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Molecular analysis of the emergence of pandemic Vibrio parahaemolyticus.

ABSTRACT: BACKGROUND: Vibrio parahaemolyticus is abundant in the aquatic environment particularly in warmer waters and is the leading cause of seafood borne gastroenteritis worldwide. Prior to 1995, numerous V. parahaemolyticus serogroups were associated with disease, however, in that year an O3:K6 serogroup emerged in Southeast Asia causing large outbreaks and rapid hospitalizations. This new highly virulent strain is now globally disseminated. RESULTS: We performed a four-way BLAST analysis on the genome sequence of V. parahaemolyticus RIMD2210633, an O3:K6 isolate from Japan recovered in 1996, versus the genomes of four published Vibrio species and constructed genome BLAST atlases. We identified 24 regions, gaps in the genome atlas, of greater than 10 kb that were unique to RIMD2210633. These 24 regions included an integron, f237 phage, 2 type III secretion systems (T3SS), a type VI secretion system (T6SS) and 7 Vibrio parahaemolyticus genomic islands (VPaI-1 to VPaI-7). Comparative genomic analysis of our fifth genome, V. parahaemolyticus AQ3810, an O3:K6 isolate recovered in 1983, identified four regions unique to each V. parahaemolyticus strain. Interestingly, AQ3810 did not encode 8 of the 24 regions unique to RMID, including a T6SS, which suggests an additional virulence mechanism in RIMD2210633. The distribution of only the VPaI regions was highly variable among a collection of 42 isolates and phylogenetic analysis of these isolates show that these regions are confined to a pathogenic clade. CONCLUSION: Our data show that there is considerable genomic flux in this species and that the new highly virulent clone arose from an O3:K6 isolate that acquired at least seven novel regions, which included both a T3SS and a T6SS.

SUBMITTER: Boyd EF

PROVIDER: S-EPMC2491623 | biostudies-literature | 2008

REPOSITORIES: biostudies-literature

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Molecular analysis of the emergence of pandemic Vibrio parahaemolyticus.

Boyd E Fidelma EF Cohen Ana Luisa V AL Naughton Lynn M LM Ussery David W DW Binnewies Tim T TT Stine O Colin OC Parent Michelle A MA

BMC microbiology 20080630

<h4>Background</h4>Vibrio parahaemolyticus is abundant in the aquatic environment particularly in warmer waters and is the leading cause of seafood borne gastroenteritis worldwide. Prior to 1995, numerous V. parahaemolyticus serogroups were associated with disease, however, in that year an O3:K6 serogroup emerged in Southeast Asia causing large outbreaks and rapid hospitalizations. This new highly virulent strain is now globally disseminated.<h4>Results</h4>We performed a four-way BLAST analysis ...[more]

PMID: 18590559

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Project description:A strain of Vibrio parahaemolyticus that emerged in 1995 caused the first known pandemic involving this species. This strain comprises clonal autochthonous ocean-dwelling bacteria whose evolution has occurred in the ocean environment. The low sequence diversity in this population enabled the discovery of information on its origin and evolution that has been hidden in bacterial clones that have evolved over a long period. Multilocus sequencing and microarray analysis, together with phylogenetic analysis, of pandemic and pre-pandemic isolates has suggested that the founder clone was an O3:K6 non-pathogenic strain that initially acquired a toxRS/new region and subsequently acquired at least seven novel genomic islands. Sequencing and comparison of whole genomes later confirmed these early observations, and it confirmed that most of the genetic changes occurred via gene conversion involving horizontally transmitted DNA. The highly clonal population rapidly diversified, especially in terms of antigenicity, and 27 serotypes have already been reported. Comparisons of the core genomes derived from the founder clone indicate that there are only a few hundred single-nucleotide variations between isolates. However, when the whole genome is considered (the core plus non-core genome and from any clonal frame), the amount of DNA with a different clonal frame can reach up to 4.2% and the number of single-nucleotide variations can reach several hundred thousand. Altogether, these and previous observations based on multilocus sequence typing, microarray analysis, and whole-genome sequencing indicate the large contribution made by DNA with different clonal genealogy to genome diversification. The evidence also indicates that horizontal gene transfer (HGT) caused the emergence of new pathogens. Furthermore, the extent of HGT seems to depend on the vicissitudes of the life of each bacterium, as exemplified by differences in thousands of base pairs acquired by HGT among almost identical genetic isolates.

Project description:In China, V. parahaemolyticus has been a leading cause of foodborne outbreaks and bacterial infectious diarrhea since the 1990s, and most infections have been associated with the pandemic V. parahaemolyticus O3:K6 and its serovariants. However, a comprehensive overview of the sero-prevalence and genetic diversity of the pandemic V. parahaemolyticus clone in China is lacking. To compensate for this deficiency, pandemic isolates in both clinical and environmental Chinese samples collected from multiple studies were analyzed in this study. Surprisingly, as many as 27 clinical pandemic serovariants were identified and were widely distributed across nine coastal provinces and two inland provinces (Beijing and Sichuan). O3:K6, O4:K68, and O1:KUT represented the predominant clinical serovars. Only four environmental pandemic serovariants had previously been reported, and they were spread throughout Shanghai (O1:KUT, O3:K6), Jiangsu (O3:K6, O4:K48), Zhejiang (O3:K6), and Guangdong (O4:K9). Notably, 24 pandemic serovariants were detected within a short time frame (from 2006 to 2012). The pandemic isolates were divided into 15 sequence types (STs), 10 of which fell within clonal complex (CC) 3. Only three STs (ST3, ST192, and ST305) were identified in environmental isolates. Substantial serotypic diversity was mainly observed among isolates within pandemic ST3, which comprised 21 combinations of O/K antigens. The pandemic O3:K6 serotype showed a high level of sequence diversity, which was shared by eight different STs (ST3, ST227, ST431, ST435, ST487, ST489, ST526, and ST672). Antimicrobial susceptibility testing revealed that most isolates shared similar antibiotic susceptibility profiles. They were resistant to ampicillin but sensitive to most other drugs that were tested. In conclusion, the high levels of serotypic and genetic diversity of the pandemic clone suggest that the involved regions are becoming important reservoirs for the emergence of novel pandemic strains. We underscore the need for routine monitoring to prevent pandemic V. parahaemolyticus infection, which includes monitoring antimicrobial responses to avoid excessive misuse of antibiotics. Further investigations are also needed to delineate the specific mechanisms underlying the possible seroconversion of pandemic isolates.

Project description:A specific serotype, O3:K6, of Vibrio parahaemolyticus has recently been causing epidemics of gastroenteritis in Southeast Asia, Japan, and North America. To examine whether the new O3:K6 strains possess characteristics that may exacerbate outbreaks, we compared V. parahaemolyticus O3:K6 strains with non-O3:K6 strains using strains isolated from individuals with traveler's diarrhea at Kansai Airport Quarantine Station, Osaka, Japan. All 24 O3:K6 strains possessed a common plasmid, pO3K6 (DNA size, 8,782 bp, with 10 open reading frames [ORFs]). The gene organization of pO3K6 was similar to that of Vf33, a filamentous phage previously described in V. parahaemolyticus. We isolated a phage (phage f237) from the culture supernatant of V. parahaemolyticus O3:K6 strain KXV237, which formed a turbid plaque on an indicator strain. The genome of f237 was single-stranded DNA, and the double-stranded DNA obtained by treatment of the genome with DNA polymerase was identical to that of pO3K6 when analyzed by agarose gel electrophoresis after HindIII digestion. Furthermore, the N-terminal amino acid sequence of the f237 major coat protein was found in ORF4 of pO3K6. Our results showed that pO3K6 is a replicative form of f237. Among the ORFs found in the f237 genome, the sequence of ORF8 had no significant homology to those of any proteins in databases. ORF8 was located on a region corresponding to the distinctive region of Vf33, and its G+C content was apparently lower than that of the remaining DNA sequence of f237. By colony hybridization, ORF8 was detected only in O3:K6 strains isolated since 1996 and was not found in O3:K6 strains isolated before 1996 and clinical V. parahaemolyticus strains other than those of serotype O3:K6. Thus, this study shows that f237 is exclusively associated with recent V. parahaemolyticus O3:K6 strains. The ORF8 gene can be a useful genetic marker for the identification of the recently widespread O3:K6 strains of V. parahaemolyticus.

Dataset Information

Molecular analysis of the emergence of pandemic Vibrio parahaemolyticus.

Publications

Molecular analysis of the emergence of pandemic Vibrio parahaemolyticus.

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