1887

Abstract

The acute diarrhoeal disease cholera is caused by the aquatic pathogen upon ingestion of contaminated food or water by the human host. The mechanisms by which is able to persist and survive in the host and aquatic environments have been studied for years; however, little is known about the factors involved in the adaptation or response of transitioning between these two environments. The transition from bacillary to coccoid morphology is thought to be one mechanism of survival that uses in response to environmental stress. Coccoid morphology has been observed for while in a viable but non-culturable (VBNC) state, during times of nutrient limitation, and in the water-diluted stool of cholera-infected patients. In this study we sought conditions to study the coccoid morphology of , and found that coccoid-shaped cells can express and produce the virulence factor toxin co-regulated pilus (TCP) and are able to colonize the infant mouse to the same extent as bacillus-shaped cells. This study suggests that TCP may be one factor that utilizes for adaptation and survival during the transition between the host and the aquatic environment.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.048561-0
2011-10-01
2019-12-05
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/10/2942.html?itemId=/content/journal/micro/10.1099/mic.0.048561-0&mimeType=html&fmt=ahah

References

  1. Baker R. M., Singleton F. L., Hood M. A.. ( 1983;). Effects of nutrient deprivation on Vibrio cholerae. . Appl Environ Microbiol 46:, 930–940.[PubMed]
    [Google Scholar]
  2. Bina J., Zhu J., Dziejman M., Faruque S., Calderwood S., Mekalanos J.. ( 2003;). ToxR regulon of Vibrio cholerae and its expression in vibrios shed by cholera patients. . Proc Natl Acad Sci U S A 100:, 2801–2806. [CrossRef][PubMed]
    [Google Scholar]
  3. Boulos L., Prévost M., Barbeau B., Coallier J., Desjardins R.. ( 1999;). LIVE/DEAD BacLight: application of a new rapid staining method for direct enumeration of viable and total bacteria in drinking water. . J Microbiol Methods 37:, 77–86. [CrossRef][PubMed]
    [Google Scholar]
  4. Carroll J. W., Mateescu M. C., Chava K., Colwell R. R., Bej A. K.. ( 2001;). Response and tolerance of toxigenic Vibro cholerae O1 to cold temperatures. . Antonie van Leeuwenhoek 79:, 377–384. [CrossRef][PubMed]
    [Google Scholar]
  5. Chaiyanan S., Chaiyanan S., Huq A., Maugel T., Colwell R. R.. ( 2001;). Viability of the nonculturable Vibrio cholerae O1 and O139. . Syst Appl Microbiol 24:, 331–341. [CrossRef][PubMed]
    [Google Scholar]
  6. Chaiyanan S., Chaiyanan S., Grim C., Maugel T., Huq A., Colwell R. R.. ( 2007;). Ultrastructure of coccoid viable but non-culturable Vibrio cholerae. . Environ Microbiol 9:, 393–402. [CrossRef][PubMed]
    [Google Scholar]
  7. Colwell R. R.. ( 2000;). Viable but nonculturable bacteria: a survival strategy. . J Infect Chemother 6:, 121–125. [CrossRef][PubMed]
    [Google Scholar]
  8. Cooper S.. ( 1997;). Division pattern of a round mutant of Escherichia coli. . J Bacteriol 179:, 5582–5584.[PubMed]
    [Google Scholar]
  9. Corbin B. D., Yu X. C., Margolin W.. ( 2002;). Exploring intracellular space: function of the Min system in round-shaped Escherichia coli. . EMBO J 21:, 1998–2008. [CrossRef][PubMed]
    [Google Scholar]
  10. Du M., Chen J., Zhang X., Li A., Li Y., Wang Y.. ( 2007;). Retention of virulence in a viable but nonculturable Edwardsiella tarda isolate. . Appl Environ Microbiol 73:, 1349–1354. [CrossRef][PubMed]
    [Google Scholar]
  11. Faruque S. M., Biswas K., Udden S. M., Ahmad Q. S., Sack D. A., Nair G. B., Mekalanos J. J.. ( 2006;). Transmissibility of cholera: in vivo-formed biofilms and their relationship to infectivity and persistence in the environment. . Proc Natl Acad Sci U S A 103:, 6350–6355. [CrossRef][PubMed]
    [Google Scholar]
  12. Felter R. A., Colwell R. R., Chapman G. B.. ( 1969;). Morphology and round body formation in Vibrio marinus. . J Bacteriol 99:, 326–335.[PubMed]
    [Google Scholar]
  13. Fischer-Le Saux M., Hervio-Heath D., Loaec S., Colwell R. R., Pommepuy M.. ( 2002;). Detection of cytotoxin-hemolysin mRNA in nonculturable populations of environmental and clinical Vibrio vulnificus strains in artificial seawater. . Appl Environ Microbiol 68:, 5641–5646. [CrossRef][PubMed]
    [Google Scholar]
  14. Halpern M., Broza Y. B., Mittler S., Arakawa E., Broza M.. ( 2004;). Chironomid egg masses as a natural reservoir of Vibrio cholerae non-O1 and non-O139 in freshwater habitats. . Microb Ecol 47:, 341–349. [CrossRef][PubMed]
    [Google Scholar]
  15. Henrici A. T.. ( 1925;). A statistical study of the form and growth of the cholera vibrio: three plates. . J Infect Dis 37:, 75–81. [CrossRef]
    [Google Scholar]
  16. Herrington D. A., Hall R. H., Losonsky G., Mekalanos J. J., Taylor R. K., Levine M. M.. ( 1988;). Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. . J Exp Med 168:, 1487–1492. [CrossRef][PubMed]
    [Google Scholar]
  17. Hulbert R. R., Taylor R. K.. ( 2002;). Mechanism of ToxT-dependent transcriptional activation at the Vibrio cholerae tcpA promoter. . J Bacteriol 184:, 5533–5544. [CrossRef][PubMed]
    [Google Scholar]
  18. Huq A., Colwell R. R., Rahman R., Ali A., Chowdhury M. A., Parveen S., Sack D. A., Russek-Cohen E.. ( 1990;). Detection of Vibrio cholerae O1 in the aquatic environment by fluorescent-monoclonal antibody and culture methods. . Appl Environ Microbiol 56:, 2370–2373.[PubMed]
    [Google Scholar]
  19. Islam M. S., Drasar B. S., Bradley D. J.. ( 1989;). Attachment of toxigenic Vibrio cholerae O1 to various freshwater plants and survival with a filamentous green alga, Rhizoclonium fontanum. . J Trop Med Hyg 92:, 396–401.[PubMed]
    [Google Scholar]
  20. Johnston M. D., Brown M. H.. ( 2002;). An investigation into the changed physiological state of Vibrio bacteria as a survival mechanism in response to cold temperatures and studies on their sensitivity to heating and freezing. . J Appl Microbiol 92:, 1066–1077. [CrossRef][PubMed]
    [Google Scholar]
  21. Justice S. S., Hung C., Theriot J. A., Fletcher D. A., Anderson G. G., Footer M. J., Hultgren S. J.. ( 2004;). Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. . Proc Natl Acad Sci U S A 101:, 1333–1338. [CrossRef][PubMed]
    [Google Scholar]
  22. Kamruzzaman M., Udden S. M., Cameron D. E., Calderwood S. B., Nair G. B., Mekalanos J. J., Faruque S. M.. ( 2010;). Quorum-regulated biofilms enhance the development of conditionally viable, environmental Vibrio cholerae. . Proc Natl Acad Sci U S A 107:, 1588–1593. [CrossRef][PubMed]
    [Google Scholar]
  23. Kaper J. B., Morris J. G. Jr, Levine M. M.. ( 1995;). Cholera. . Clin Microbiol Rev 8:, 48–86.[PubMed]
    [Google Scholar]
  24. Karaolis D. K., Somara S., Maneval D. R. Jr, Johnson J. A., Kaper J. B.. ( 1999;). A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria. . Nature 399:, 375–379. [CrossRef][PubMed]
    [Google Scholar]
  25. Kirn T. J., Taylor R. K.. ( 2005;). TcpF is a soluble colonization factor and protective antigen secreted by El Tor and classical O1 and O139 Vibrio cholerae serogroups. . Infect Immun 73:, 4461–4470. [CrossRef][PubMed]
    [Google Scholar]
  26. Kirn T. J., Lafferty M. J., Sandoe C. M., Taylor R. K.. ( 2000;). Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. . Mol Microbiol 35:, 896–910. [CrossRef][PubMed]
    [Google Scholar]
  27. Kirn T. J., Jude B. A., Taylor R. K.. ( 2005;). A colonization factor links Vibrio cholerae environmental survival and human infection. . Nature 438:, 863–866. [CrossRef][PubMed]
    [Google Scholar]
  28. Koch R.. ( 1884;). Über die Cholerabakterien. . Dtsch Med Wochenschr 10:, 725–728. [CrossRef]
    [Google Scholar]
  29. Krogfelt K. A., Poulsen L. K., Molin S.. ( 1993;). Identification of coccoid Escherichia coli BJ4 cells in the large intestine of streptomycin-treated mice. . Infect Immun 61:, 5029–5034.[PubMed]
    [Google Scholar]
  30. Lleò M. M., Pierobon S., Tafi M. C., Signoretto C., Canepari P.. ( 2000;). mRNA detection by reverse transcription-PCR for monitoring viability over time in an Enterococcus faecalis viable but nonculturable population maintained in a laboratory microcosm. . Appl Environ Microbiol 66:, 4564–4567. [CrossRef][PubMed]
    [Google Scholar]
  31. Lleò M. M., Bonato B., Signoretto C., Canepari P.. ( 2003;). Vancomycin resistance is maintained in enterococci in the viable but nonculturable state and after division is resumed. . Antimicrob Agents Chemother 47:, 1154–1156. [CrossRef][PubMed]
    [Google Scholar]
  32. Merrell D. S., Hava D. L., Camilli A.. ( 2002;). Identification of novel factors involved in colonization and acid tolerance of Vibrio cholerae. . Mol Microbiol 43:, 1471–1491. [CrossRef][PubMed]
    [Google Scholar]
  33. Miller J. H.. ( 1972;). Experiments in Molecular Genetics. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  34. Nilsson L., Oliver J. D., Kjelleberg S.. ( 1991;). Resuscitation of Vibrio vulnificus from the viable but nonculturable state. . J Bacteriol 173:, 5054–5059.[PubMed]
    [Google Scholar]
  35. Nye M. B., Pfau J. D., Skorupski K., Taylor R. K.. ( 2000;). Vibrio cholerae H-NS silences virulence gene expression at multiple steps in the ToxR regulatory cascade. . J Bacteriol 182:, 4295–4303. [CrossRef][PubMed]
    [Google Scholar]
  36. Oliver J. D.. ( 2005;). The viable but nonculturable state in bacteria. . J Microbiol 43: (Spec No), 93–100.[PubMed]
    [Google Scholar]
  37. Oliver J. D., Nilsson L., Kjelleberg S.. ( 1991;). Formation of nonculturable Vibrio vulnificus cells and its relationship to the starvation state. . Appl Environ Microbiol 57:, 2640–2644.[PubMed]
    [Google Scholar]
  38. Rahman I., Shahamat M., Kirchman P. A., Russek-Cohen E., Colwell R. R.. ( 1994;). Methionine uptake and cytopathogenicity of viable but nonculturable Shigella dysenteriae type 1. . Appl Environ Microbiol 60:, 3573–3578.[PubMed]
    [Google Scholar]
  39. Rahman I., Shahamat M., Chowdhury M. A., Colwell R. R.. ( 1996;). Potential virulence of viable but nonculturable Shigella dysenteriae type 1. . Appl Environ Microbiol 62:, 115–120.[PubMed]
    [Google Scholar]
  40. Reguera G., Kolter R.. ( 2005;). Virulence and the environment: a novel role for Vibrio cholerae toxin-coregulated pili in biofilm formation on chitin. . J Bacteriol 187:, 3551–3555. [CrossRef][PubMed]
    [Google Scholar]
  41. Rice S. A., McDougald D., Kjelleberg S.. ( 2000;). Vibrio vulnificus: a physiological and genetic approach to the viable but nonculturable response. . J Infect Chemother 6:, 115–120. [CrossRef][PubMed]
    [Google Scholar]
  42. Signoretto C., Di Stefano F., Canepari P.. ( 1996;). Modified peptidoglycan chemical composition in shape-altered Escherichia coli. . Microbiology 142:, 1919–1926. [CrossRef][PubMed]
    [Google Scholar]
  43. Smith B., Oliver J. D.. ( 2006a;). In situ gene expression by Vibrio vulnificus. . Appl Environ Microbiol 72:, 2244–2246. [CrossRef][PubMed]
    [Google Scholar]
  44. Smith B., Oliver J. D.. ( 2006b;). In situ and in vitro gene expression by Vibrio vulnificus during entry into, persistence within, and resuscitation from the viable but nonculturable state. . Appl Environ Microbiol 72:, 1445–1451. [CrossRef][PubMed]
    [Google Scholar]
  45. Sun D. X., Seyer J. M., Kovari I., Sumrada R. A., Taylor R. K.. ( 1991;). Localization of protective epitopes within the pilin subunit of the Vibrio cholerae toxin-coregulated pilus. . Infect Immun 59:, 114–118.[PubMed]
    [Google Scholar]
  46. Tamplin M. L., Gauzens A. L., Huq A., Sack D. A., Colwell R. R.. ( 1990;). Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. . Appl Environ Microbiol 56:, 1977–1980.[PubMed]
    [Google Scholar]
  47. Taylor R. K., Miller V. L., Furlong D. B., Mekalanos J. J.. ( 1986;). Identification of a pilus colonization factor that is coordinately regulated with cholera toxin. . Ann Sclavo Collana Monogr 3:, 51–61.[PubMed]
    [Google Scholar]
  48. Taylor R. K., Miller V. L., Furlong D. B., Mekalanos J. J.. ( 1987;). Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. . Proc Natl Acad Sci U S A 84:, 2833–2837. [CrossRef][PubMed]
    [Google Scholar]
  49. Watnick P. I., Kolter R.. ( 1999;). Steps in the development of a Vibrio cholerae El Tor biofilm. . Mol Microbiol 34:, 586–595. [CrossRef][PubMed]
    [Google Scholar]
  50. Weichart D., Kjelleberg S.. ( 1996;). Stress resistance and recovery potential of culturable and viable but nonculturable cells of Vibrio vulnificus. . Microbiology 142:, 845–853. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.048561-0
Loading
/content/journal/micro/10.1099/mic.0.048561-0
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