Abstract
Many bacteria that cause diseases must be able to survive inside and outside the host. Attachment to and colonization of abiotic or biotic surfaces is a common mechanism by which various microorganisms enhance their ability to survive in diverse environments1. Vibrio cholerae is a Gram-negative aquatic bacillus that is often found in the environment attached to the chitinous exoskeletons of zooplankton2,3. It has been suggested that attachment to zooplankton enhances environmental survival of Vibrio spp., probably by providing both an abundant source of carbon and nitrogen and protection from numerous environmental challenges4. On ingestion by humans, some serogroups of V. cholerae cause the diarrhoeal disease cholera5. The pathophysiology of cholera is a result of the effects of cholera toxin on intestinal epithelial cells. For sufficient quantities of cholera toxin to reach the intestinal epithelium and to produce clinical symptoms, colonization of the small bowel must occur. Because most V. cholerae do not colonize humans, but all probably require strategies for survival in the environment, we considered that colonization factors selected for in the environment may be the same as those required for intestinal colonization of humans. In support of this hypothesis, here we have identified a single protein required for efficient intestinal colonization that mediates attachment to both zooplankton and human epithelial cells by binding to a sugar present on both surfaces.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout




Similar content being viewed by others
References
Reidl, J. & Klose, K. E. Vibrio cholerae and cholera: out of the water and into the host. FEMS Microbiol. Rev. 26, 125–139 (2002)
Tamplin, M. L., Gauzens, A. L., Huq, A., Sack, D. A. & Colwell, R. R. Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl. Environ. Microbiol. 56, 1977–1980 (1990)
Cottingham, K. L., Chiavelli, D. A. & Taylor, R. K. Environmental microbe and human pathogen: the ecology and microbiology of Vibrio cholerae. Front. Ecol. Environ. 1, 80–86 (2003)
Huq, A., Small, E., West, P. & Colwell, R. R. The role of planktonic copepods in the survival and multiplication of Vibrio cholerae in the aquatic environment. in Vibrios in the Environment (ed. Colwell, R. R.) 521–534 (John Wiley & Sons, New York, NY, 1984)
Kaper, J. B., Morris, J. G. & Levine, M. M. Cholera. Clin. Microbiol. Rev. 8, 48–86 (1995)
Heidelberg, J. F. et al. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406, 477–483 (2000)
Nalin, D. R., Daya, V., Reid, A., Levine, M. M. & Cisneros, L. Adsorption and growth of Vibrio cholerae on chitin. Infect. Immun. 25, 768–770 (1979)
Meibom, K. L. et al. The Vibrio cholerae chitin utilization program. Proc. Natl Acad. Sci. USA 101, 2524–2529 (2004)
Zampini, M. et al. Vibrio cholerae persistence in aquatic environments and colonization of intestinal cells: involvement of a common adhesion mechanism. FEMS Microbiol. Lett. 244, 267–273 (2005)
Tarsi, R. & Pruzzo, C. Role of surface proteins in Vibrio cholerae attachment to chitin. Appl. Environ. Microbiol. 65, 1348–1351 (1999)
Sasmal, D., Guhathakurta, B., Ghosh, A. N., Pal, C. R. & Datta, A. N-acetyl-d-glucosamine-specific lectin purified from Vibrio cholerae 01. FEMS Microbiol. Lett. 77, 217–224 (1992)
Finne, J. et al. Novel polyfucosylated N-linked glycopeptides with blood group A, H, X, and Y determinants from human small intestinal epithelial cells. J. Biol. Chem. 264, 5720–5735 (1989)
Bjork, S., Breimer, M. E., Hansson, G. C., Karlsson, K. A. & Leffler, H. Structures of blood group glycosphingolipids of human small intestine. A relation between the expression of fucolipids of epithelial cells and the ABO, Le and Se phenotype of the donor. J. Biol. Chem. 262, 6758–6765 (1987)
Miller, W. G. & Lindow, S. E. An improved GFP cloning cassette designed for prokaryotic transcriptional fusions. Gene 191, 149–153 (1997)
Chiavelli, D. A., Marsh, J. W. & Taylor, R. K. The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl. Environ. Microbiol. 67, 3220–3225 (2001)
Huo, A. et al. A simple filtration method to remove plankton-associated Vibrio cholerae in raw water supplies in developing countries. Appl. Environ. Microbiol. 62, 2508–2512 (1996)
Colwell, R. R. et al. Reduction of cholera in Bangladeshi villages by simple filtration. Proc. Natl Acad. Sci. USA 100, 1051–1055 (2003)
Sun, D. X., Mekalanos, J. J. & Taylor, R. K. Antibodies directed against the toxin-coregulated pilus isolated from Vibrio cholerae provide protection in the infant mouse experimental cholera model. J. Infect. Dis. 161, 1231–1236 (1990)
Connell, T. D., Metzger, D. J., Lynch, J. & Folster, J. P. Endochitinase is transported to the extracellular milieu by the eps-encoded general secretory pathway of Vibrio cholerae. J. Bacteriol. 180, 5591–5600 (1998)
Davis, B. M. et al. Convergence of the secretory pathways for cholera toxin and the filamentous phage, CTXφ. Science 288, 333–335 (2000)
Taylor, R. K., Miller, V. L., Furlong, D. B. & Mekalanos, J. J. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl Acad. Sci. USA 84, 2833–2837 (1987)
Skorupski, K. & Taylor, R. K. Sequence and functional analysis of the gene encoding Vibrio cholerae cAMP receptor protein. Gene 198, 297–303 (1997)
Skorupski, K. & Taylor, R. K. Cyclic AMP and its receptor protein negatively regulate the coordinate expression of cholera toxin and toxin-coregulated pilus in Vibrio cholerae. Proc. Natl Acad. Sci. USA 94, 265–270 (1997)
Skorupski, K. & Taylor, R. K. Positive selection vectors for allelic exchange. Gene 169, 47–52 (1996)
Benitez, J. A. et al. Adherence of Vibrio cholerae to cultured differentiated human intestinal cells: an in vitro colonization model. Infect. Immun. 65, 3474–3477 (1997)
Kirn, T. J. & Taylor, R. K. 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 (2005)
Kirn, T. J., Bose, N. & Taylor, R. K. Secretion of a soluble colonization factor by the TCP type 4 pilus biogenesis pathway in Vibrio cholerae. Mol. Microbiol. 49, 81–92 (2003)
Acknowledgements
We thank C. Sandoe for technical assistance. This work was supported by the NIH and a Rosalind Borison memorial fellowship.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.
Supplementary information
Supplementary Figures
This file contains Supplementary Figures 1–5. (PPT 907 kb)
Supplementary Figure Legends
This file contains text to accompany the above Supplementary Figures. (DOC 39 kb)
Rights and permissions
About this article
Cite this article
Kirn, T., Jude, B. & Taylor, R. A colonization factor links Vibrio cholerae environmental survival and human infection. Nature 438, 863–866 (2005). https://doi.org/10.1038/nature04249
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature04249
This article is cited by
-
The origins of pathogenesis
Nature Reviews Microbiology (2024)
-
Vibrio cholerae biofilms use modular adhesins with glycan-targeting and nonspecific surface binding domains for colonization
Nature Communications (2023)
-
Chitin degradation by Synechococcus WH7803
Scientific Reports (2023)
-
Chitinolytic enzymes contribute to the pathogenicity of Aliivibrio salmonicida LFI1238 in the invasive phase of cold-water vibriosis
BMC Microbiology (2022)
-
Bacterial protein MakA causes suppression of tumour cell proliferation via inhibition of PIP5K1α/Akt signalling
Cell Death & Disease (2022)