1887

Abstract

The major gastrointestinal pathogen is shown to exist as three forms of monospecies biofilm in liquid culture. It attaches to a glass surface; forms an unattached aggregate (floc); and forms a pellicle at the liquid–gas interface. The three forms of biofilm resemble each other when examined by scanning electron microscopy. The biofilm mode of growth confers protection against environmental stress, the microaerobic bacteria in flocs surviving up to 24 days at ambient temperature and atmosphere compared to 12 days survival by planktonic bacteria. The wild-type strains 33106, 32799, 33084 and 31485 did not form flocs, and floc formation was reduced in strains mutant in a putative flagellar protein (FliS) and in a phosphate acetyltransferase (Cj0688). All other strains tested, including strains with mutations affecting capsular polysaccharide (), flagella (), protein glycosylation () and lipo-oligosaccharide () formed flocs. Similarly, all strains tested formed a pellicle and attached to glass except the aflagellate mutant ; pellicle formation was reduced in and mutants. Different mechanisms, therefore, may control formation of different forms of biofilm. It is proposed that these poorly characterized forms of growth are important for the persistence of in the environment and may in part explain the high incidence of Campylobacter-associated food borne disease.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28358-0
2006-02-01
2019-11-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/2/387.html?itemId=/content/journal/micro/10.1099/mic.0.28358-0&mimeType=html&fmt=ahah

References

  1. Black, R. E., Levine, M. M., Clements, M. L., Hughes, T. P. & Blaser, M. J. ( 1988; ). Experimental Campylobacter jejuni infection in humans. J Infect Dis 157, 472–479.[CrossRef]
    [Google Scholar]
  2. Buswell, C. M., Herlihy, Y. M., Lawrence, L. M., McGuiggan, J. T., Marsh, P. D., Keevil, C. W. & Leach, S. A. ( 1998; ). Extended survival and persistence of Campylobacter spp. in water and aquatic biofilms and their detection by immunofluorescent-antibody and -rRNA staining. Appl Environ Microbiol 64, 733–741.
    [Google Scholar]
  3. Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R. & Lappin-Scott, H. M. ( 1995; ). Microbial biofilms. Annu Rev Microbiol 49, 711–745.[CrossRef]
    [Google Scholar]
  4. CPLS ( 2000; ). Common gastrointestinal infections. Communicable Diseases Report Weekly England and Wales 10, 9–12.
    [Google Scholar]
  5. Danese, P. N., Pratt, L. A. & Kolter, R. ( 2000; ). Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J Bacteriol 182, 3593–3596.[CrossRef]
    [Google Scholar]
  6. Domingue, G., Ellis, B., Dasgupta, M. & Costerton, J. W. ( 1994; ). Testing antimicrobial susceptibilities of adherent bacteria by a method that incorporates guidelines of the National Committee for Clinical Laboratory Standards. J Clin Microbiol 32, 2564–2568.
    [Google Scholar]
  7. Friedman, L. & Kolter, R. ( 2004; ). Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51, 675–690.
    [Google Scholar]
  8. Golden, N. J. & Acheson, D. W. ( 2002; ). Identification of motility and autoagglutination Campylobacter jejuni mutants by random transposon mutagenesis. Infect Immun 70, 1761–1771.[CrossRef]
    [Google Scholar]
  9. Hall-Stoodley, L., Costerton, J. W. & Stoodley, P. ( 2004; ). Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2, 95–108.[CrossRef]
    [Google Scholar]
  10. Harris, R. H. & Mitchell, R. ( 1973; ). The role of polymers in microbial aggregation. Annu Rev Microbiol 27, 27–50.[CrossRef]
    [Google Scholar]
  11. Huber, B., Riedel, K., Hentzer, M., Heydorn, A., Gotschlich, A., Givskov, M., Molin, S. & Eberl, L. ( 2001; ). The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147, 2517–2528.
    [Google Scholar]
  12. Karlyshev, A. V. & Wren, B. W. ( 2005; ). Development and application of an insertional system for gene delivery and expression in Campylobacter jejuni. Appl Environ Microbiol 71, 4004–4013.[CrossRef]
    [Google Scholar]
  13. Karlyshev, A. V., Linton, D., Gregson, N. A., Lastovica, A. J. & Wren, B. W. ( 2000; ). Genetic and biochemical evidence of a Campylobacter jejuni capsular polysaccharide that accounts for Penner serotype specificity. Mol Microbiol 35, 529–541.
    [Google Scholar]
  14. 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.
    [Google Scholar]
  15. Keevil, C. W. ( 2003; ). Rapid detection of biofilms and adherent pathogens using scanning confocal laser microscopy and episcopic differential interference contrast microscopy. Water Sci Technol 47, 105–116.
    [Google Scholar]
  16. Kirov, S. M., Castrisios, M. & Shaw, J. G. ( 2004; ). Aeromonas flagella (polar and lateral) are enterocyte adhesins that contribute to biofilm formation on surfaces. Infect Immun 72, 1939–1945.[CrossRef]
    [Google Scholar]
  17. Linton, D., Karlyshev, A. V., Hitchen, P. G., Morris, H. R., Dell, A., Gregson, N. A. & Wren, B. W. ( 2000; ). Multiple N-acetyl neuraminic acid synthetase (neuB) genes in Campylobacter jejuni: identification and characterization of the gene involved in sialylation of lipo-oligosaccharide. Mol Microbiol 35, 1120–1134.[CrossRef]
    [Google Scholar]
  18. Linton, D., Allan, E., Karlyshev, A. V., Cronshaw, A. D. & Wren, B. W. ( 2002; ). Identification of N-acetylgalactosamine-containing glycoproteins PEB3 and CgpA in Campylobacter jejuni. Mol Microbiol 43, 497–508.[CrossRef]
    [Google Scholar]
  19. Loo, C. Y., Corliss, D. A. & Ganeshkumar, N. ( 2000; ). Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. J Bacteriol 182, 1374–1382.[CrossRef]
    [Google Scholar]
  20. Mack, D., Rohde, H., Dobinsky, S., Riedewald, J., Nedelmann, M., Knobloch, J. K., Elsner, H. A. & Feucht, H. H. ( 2000; ). Identification of three essential regulatory gene loci governing expression of Staphylococcus epidermidis polysaccharide intercellular adhesin and biofilm formation. Infect Immun 68, 3799–3807.[CrossRef]
    [Google Scholar]
  21. Marchant, J., Wren, B. & Ketley, J. ( 2002; ). Exploiting genome sequence: predictions for mechanisms of Campylobacter chemotaxis. Trends Microbiol 10, 155–159.[CrossRef]
    [Google Scholar]
  22. McLennan, M., Ringoir, D., Jarrell, H. C. Szymanski, C. & Gaynor, E. ( 2005; ). Characterisation of Campylobacter jejuni surface moiety that cross-reacts with calcofluor white: implications for surface carbohydrates, stress response, and pathogenesis. Abstracts of CHRO Meeting F32, 87.
    [Google Scholar]
  23. Misawa, N. & Blaser, M. J. ( 2000; ). Detection and characterization of autoagglutination activity by Campylobacter jejuni. Infect Immun 68, 6168–6175.[CrossRef]
    [Google Scholar]
  24. Moser, I. & Schroder, W. ( 1997; ). Hydrophobic characterization of thermophilic Campylobacter species and adhesion to INT 407 cell membranes and fibronectin. Microb Pathog 22, 155–164.[CrossRef]
    [Google Scholar]
  25. 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]
  26. Nichols, W. W. ( 1991; ). Biofilms, antibiotics and penetration. Rev Med Microbiol 2, 177–181.
    [Google Scholar]
  27. Ornek, D., Jayaraman, A., Syrett, B. C., Hsu, C. H., Mansfeld, F. B. & Wood, T. K. ( 2002; ). Pitting corrosion inhibition of aluminum 2024 by Bacillus biofilms secreting polyaspartate or gamma-polyglutamate. Appl Microbiol Biotechnol 58, 651–657.[CrossRef]
    [Google Scholar]
  28. Parkhill, J., Wren, B. W., Mungall, K. & 18 other authors ( 2000; ). The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665–668.[CrossRef]
    [Google Scholar]
  29. Pearson, A. D., Greenwood, M. H., Feltham, R. K., Healing, T. D., Donaldson, J., Jones, D. M. & Colwell, R. R. ( 1996; ). Microbial ecology of Campylobacter jejuni in a United Kingdom chicken supply chain: intermittent common source, vertical transmission, and amplification by flock propagation. Appl Environ Microbiol 62, 4614–4620.
    [Google Scholar]
  30. Salloway, S., Mermel, L. A., Seamans, M., Aspinall, G. O., Nam Shin, J. E., Kurjanczyk, L. A. & Penner, J. L. ( 1996; ). Miller-Fisher syndrome associated with Campylobacter jejuni bearing lipopolysaccharide molecules that mimic human ganglioside GD3. Infect Immun 64, 2945–2949.
    [Google Scholar]
  31. Sherlock, O., Vejborg, R. M. & Klemm, P. ( 2005; ). The TibA adhesin/invasin from enterotoxigenic Escherichia coli is self recognizing and induces bacterial aggregation and biofilm formation. Infect Immun 73, 1954–1963.[CrossRef]
    [Google Scholar]
  32. Solano, C., Garcia, B., Valle, J., Berasain, C., Ghigo, J. M., Gamazo, C. & Lasa, I. ( 2002; ). Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol Microbiol 43, 793–808.[CrossRef]
    [Google Scholar]
  33. Somers, E. B., Schoeni, J. L. & Wong, A. C. ( 1994; ). Effect of trisodium phosphate on biofilm and planktonic cells of Campylobacter jejuni, Escherichia coli O157 : H7, Listeria monocytogenes and Salmonella typhimurium. Int J Food Microbiol 22, 269–276.[CrossRef]
    [Google Scholar]
  34. Szymanski, C. M. & Wren, B. W. ( 2005; ). Protein glycosylation in bacterial mucosal pathogens. Nat Rev Microbiol 3, 225–237.[CrossRef]
    [Google Scholar]
  35. Trachoo, N., Frank, J. F. & Stern, N. J. ( 2002; ). Survival of Campylobacter jejuni in biofilms isolated from chicken houses. J Food Prot 65, 1110–1116.
    [Google Scholar]
  36. van Vliet, A. H., Wooldridge, K. G. & Ketley, J. M. ( 1998; ). Iron-responsive gene regulation in a Campylobacter jejuni fur mutant. J Bacteriol 180, 5291–5298.
    [Google Scholar]
  37. Watnick, P. I., Lauriano, C. M., Klose, K. E., Croal, L. & Kolter, R. ( 2001; ). The absence of a flagellum leads to altered colony morphology, biofilm development and virulence in Vibrio cholerae O139. Mol Microbiol 39, 223–235.[CrossRef]
    [Google Scholar]
  38. Whitchurch, C. B., Tolker-Nielsen, T., Ragas, P. C. & Mattick, J. S. ( 2002; ). Extracellular DNA required for bacterial biofilm formation. Science 295, 1487.[CrossRef]
    [Google Scholar]
  39. Whiteley, M., Ott, J. R., Weaver, E. A. & McLean, R. J. ( 2001; ). Effects of community composition and growth rate on aquifer biofilm bacteria and their susceptibility to betadine disinfection. Environ Microbiol 3, 43–52.[CrossRef]
    [Google Scholar]
  40. Wolfe, A. J., Chang, D. E., Walker, J. D. & 10 other authors ( 2003; ). Evidence that acetyl phosphate functions as a global signal during biofilm development. Mol Microbiol 48, 977–988.[CrossRef]
    [Google Scholar]
  41. Yuki, N. ( 1997; ). Molecular mimicry between gangliosides and lipopolysaccharides of Campylobacter jejuni isolated from patients with Guillain-Barre syndrome and Miller Fisher syndrome. J Infect Dis 176, Suppl 2, S150–S153.[CrossRef]
    [Google Scholar]
  42. Zimmer, M., Barnhart, H., Idris, U. & Lee, M. D. ( 2003; ). Detection of Campylobacter jejuni strains in the water lines of a commercial broiler house and their relationship to the strains that colonized the chickens. Avian Dis 47, 101–107.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28358-0
Loading
/content/journal/micro/10.1099/mic.0.28358-0
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