Abstract
The environmental reservoirs for Vibrio cholerae are natural aquatic habitats, where it colonizes the chitinous exoskeletons of copepod molts. Growth of V. cholerae on a chitin surface induces competence for natural transformation, a mechanism for intra-species gene exchange. The antigenically diverse O-serogroup determinants of V. cholerae are encoded by a genetically variable biosynthetic cluster of genes that is flanked on either side by chromosomal regions that are conserved between different serogroups. To determine whether this genomic motif and chitin-induced natural transformation might enable the exchange of serogroup-specific gene clusters between different O serogroups of V. cholerae, a strain of V. cholerae O1 El Tor was co-cultured with a strain of V. cholerae O139 Bengal within a biofilm on the same chitin surface immersed in seawater, and O1-to-O139 transformants were obtained. Serogroup conversion of the O1 recipient by the O139 donor was demonstrated by comparative genomic hybridization, biochemical and serological characterization of the O-antigenic determinant, and resistance of O1-to-O139 transformants to bacteriolysis by a virulent O1-specific phage. Serogroup conversion was shown to have occurred as a single-step exchange of large fragments of DNA. Crossovers were localized to regions of homology common to other V. cholerae serogroups that flank serogroup-specific encoding sequences. This result and the successful serogroup conversion of an O1 strain by O37 genomic DNA indicate that chitin-induced natural transformation might be a common mechanism for serogroup conversion in aquatic habitats and for the emergence of V. cholerae variants that are better adapted for survival in environmental niches or more pathogenic for humans.
Highlights
The reservoirs in nature for Vibrio cholerae, the cause of Asiatic cholera, are rivers, estuaries, and coastal waters, where it associates with the chitinous exoskeletons of copepod molts [1,2]
Genetic analysis showed that this outbreak was due to the acquisition of a gene cluster that converted the ancestral V. cholerae O1 El Tor serogroup to an entirely new serogroup, designated O139 Bengal
This report shows that acquisition of the O139 gene cluster by an O1 El Tor strain can be mediated by natural transformation and that this can occur within a community of bacteria living on a chitin surface
Summary
The reservoirs in nature for Vibrio cholerae, the cause of Asiatic cholera, are rivers, estuaries, and coastal waters, where it associates with the chitinous exoskeletons of copepod molts [1,2]. In the initial report of this phenomenon, competence was experimentally demonstrated by showing that it could mediate the acquisition of genes conferring antibiotic resistance during growth of a V. cholerae strain on a crab shell fragment immersed in seawater. This simple experimental system led to the identification of three positive regulators of the competence phenotype in V. cholerae, HapR, RpoS, and TfoX, and a type IV competence pseudopilus. In the work reported here, we begin to examine these issues by testing whether chitin-induced natural competence can mediate the uptake of genes that specify different V. cholerae O serogroups
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