Campylobacter jejuni. FEMS Microbiol Lett 150, 141–147.[CrossRef]
    [Google Scholar]
  39. Sheppard, S. K., McCarthy, N. D., Falush, D. & Maiden, M. C. ( 2008; ). Convergence of Campylobacter species: implications for bacterial evolution. Science 320, 237–239.[CrossRef]
    [Google Scholar]
  40. Sheppard, S. K., Dallas, J. F., Strachan, N. J., MacRae, M., McCarthy, N. D., Wilson, D. J., Gormley, F. J., Falush, D., Ogden, I. D. & other authors ( 2009; ). Campylobacter genotyping to determine the source of human infection. Clin Infect Dis 48, 1072–1078.[CrossRef]
    [Google Scholar]
  41. Stanley, K. & Jones, K. ( 2003; ). Cattle and sheep farms as reservoirs of Campylobacter. J Appl Microbiol 94 (Suppl), 104S–113S.[CrossRef]
    [Google Scholar]
  42. Wagenaar, J. A., Mevius, D. J. & Havelaar, A. H. ( 2006; ). Campylobacter in primary animal production and control strategies to reduce the burden of human campylobacteriosis. Rev Sci Tech 25, 581–594.
    [Google Scholar]
  43. Wang, G., Clark, C. G., Taylor, T. M., Pucknell, C., Barton, C., Price, L., Woodward, D. L. & Rodgers, F. G. ( 2002; ). Colony multiplex PCR assay for identification and differentiation of Campylobacter jejuni, C. coli, C. lari, C. upsaliensis, and C. fetus subsp. fetus. J Clin Microbiol 40, 4744–4747.[CrossRef]
    [Google Scholar]
  44. Wilson, D. J., Gabriel, E., Leatherbarrow, A. J., Cheesbrough, J., Gee, S., Bolton, E., Fox, A., Hart, C. A., Diggle, P. J. & Fearnhead, P. ( 2009; ). Rapid evolution and the importance of recombination to the gastroenteric pathogen Campylobacter jejuni. Mol Biol Evol 26, 385–397.[CrossRef]
    [Google Scholar]
  45. Wingstrand, A., Neimann, J., Engberg, J., Nielsen, E. M., Gerner-Smidt, P., Wegener, H. C. & Molbak, K. ( 2006; ). Fresh chicken as main risk factor for campylobacteriosis, Denmark. Emerg Infect Dis 12, 280–285.[CrossRef]
    [Google Scholar]
  46. Young, K. T., Davis, L. M. & Dirita, V. J. ( 2007; ). Campylobacter jejuni: molecular biology and pathogenesis. Nat Rev Microbiol 5, 665–679.[CrossRef]
    [Google Scholar]
  47. Zhang, Q., Meitzler, J. C., Huang, S. & Morishita, T. ( 2000; ). Sequence polymorphism, predicted secondary structures, and surface-exposed conformational epitopes of Campylobacter major outer membrane protein. Infect Immun 68, 5679–5689.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.031047-0
Loading
/content/journal/micro/10.1099/mic.0.031047-0
Loading

Data & Media loading...

Supplements

[ PDF] (48KB), containing:

PDF

MLST, clonal complex (CC) and antigen data from human Campylobacter isolates obtained in Oxfordshire, UK, between mid-September 2003 and mid-September 2004. [ Excel File] (85KB) MLST, clonal complex (CC) and antigen data from humans who provided more than one Campylobacter sample per episode of illness in Oxfordshire, UK between September 2004 and July 2006. [ Excel File] (41KB) MLST, clonal complex (CC) and antigen data from Campylobacter isolates obtained from family outbreaks, where members of the same household presented with gastroenteritis within a time period of 0–7 days. [ Excel File] (26KB)

EXCEL

MLST, clonal complex (CC) and antigen data from human Campylobacter isolates obtained in Oxfordshire, UK, between mid-September 2003 and mid-September 2004. [ Excel File] (85KB) MLST, clonal complex (CC) and antigen data from humans who provided more than one Campylobacter sample per episode of illness in Oxfordshire, UK between September 2004 and July 2006. [ Excel File] (41KB) MLST, clonal complex (CC) and antigen data from Campylobacter isolates obtained from family outbreaks, where members of the same household presented with gastroenteritis within a time period of 0–7 days. [ Excel File] (26KB)

EXCEL

MLST, clonal complex (CC) and antigen data from human Campylobacter isolates obtained in Oxfordshire, UK, between mid-September 2003 and mid-September 2004. [ Excel File] (85KB) MLST, clonal complex (CC) and antigen data from humans who provided more than one Campylobacter sample per episode of illness in Oxfordshire, UK between September 2004 and July 2006. [ Excel File] (41KB) MLST, clonal complex (CC) and antigen data from Campylobacter isolates obtained from family outbreaks, where members of the same household presented with gastroenteritis within a time period of 0–7 days. [ Excel File] (26KB)

EXCEL
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