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      Horizontally transmitted symbiont populations in deep-sea mussels are genetically isolated

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          Abstract

          Eukaryotes are habitats for bacterial organisms where the host colonization and dispersal among individual hosts have consequences for the bacterial ecology and evolution. Vertical symbiont transmission leads to geographic isolation of the microbial population and consequently to genetic isolation of microbiotas from individual hosts. In contrast, the extent of geographic and genetic isolation of horizontally transmitted microbiota is poorly characterized. Here we show that chemosynthetic symbionts of individual Bathymodiolus brooksi mussels constitute genetically isolated subpopulations. The reconstruction of core genome-wide strains from high-resolution metagenomes revealed distinct phylogenetic clades. Nucleotide diversity and strain composition vary along the mussel life span and individual hosts show a high degree of genetic isolation. Our results suggest that the uptake of environmental bacteria is a restricted process in B. brooksi, where self-infection of the gill tissue results in serial founder effects during symbiont evolution. We conclude that bacterial colonization dynamics over the host life cycle is thus an important determinant of population structure and genome evolution of horizontally transmitted symbionts.

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          Most cited references34

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          Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors.

          In vertebrates, including humans, individuals harbor gut microbial communities whose species composition and relative proportions of dominant microbial groups are tremendously varied. Although external and stochastic factors clearly contribute to the individuality of the microbiota, the fundamental principles dictating how environmental factors and host genetic factors combine to shape this complex ecosystem are largely unknown and require systematic study. Here we examined factors that affect microbiota composition in a large (n = 645) mouse advanced intercross line originating from a cross between C57BL/6J and an ICR-derived outbred line (HR). Quantitative pyrosequencing of the microbiota defined a core measurable microbiota (CMM) of 64 conserved taxonomic groups that varied quantitatively across most animals in the population. Although some of this variation can be explained by litter and cohort effects, individual host genotype had a measurable contribution. Testing of the CMM abundances for cosegregation with 530 fully informative SNP markers identified 18 host quantitative trait loci (QTL) that show significant or suggestive genome-wide linkage with relative abundances of specific microbial taxa. These QTL affect microbiota composition in three ways; some loci control individual microbial species, some control groups of related taxa, and some have putative pleiotropic effects on groups of distantly related organisms. These data provide clear evidence for the importance of host genetic control in shaping individual microbiome diversity in mammals, a key step toward understanding the factors that govern the assemblages of gut microbiota associated with complex diseases.
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            SplitsTree: analyzing and visualizing evolutionary data.

            D Huson (1998)
            Real evolutionary data often contain a number of different and sometimes conflicting phylogenetic signals, and thus do not always clearly support a unique tree. To address this problem, Bandelt and Dress (Adv. Math., 92, 47-05, 1992) developed the method of split decomposition. For ideal data, this method gives rise to a tree, whereas less ideal data are represented by a tree-like network that may indicate evidence for different and conflicting phylogenies. SplitsTree is an interactive program, for analyzing and visualizing evolutionary data, that implements this approach. It also supports a number of distances transformations, the computation of parsimony splits, spectral analysis and bootstrapping.
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              Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus.

              Extensive genomic diversity within coexisting members of a microbial species has been revealed through selected cultured isolates and metagenomic assemblies. Yet, the cell-by-cell genomic composition of wild uncultured populations of co-occurring cells is largely unknown. In this work, we applied large-scale single-cell genomics to study populations of the globally abundant marine cyanobacterium Prochlorococcus. We show that they are composed of hundreds of subpopulations with distinct "genomic backbones," each backbone consisting of a different set of core gene alleles linked to a small distinctive set of flexible genes. These subpopulations are estimated to have diverged at least a few million years ago, suggesting ancient, stable niche partitioning. Such a large set of coexisting subpopulations may be a general feature of free-living bacterial species with huge populations in highly mixed habitats.
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                Author and article information

                Contributors
                dpicazo@ifam.uni-kiel.de
                akupczok@ifam.uni-kiel.de
                Journal
                ISME J
                ISME J
                The ISME Journal
                Nature Publishing Group UK (London )
                1751-7362
                1751-7370
                8 August 2019
                8 August 2019
                December 2019
                : 13
                : 12
                : 2954-2968
                Affiliations
                [1 ]ISNI 0000 0001 2153 9986, GRID grid.9764.c, Genomic Microbiology Group, Institute of General Microbiology, , Christian-Albrechts University, ; Kiel, Germany
                [2 ]ISNI 0000 0004 0491 3210, GRID grid.419529.2, Max Planck Institute for Marine Microbiology, ; Bremen, Germany
                [3 ]ISNI 0000 0001 2286 1424, GRID grid.10420.37, Division of Microbiology and Ecosystem Science, , University of Vienna, ; Wien, Austria
                Author information
                http://orcid.org/0000-0002-9042-192X
                http://orcid.org/0000-0002-9394-825X
                Article
                475
                10.1038/s41396-019-0475-z
                6863903
                31395952
                1abcd594-83db-4368-b136-f52d884788a3
                © The Author(s) 2019

                Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 20 February 2019
                : 22 May 2019
                : 16 June 2019
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft (German Research Foundation);
                Award ID: CRC1182
                Award ID: CRC1182
                Award ID: CRC1182
                Award ID: CRC1182
                Award Recipient :
                Categories
                Article
                Custom metadata
                © The Author(s), under exclusive licence to International Society for Microbial Ecology 2019

                Microbiology & Virology
                population genetics,phylogenetics,microbial ecology,symbiosis,metagenomics
                Microbiology & Virology
                population genetics, phylogenetics, microbial ecology, symbiosis, metagenomics

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