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      Comparative Genome Analyses of Vibrio anguillarum Strains Reveal a Link with Pathogenicity Traits

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          Abstract

          Comparative genome analysis of strains of a pathogenic bacterial species can be a powerful tool to discover acquisition of mobile genetic elements related to virulence. Here, we compared 28 V. anguillarum strains that differed in virulence in fish larval models. By pan-genome analyses, we found that six of nine highly virulent strains had a unique core and accessory genome. In contrast, V. anguillarum strains that were medium to nonvirulent had low genomic diversity. Integration of genomic and phenotypic features provides insights into the evolution of V. anguillarum and can also be important for survey and diagnostic purposes.

          ABSTRACT

          Vibrio anguillarum is a marine bacterium that can cause vibriosis in many fish and shellfish species, leading to high mortalities and economic losses in aquaculture. Although putative virulence factors have been identified, the mechanism of pathogenesis of V. anguillarum is not fully understood. Here, we analyzed whole-genome sequences of a collection of V. anguillarum strains and compared them to virulence of the strains as determined in larval challenge assays. Previously identified virulence factors were globally distributed among the strains, with some genetic diversity. However, the pan-genome revealed that six out of nine high-virulence strains possessed a unique accessory genome that was attributed to pathogenic genomic islands, prophage-like elements, virulence factors, and a new set of gene clusters involved in biosynthesis, modification, and transport of polysaccharides. In contrast, V. anguillarum strains that were medium to nonvirulent had a high degree of genomic homogeneity. Finally, we found that a phylogeny based on the core genomes clustered the strains with moderate to no virulence, while six out of nine high-virulence strains represented phylogenetically separate clusters. Hence, we suggest a link between genotype and virulence characteristics of Vibrio anguillarum, which can be used to unravel the molecular evolution of V. anguillarum and can also be important from survey and diagnostic perspectives.

          IMPORTANCE Comparative genome analysis of strains of a pathogenic bacterial species can be a powerful tool to discover acquisition of mobile genetic elements related to virulence. Here, we compared 28 V. anguillarum strains that differed in virulence in fish larval models. By pan-genome analyses, we found that six of nine highly virulent strains had a unique core and accessory genome. In contrast, V. anguillarum strains that were medium to nonvirulent had low genomic diversity. Integration of genomic and phenotypic features provides insights into the evolution of V. anguillarum and can also be important for survey and diagnostic purposes.

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          Most cited references65

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          The microbial pan-genome.

          A decade after the beginning of the genomic era, the question of how genomics can describe a bacterial species has not been fully addressed. Experimental data have shown that in some species new genes are discovered even after sequencing the genomes of several strains. Mathematical modeling predicts that new genes will be discovered even after sequencing hundreds of genomes per species. Therefore, a bacterial species can be described by its pan-genome, which is composed of a "core genome" containing genes present in all strains, and a "dispensable genome" containing genes present in two or more strains and genes unique to single strains. Given that the number of unique genes is vast, the pan-genome of a bacterial species might be orders of magnitude larger than any single genome.
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            Genomic islands in pathogenic and environmental microorganisms.

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              Estimating maximum likelihood phylogenies with PhyML.

              Our understanding of the origins, the functions and/or the structures of biological sequences strongly depends on our ability to decipher the mechanisms of molecular evolution. These complex processes can be described through the comparison of homologous sequences in a phylogenetic framework. Moreover, phylogenetic inference provides sound statistical tools to exhibit the main features of molecular evolution from the analysis of actual sequences. This chapter focuses on phylogenetic tree estimation under the maximum likelihood (ML) principle. Phylogenies inferred under this probabilistic criterion are usually reliable and important biological hypotheses can be tested through the comparison of different models. Estimating ML phylogenies is computationally demanding, and careful examination of the results is warranted. This chapter focuses on PhyML, a software that implements recent ML phylogenetic methods and algorithms. We illustrate the strengths and pitfalls of this program through the analysis of a real data set. PhyML v3.0 is available from (http://atgc_montpellier.fr/phyml/).
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                Author and article information

                Contributors
                Role: Editor
                Journal
                mSystems
                mSystems
                msys
                msys
                mSystems
                mSystems
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2379-5077
                28 February 2017
                Jan-Feb 2017
                : 2
                : 1
                : e00001-17
                Affiliations
                [a ]Marine Biological Section, University of Copenhagen, Helsingør, Denmark
                [b ]Department of Biotechnology and Biomedicine, Technical University of Denmark, Kgs Lyngby, Denmark
                [c ]Copenhagen Bio Science Park, Denmark
                [d ]BGI Park, Yantian District, Shenzhen, China
                Dartmouth College
                Author notes
                Address correspondence to Lone Gram, gram@ 123456bio.dtu.dk .

                Citation Castillo D, Alvise PD, Xu R, Zhang F, Middelboe M, Gram L. 2017. Comparative genome analyses of Vibrio anguillarum strains reveal a link with pathogenicity traits. mSystems 2:e00001-17. https://doi.org/10.1128/mSystems.00001-17.

                Article
                mSystems00001-17
                10.1128/mSystems.00001-17
                5347184
                28293680
                a27f11df-3901-4a3a-af9d-c97409e81456
                Copyright © 2017 Castillo et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 5 January 2017
                : 30 January 2017
                Page count
                supplementary-material: 10, Figures: 5, Tables: 1, Equations: 0, References: 93, Pages: 14, Words: 9691
                Funding
                Funded by: Innovation Fund Denmark
                Award ID: 0603-00515B
                Award Recipient : Daniel Castillo Award Recipient : Paul D. Alvise Award Recipient : Ruiqi Xu Award Recipient : Faxing Zhang Award Recipient : Mathias Middelboe Award Recipient : Lone Gram
                Categories
                Research Article
                Ecological and Evolutionary Science
                Editor's Pick
                Custom metadata
                January/February 2017

                pan-genome,genomics,virulence factors
                pan-genome, genomics, virulence factors

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