Genetic diversity and virulence potential of environmental Vibrio cholerae population in a cholera-endemic area

Shah M. Faruque, Nityananda Chowdhury, M. Kamruzzaman, Michelle Dziejman, M. Hasibur Rahman, David A. Sack, G. Balakrish Nair, John J. Mekalanos

Research output: Contribution to journalArticle

Abstract

To understand the evolutionary events and possible selection mechanisms involved in the emergence of pathogenic Vibrio cholerae, we analyzed diverse strains of V. cholerae isolated from environmental waters in Bangladesh by direct enrichment in the intestines of adult rabbits and by conventional laboratory culture. Strains isolated by conventional culture were mostly (99.2%) negative for the major virulence gene clusters encoding toxin-coregulated pilus (TCP) and cholera toxin (CT) and were nonpathogenic in animal models. In contrast, all strains selected in rabbits were competent for colonizing infant mice, and 56.8% of these strains carried genes encoding TCP alone or both TCP and CT. Ribotypes of toxigenic 01 and 0139 strains from the environment were similar to pandemic strains, whereas ribotypes of non-01 non-0139 strains and TCP- nontoxigenic 01 strains diverged widely from the seventh pandemic 01 and the 0139 strains. Results of this study suggest that (i) the environmental V. cholerae population in a cholera-endemic area is highly heterogeneous, (ii) selection in the mammalian intestine can cause enrichment of environmental strains with virulence potential, (iii) pathogenicity of V. cholerae involves more virulence genes than currently appreciated, and (iv) most environmental V. cholerae strains are unlikely to attain a pandemic potential by acquisition of TCP and CT genes alone. Because most of the recorded cholera pandemics originated in the Ganges Delta region, this ecological setting presumably favors extensive genetic exchange among V. cholerae strains and thus promotes the rare, multiple-gene transfer events needed to assemble the critical combination of genes required for pandemic spread.

Original languageEnglish (US)
Pages (from-to)2123-2128
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume101
Issue number7
DOIs
StatePublished - Feb 17 2004
Externally publishedYes

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Vibrio cholerae
Cholera
Pandemics
Virulence
Cholera Toxin
Population
Ribotyping
Genes
Intestines
Rabbits
Bangladesh
Multigene Family
Animal Models
Water

ASJC Scopus subject areas

  • Genetics
  • General

Cite this

Genetic diversity and virulence potential of environmental Vibrio cholerae population in a cholera-endemic area. / Faruque, Shah M.; Chowdhury, Nityananda; Kamruzzaman, M.; Dziejman, Michelle; Rahman, M. Hasibur; Sack, David A.; Nair, G. Balakrish; Mekalanos, John J.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 101, No. 7, 17.02.2004, p. 2123-2128.

Research output: Contribution to journalArticle

Faruque, Shah M. ; Chowdhury, Nityananda ; Kamruzzaman, M. ; Dziejman, Michelle ; Rahman, M. Hasibur ; Sack, David A. ; Nair, G. Balakrish ; Mekalanos, John J. / Genetic diversity and virulence potential of environmental Vibrio cholerae population in a cholera-endemic area. In: Proceedings of the National Academy of Sciences of the United States of America. 2004 ; Vol. 101, No. 7. pp. 2123-2128.
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