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      Molecular Epidemiology and Genetic Variation of Pathogenic Vibrio parahaemolyticus in Peru

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          Abstract

          Vibrio parahaemolyticus is a foodborne pathogen that has become a public health concern at the global scale. The epidemiological significance of V. parahaemolyticus infections in Latin America received little attention until the winter of 1997 when cases related to the pandemic clone were detected in the region, changing the epidemic dynamics of this pathogen in Peru. With the aim to assess the impact of the arrival of the pandemic clone on local populations of pathogenic V. parahaemolyticus in Peru, we investigated the population genetics and genomic variation in a complete collection of non-pandemic strains recovered from clinical sources in Peru during the pre- and post-emergence periods of the pandemic clone. A total of 56 clinical strains isolated in Peru during the period 1994 to 2007, 13 strains from Chile and 20 strains from Asia were characterized by Multilocus Sequence Typing (MLST) and checked for the presence of Variable Genomic Regions (VGRs). The emergence of O3:K6 cases in Peru implied a drastic disruption of the seasonal dynamics of infections and a shift in the serotype dominance of pathogenic V. parahaemolyticus. After the arrival of the pandemic clone, a great diversity of serovars not previously reported was detected in the country, which supports the introduction of additional populations cohabitating with the pandemic group. Moreover, the presence of genomic regions characteristic of the pandemic clone in other non-pandemic strains may represent early evidence of genetic transfer from the introduced population to the local communities. Finally, the results of this study stress the importance of population admixture, horizontal genetic transfer and homologous recombination as major events shaping the structure and diversity of pathogenic V. parahaemolyticus.

          Author Summary

          Infections caused by Vibrio parahaemolyticus have increased significantly over the last two decades, with cases now regularly reported globally. The emergence of cholera at global scale has brought the attention toward other Vibrio diseases in developing countries. This was the situation in Peru, where the investigation of V. cholerae in hospitals and regional public health laboratories after the dramatic emergence of cholera epidemic in 1991 enabled the identification of other pathogenic Vibrio throughout the whole country. The submission of all these bacteria to the Instituto Nacional de Salud (INS, Lima, Peru) for characterization generated an extraordinary repository of records and isolates which have been decisive for sizing the impact of V. parahaemolyticus infections on the population. The present study addresses, for first time, the impact of the arrival of a non-endemic population of V. parahaemolyticus on the genetic structure and virulence attributes of local populations. The detection of the pandemic clone of V. parahaemolyticus to Peru in 1997 changed not only the epidemic dynamics of this pathogen, but also the population structure and genetic variation of native populations through population admixture, horizontal genetic transfer and homologous recombination between native and introduced populations of pathogenic V. parahaemolyticus.

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          Most cited references33

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          eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data.

          The introduction of multilocus sequence typing (MLST) for the precise characterization of isolates of bacterial pathogens has had a marked impact on both routine epidemiological surveillance and microbial population biology. In both fields, a key prerequisite for exploiting this resource is the ability to discern the relatedness and patterns of evolutionary descent among isolates with similar genotypes. Traditional clustering techniques, such as dendrograms, provide a very poor representation of recent evolutionary events, as they attempt to reconstruct relationships in the absence of a realistic model of the way in which bacterial clones emerge and diversify to form clonal complexes. An increasingly popular approach, called BURST, has been used as an alternative, but present implementations are unable to cope with very large data sets and offer crude graphical outputs. Here we present a new implementation of this algorithm, eBURST, which divides an MLST data set of any size into groups of related isolates and clonal complexes, predicts the founding (ancestral) genotype of each clonal complex, and computes the bootstrap support for the assignment. The most parsimonious patterns of descent of all isolates in each clonal complex from the predicted founder(s) are then displayed. The advantages of eBURST for exploring patterns of evolutionary descent are demonstrated with a number of examples, including the simple Spain(23F)-1 clonal complex of Streptococcus pneumoniae, "population snapshots" of the entire S. pneumoniae and Staphylococcus aureus MLST databases, and the more complicated clonal complexes observed for Campylobacter jejuni and Neisseria meningitidis.
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            Transforming clinical microbiology with bacterial genome sequencing.

            Whole-genome sequencing of bacteria has recently emerged as a cost-effective and convenient approach for addressing many microbiological questions. Here, we review the current status of clinical microbiology and how it has already begun to be transformed by using next-generation sequencing. We focus on three essential tasks: identifying the species of an isolate, testing its properties, such as resistance to antibiotics and virulence, and monitoring the emergence and spread of bacterial pathogens. We predict that the application of next-generation sequencing will soon be sufficiently fast, accurate and cheap to be used in routine clinical microbiology practice, where it could replace many complex current techniques with a single, more efficient workflow.
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              Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V cholerae.

              Vibrio parahaemolyticus, a gram-negative marine bacterium, is a worldwide cause of food-borne gastroenteritis. V parahaemolyticus strains of a few specific serotypes, probably derived from a common clonal ancestor, have lately caused a pandemic of gastroenteritis. The organism is phylogenetically close to V cholerae, the causative agent of cholera. The whole genome sequence of a clinical V parahaemolyticus strain RIMD2210633 was established by shotgun sequencing. The coding sequences were identified by use of Gambler and Glimmer programs. Comparative analysis with the V cholerae genome was undertaken with MUMmer. The genome consisted of two circular chromosomes of 3288558 bp and 1877212 bp; it contained 4832 genes. Comparison of the V parahaemolyticus genome with that of V cholerae showed many rearrangements within and between the two chromosomes. Genes for the type III secretion system (TTSS) were identified in the genome of V parahaemolyticus; V cholerae does not have these genes. The TTSS is a central virulence factor of diarrhoea-causing bacteria such as shigella, salmonella, and enteropathogenic Escherichia coli, which cause gastroenteritis by invading or intimately interacting with intestinal epithelial cells. Our results suggest that V parahaemolyticus and V cholerae use distinct mechanisms to establish infection. This finding explains clinical features of V parahaemolyticus infections, which commonly include inflammatory diarrhoea and in some cases systemic manifestations such as septicaemia, distinct from those of V cholerae infections, which are generally associated with non-inflammatory diarrhoea.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                May 2013
                16 May 2013
                : 7
                : 5
                : e2210
                Affiliations
                [1 ]Instituto de Acuicultura, Universidad de Santiago de Compostela, Campus Universitario Sur, Santiago de Compostela, Spain
                [2 ]Instituto Nacional de Salud, Jesus Maria, Lima, Peru
                Universidad Peruana Cayetano Heredia, Peru
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: RGG JMU. Performed the experiments: RGG. Analyzed the data: RGG MLZ JMU. Contributed reagents/materials/analysis tools: MLZ JMU. Wrote the paper: RGG JMU.

                [¤a]

                Current address: Institute for Scientific Research and Technology Services (INDICASAT), Clayton, City of Knowledge, Republic of Panama.

                [¤b]

                Current address: European Centre for Disease Prevention and Control (ECDC), Stockholm, Sweden.

                Article
                PNTD-D-12-01434
                10.1371/journal.pntd.0002210
                3656152
                23696906
                9201095c-b01c-43b4-a53e-7fdd283e9ddd
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 6 November 2012
                : 29 March 2013
                Page count
                Pages: 11
                Funding
                This work was partially supported by project 2007/CP381 from the Department for International Cooperation of the Regional Government of Galicia, Spain. This project finished in 2008. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Microbiology
                Microbial Evolution
                Microbial Pathogens
                Medicine
                Epidemiology
                Infectious Disease Epidemiology
                Molecular Epidemiology

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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