Dataset Information

Genome plasticity of Vibrio parahaemolyticus: microevolution of the 'pandemic group'.

ABSTRACT:

Background

Outbreak of V. parahaemolyticus infections occurred since 1996 was linked to a proposed clonal complex, the pandemic group. The whole genome sequence provides an unprecedented opportunity for dissecting genome plasticity and phylogeny of the populations of V. parahaemolyticus. In the present work, a whole-genome cDNA microarray was constructed to compare the genomic contents of a collection of 174 strains of V. parahaemolyticus.

Results

Genes that present variably in the genome accounted for about 22% of the whole gene pool on the genome. The phylogenetic analysis of microarray data generated a minimum spanning tree that depicted the phylogenetic structure of the 174 strains. Strains were assigned into five complexes (C1 to C5), and those in each complex were related genetically and phylogenetically. C3 and C4 represented highly virulent clinical clones. C2 and C3 constituted two different clonal complexes 'old-O3:K6 clone' and 'pandemic clone', respectively. C3 included all the 39 pandemic strains tested (trh-, tdh+ and GS-PCR+), while C2 contained 12 pre-1996 'old' O3:K6 strains (trh+, tdh- and GS-PCR-) tested herein. The pandemic clone (post-1996 'new' O3:K6 and its derivates O4:K68, O1:K25, O1:KUT and O6:K18) might be emerged from the old-O3:K6 clone, which was promoted by acquisition of toxRS/new sequence and genomic islands. A phylogenetic intermediate O3:K6 clade (trh-, tdh- and GS-PCR+) was identified between the pandemic and old-O3:K6 clones.

Conclusion

A comprehensive overview of genomic contents in a large collection of global isolates from the microarray-based comparative genomic hybridization data enabled us to construct a phylogenetic structure of V. parahaemolyticus and an evolutionary history of the pandemic group (clone) of this pathogen.

SUBMITTER: Han H

PROVIDER: S-EPMC2612023 | biostudies-literature | 2008 Nov

REPOSITORIES: biostudies-literature

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Publications

Genome plasticity of Vibrio parahaemolyticus: microevolution of the 'pandemic group'.

Han Haihong H Wong Hin-Chung HC Kan Biao B Guo Zhaobiao Z Zeng Xiaotao X Yin Shengjun S Liu Xiumei X Yang Ruifu R Zhou Dongsheng D

BMC genomics 20081128

<h4>Background</h4>Outbreak of V. parahaemolyticus infections occurred since 1996 was linked to a proposed clonal complex, the pandemic group. The whole genome sequence provides an unprecedented opportunity for dissecting genome plasticity and phylogeny of the populations of V. parahaemolyticus. In the present work, a whole-genome cDNA microarray was constructed to compare the genomic contents of a collection of 174 strains of V. parahaemolyticus.<h4>Results</h4>Genes that present variably in th ...[more]

PMID: 19038058

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Project description:Vibrio parahaemolyticus is becoming the leading cause of acute bacterial gastroenteritis, but its population dynamics in aquafarms have received limited attention. To address this research gap, we selected three shellfish farms to examine the impacts of ocean currents and the transport of live aquatic animals on the transmission and microevolution of V. parahaemolyticus by using multilocus sequence typing (MLST) and whole-genome sequencing. MLST and genomic analysis revealed that the community structure of V. parahaemolyticus in Dalian and Donggang was relatively stable in the presence of ocean currents; however, horizontal gene transfer of mobile genetic elements (MGEs) between Dalian and Donggang was very common. Further analysis indicated that the transport of live aquatic animals from Dalian to Xiamen not only introduced new V. parahaemolyticus populations but also allowed the exchange of genetic material between the two sites. More interestingly, Dalian-originated strain ST722 was introduced to Xiamen farms, resulting in one MLST allele change and the acquisition of two genomic islands from indigenous isolates in Xiamen within 8 months; such alterations are thought to promote the adaptation of V. parahaemolyticus These results provide direct observations of how ocean currents and the transport of live aquatic animals contribute to the dissemination and genetic mixture of V. parahaemolyticus, which provides insights into the dynamics and microevolution of V. parahaemolyticus in aquacultural environments.IMPORTANCE Globally, V. parahaemolyticus-related gastroenteritis outbreaks caused by seafood consumption represent an increasing threat to human health. Despite advances in our understanding of the global epidemiology of pandemic V. parahaemolyticus, fundamental questions about the key driving forces for the spread of V. parahaemolyticus at regional and national scales remain unanswered. This study revealed that the transregional transport of aquatic animals and the movement of ocean currents both contributed to the mixing of V. parahaemolyticus populations. More importantly, this study demonstrated how genetic mixture occurred between introduced and endemic V. parahaemolyticus populations via the transport of aquatic animals, which accelerated bacterial adaptation by transferring ecologically important functions. These results suggest that human activities entail a risk of the emergence of new virulent populations for both aquatic animals and humans by horizontal gene transfer and provide important insights into the microevolution and population mixing of V. parahaemolyticus.

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.

Dataset Information

Genome plasticity of Vibrio parahaemolyticus: microevolution of the 'pandemic group'.

Background

Results

Conclusion

Publications

Genome plasticity of Vibrio parahaemolyticus: microevolution of the 'pandemic group'.

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