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Genomic and phenotypic characterization of Vibrio cholerae non-O1 isolates from a US Gulf Coast cholera outbreak.

Haley BJ, Choi SY, Grim CJ, Onifade TJ, Cinar HN, Tall BD, Taviani E, Hasan NA, Abdullah AH, Carter L, Sahu SN, Kothary MH, Chen A, Baker R, Hutchinson R, Blackmore C, Cebula TA, Huq A, Colwell RR - PLoS ONE (2014)

Bottom Line: From the 11 diagnosed cases, eight isolates of V. cholerae were isolated and their genomes were sequenced.Comparative genomics, phenotypic analyses, and a Caenorhabditis elegans model of infection for the isolates were conducted.This analysis coupled with isolation data of V. cholerae O75 and O141 suggests these strains may represent an underappreciated clade of cholera-causing strains responsible for significant disease burden globally.

View Article: PubMed Central - PubMed

Affiliation: Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland, United States of America.

ABSTRACT
Between November 2010, and May 2011, eleven cases of cholera, unrelated to a concurrent outbreak on the island of Hispaniola, were recorded, and the causative agent, Vibrio cholerae serogroup O75, was traced to oysters harvested from Apalachicola Bay, Florida. From the 11 diagnosed cases, eight isolates of V. cholerae were isolated and their genomes were sequenced. Genomic analysis demonstrated the presence of a suite of mobile elements previously shown to be involved in the disease process of cholera (ctxAB, VPI-1 and -2, and a VSP-II like variant) and a phylogenomic analysis showed the isolates to be sister taxa to toxigenic V. cholerae V51 serogroup O141, a clinical strain isolated 23 years earlier. Toxigenic V. cholerae O75 has been repeatedly isolated from clinical cases in the southeastern United States and toxigenic V. cholerae O141 isolates have been isolated globally from clinical cases over several decades. Comparative genomics, phenotypic analyses, and a Caenorhabditis elegans model of infection for the isolates were conducted. This analysis coupled with isolation data of V. cholerae O75 and O141 suggests these strains may represent an underappreciated clade of cholera-causing strains responsible for significant disease burden globally.

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Neighbour-joining tree inferring phylogenetic relationships of 84 V. cholerae genomes based on 995 orthologous protein-coding genes (954,646 bp).V. cholerae FL Group is labelled in red and V. cholerae V51 is labelled in blue. Haiti non-O1/non-O139 clinical groups-1 and -2 are further defined by Hasan et al. [6]. Numbers at nodes represent bootstrap values. Nucleotide substitution model is the Kimura-2-parameter. Bar length = 0.002 nucleotide substitutions per site.
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pone-0086264-g001: Neighbour-joining tree inferring phylogenetic relationships of 84 V. cholerae genomes based on 995 orthologous protein-coding genes (954,646 bp).V. cholerae FL Group is labelled in red and V. cholerae V51 is labelled in blue. Haiti non-O1/non-O139 clinical groups-1 and -2 are further defined by Hasan et al. [6]. Numbers at nodes represent bootstrap values. Nucleotide substitution model is the Kimura-2-parameter. Bar length = 0.002 nucleotide substitutions per site.

Mentions: The eight isolates subjected to analysis in this study have been labeled by number (isolates CP1110, 1111, 1112, 1113, 1114, 1115, 1116 and 1117) and are hereafter collectively referred to as the V. cholerae FL Group. The phylogeny of 84 fully and partially sequenced V. cholerae strains, including the eight V. cholerae FL Group genomes, was inferred (Figure 1). Results of the analysis demonstrate that the V. cholerae FL Group are sister taxa with V. cholerae V51, a clinical V. cholerae O141 serogroup strain isolated from a human clinical case in the United States in 1987, suggesting a common ancestor after it had diverged from other V. cholerae lineages. From a public health perspective, the results of the analysis demonstrate the group represents a phyletic lineage of V. cholerae non-O1/non-O139 strains that persist in the United States as a cause of morbidity. Although, not added to this analysis due to the absence of their sequenced genomes, results of this analysis coupled with V. cholerae isolation data from cholera patients worldwide demonstrate that other V. cholerae serogroup O141 and O75 strains result in similar clinical manifestations as the strains in this study, that is symptoms of cholera [30], [31]. As with the isolates sequenced in this analysis, other V. cholerae O141 and O75 infections in the United States were associated with either seafood consumption or presence of the patient in a coastal state, suggesting infections with strains of these serogroups are transmitted to people in a similar manner as those of the O1 serogroup and therefore they have a similar ecology as serogroup O1 strains in the United States [32], [33].


Genomic and phenotypic characterization of Vibrio cholerae non-O1 isolates from a US Gulf Coast cholera outbreak.

Haley BJ, Choi SY, Grim CJ, Onifade TJ, Cinar HN, Tall BD, Taviani E, Hasan NA, Abdullah AH, Carter L, Sahu SN, Kothary MH, Chen A, Baker R, Hutchinson R, Blackmore C, Cebula TA, Huq A, Colwell RR - PLoS ONE (2014)

Neighbour-joining tree inferring phylogenetic relationships of 84 V. cholerae genomes based on 995 orthologous protein-coding genes (954,646 bp).V. cholerae FL Group is labelled in red and V. cholerae V51 is labelled in blue. Haiti non-O1/non-O139 clinical groups-1 and -2 are further defined by Hasan et al. [6]. Numbers at nodes represent bootstrap values. Nucleotide substitution model is the Kimura-2-parameter. Bar length = 0.002 nucleotide substitutions per site.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3974666&req=5

pone-0086264-g001: Neighbour-joining tree inferring phylogenetic relationships of 84 V. cholerae genomes based on 995 orthologous protein-coding genes (954,646 bp).V. cholerae FL Group is labelled in red and V. cholerae V51 is labelled in blue. Haiti non-O1/non-O139 clinical groups-1 and -2 are further defined by Hasan et al. [6]. Numbers at nodes represent bootstrap values. Nucleotide substitution model is the Kimura-2-parameter. Bar length = 0.002 nucleotide substitutions per site.
Mentions: The eight isolates subjected to analysis in this study have been labeled by number (isolates CP1110, 1111, 1112, 1113, 1114, 1115, 1116 and 1117) and are hereafter collectively referred to as the V. cholerae FL Group. The phylogeny of 84 fully and partially sequenced V. cholerae strains, including the eight V. cholerae FL Group genomes, was inferred (Figure 1). Results of the analysis demonstrate that the V. cholerae FL Group are sister taxa with V. cholerae V51, a clinical V. cholerae O141 serogroup strain isolated from a human clinical case in the United States in 1987, suggesting a common ancestor after it had diverged from other V. cholerae lineages. From a public health perspective, the results of the analysis demonstrate the group represents a phyletic lineage of V. cholerae non-O1/non-O139 strains that persist in the United States as a cause of morbidity. Although, not added to this analysis due to the absence of their sequenced genomes, results of this analysis coupled with V. cholerae isolation data from cholera patients worldwide demonstrate that other V. cholerae serogroup O141 and O75 strains result in similar clinical manifestations as the strains in this study, that is symptoms of cholera [30], [31]. As with the isolates sequenced in this analysis, other V. cholerae O141 and O75 infections in the United States were associated with either seafood consumption or presence of the patient in a coastal state, suggesting infections with strains of these serogroups are transmitted to people in a similar manner as those of the O1 serogroup and therefore they have a similar ecology as serogroup O1 strains in the United States [32], [33].

Bottom Line: From the 11 diagnosed cases, eight isolates of V. cholerae were isolated and their genomes were sequenced.Comparative genomics, phenotypic analyses, and a Caenorhabditis elegans model of infection for the isolates were conducted.This analysis coupled with isolation data of V. cholerae O75 and O141 suggests these strains may represent an underappreciated clade of cholera-causing strains responsible for significant disease burden globally.

View Article: PubMed Central - PubMed

Affiliation: Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland, United States of America.

ABSTRACT
Between November 2010, and May 2011, eleven cases of cholera, unrelated to a concurrent outbreak on the island of Hispaniola, were recorded, and the causative agent, Vibrio cholerae serogroup O75, was traced to oysters harvested from Apalachicola Bay, Florida. From the 11 diagnosed cases, eight isolates of V. cholerae were isolated and their genomes were sequenced. Genomic analysis demonstrated the presence of a suite of mobile elements previously shown to be involved in the disease process of cholera (ctxAB, VPI-1 and -2, and a VSP-II like variant) and a phylogenomic analysis showed the isolates to be sister taxa to toxigenic V. cholerae V51 serogroup O141, a clinical strain isolated 23 years earlier. Toxigenic V. cholerae O75 has been repeatedly isolated from clinical cases in the southeastern United States and toxigenic V. cholerae O141 isolates have been isolated globally from clinical cases over several decades. Comparative genomics, phenotypic analyses, and a Caenorhabditis elegans model of infection for the isolates were conducted. This analysis coupled with isolation data of V. cholerae O75 and O141 suggests these strains may represent an underappreciated clade of cholera-causing strains responsible for significant disease burden globally.

Show MeSH
Related in: MedlinePlus