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      Genomic variation among closely related Vibrio alginolyticus strains is located on mobile genetic elements

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          Abstract

          Background

          Species of the genus Vibrio, one of the most diverse bacteria genera, have undergone niche adaptation followed by clonal expansion. Niche adaptation and ultimately the formation of ecotypes and speciation in this genus has been suggested to be mainly driven by horizontal gene transfer (HGT) through mobile genetic elements (MGEs). Our knowledge about the diversity and distribution of Vibrio MGEs is heavily biased towards human pathogens and our understanding of the distribution of core genomic signatures and accessory genes encoded on MGEs within specific Vibrio clades is still incomplete. We used nine different strains of the marine bacterium Vibrio alginolyticus isolated from pipefish in the Kiel-Fjord to perform a multiscale-comparative genomic approach that allowed us to investigate [1] those genomic signatures that characterize a habitat-specific ecotype and [2] the source of genomic variation within this ecotype.

          Results

          We found that the nine isolates from the Kiel-Fjord have a closed-pangenome and did not differ based on core-genomic signatures. Unique genomic regions and a unique repertoire of MGEs within the Kiel-Fjord isolates suggest that the acquisition of gene-blocks by HGT played an important role in the evolution of this ecotype. Additionally, we found that ~ 90% of the genomic variation among the nine isolates is encoded on MGEs, which supports ongoing theory that accessory genes are predominately located on MGEs and shared by HGT. Lastly, we could show that these nine isolates share a unique virulence and resistance profile which clearly separates them from all other investigated V. alginolyticus strains and suggests that these are habitat-specific genes, required for a successful colonization of the pipefish, the niche of this ecotype.

          Conclusion

          We conclude that all nine V. alginolyticus strains from the Kiel-Fjord belong to a unique ecotype, which we named the Kiel- alginolyticus ecotype. The low sequence variation of the core-genome in combination with the presence of MGE encoded relevant traits, as well as the presence of a suitable niche (here the pipefish), suggest, that this ecotype might have evolved from a clonal expansion following HGT driven niche-adaptation.

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          Most cited references24

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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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            • Record: found
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            Comparative genomics: the bacterial pan-genome.

            Bacterial genome sequencing has become so easy and accessible that the genomes of multiple strains of more and more individual species have been and will be generated. These data sets provide for in depth analysis of intra-species diversity from various aspects. The pan-genome analysis, whereby the size of the gene repertoire accessible to any given species is characterized together with an estimate of the number of whole genome sequences required for proper analysis, is being increasingly applied. Different models exist for the analysis and their accuracy and applicability depend on the case at hand. Here we discuss current models and suggest a new model of broad applicability, including examples of its implementation.
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              • Record: found
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              The Ecology and Evolution of Pangenomes

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                Author and article information

                Contributors
                carolin.wendling@env.ethz.ch
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                11 May 2020
                11 May 2020
                2020
                : 21
                : 354
                Affiliations
                [1 ]GRID grid.7450.6, ISNI 0000 0001 2364 4210, Department of Genomic and Applied Microbiology, , Institute of Microbiology and Genetics, Georg-August-University, ; 37077 Göttingen, Germany
                [2 ]GRID grid.7450.6, ISNI 0000 0001 2364 4210, Institute for Microbiology and Genetics, Georg-August University Goettingen, ; Grisebachstr. 8, 37077 Goettingen, Germany
                [3 ]GRID grid.15649.3f, ISNI 0000 0000 9056 9663, GEOMAR, Helmholtz Centre for Ocean Research, Marine Evolutionary Ecology, ; Duesternbrooker Weg 20, 24105 Kiel, Germany
                [4 ]GRID grid.5801.c, ISNI 0000 0001 2156 2780, Department of Environmental Systems Science, , ETH Zürich, ; Universitätsstraße 16, 8092 Zürich, Switzerland
                Author information
                http://orcid.org/0000-0003-4532-7528
                Article
                6735
                10.1186/s12864-020-6735-5
                7216594
                32393168
                09d53bcb-bafd-4fa0-9c05-35d3c68634bc
                © The Author(s). 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 10 February 2020
                : 14 April 2020
                Funding
                Funded by: Deutsche Forschungsgemeinschaft
                Award ID: WE 5822/ 1-1
                Award ID: WE5822/1-2
                Award ID: RO462/4-2
                Award Recipient :
                Funded by: KAAD
                Award ID: na
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2020

                Genetics
                pangenome,mega-plasmids,mobile genetic elements,horizontal gene transfer,genomic islands,niche-adaptation

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