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      Host genetics and geography influence microbiome composition in the sponge Ircinia campana

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          Abstract

          1. Marine sponges are hosts to large, diverse communities of microorganisms. These microbiomes are distinct among sponge species and from seawater bacterial communities, indicating a key role of host identity in shaping its resident microbial community. However, the factors governing intraspecific microbiome variability are underexplored and may shed light on the evolutionary and ecological relationships between host and microbiome.

          2. Here, we examined the influence of genetic variation and geographic location on the composition of the Ircinia campana microbiome.

          3. We developed new microsatellite markers to genotype I. campana from two locations in the Florida Keys, USA, and characterized their microbiomes using V4 16S rRNA amplicon sequencing.

          4. We show that microbial community composition and diversity is influenced by host genotype, with more genetically similar sponges hosting more similar microbial communities. We also found that although I. campana was not genetically differentiated between sites, microbiome composition differed by location.

          5. Our results demonstrate that both host genetics and geography influence the composition of the sponge microbiome. Host genotypic influence on microbiome composition may be due to stable vertical transmission of the microbial community from parent to offspring, making microbiomes more similar by descent. Alternatively, sponge genotypic variation may reflect variation in functional traits that influence the acquisition of environmental microbes. This study reveals drivers of microbiome variation within and among locations, and shows the importance of intraspecific variability in mediating eco‐evolutionary dynamics of host‐associated microbiomes.

          Abstract

          For the first time, the authors show that intraspecific genetic variation affects microbiome composition in a marine sponge ( Ircinia campana), with positive correlations observed between genetic and microbiome similarity. This has significant implications for our understanding of the ecological and evolutionary relationships between host and microbiome in this important model system.

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          Most cited references66

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          Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.

          The ongoing revolution in high-throughput sequencing continues to democratize the ability of small groups of investigators to map the microbial component of the biosphere. In particular, the coevolution of new sequencing platforms and new software tools allows data acquisition and analysis on an unprecedented scale. Here we report the next stage in this coevolutionary arms race, using the Illumina GAIIx platform to sequence a diverse array of 25 environmental samples and three known "mock communities" at a depth averaging 3.1 million reads per sample. We demonstrate excellent consistency in taxonomic recovery and recapture diversity patterns that were previously reported on the basis of metaanalysis of many studies from the literature (notably, the saline/nonsaline split in environmental samples and the split between host-associated and free-living communities). We also demonstrate that 2,000 Illumina single-end reads are sufficient to recapture the same relationships among samples that we observe with the full dataset. The results thus open up the possibility of conducting large-scale studies analyzing thousands of samples simultaneously to survey microbial communities at an unprecedented spatial and temporal resolution.
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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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              Beyond the Venn diagram: the hunt for a core microbiome.

              Discovering a core microbiome is important for understanding the stable, consistent components across complex microbial assemblages. A core is typically defined as the suite of members shared among microbial consortia from similar habitats, and is represented by the overlapping areas of circles in Venn diagrams, in which each circle contains the membership of the sample or habitats being compared. Ecological insight into core microbiomes can be enriched by 'omics approaches that assess gene expression, thereby extending the concept of the core beyond taxonomically defined membership to community function and behaviour. Parameters defined by traditional ecology theory, such as composition, phylogeny, persistence and connectivity, will also create a more complex portrait of the core microbiome and advance understanding of the role of key microorganisms and functions within and across ecosystems. © 2011 Society for Applied Microbiology and Blackwell Publishing Ltd.
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                Author and article information

                Contributors
                griffiths.sarahm@gmail.com
                Journal
                J Anim Ecol
                J Anim Ecol
                10.1111/(ISSN)1365-2656
                JANE
                The Journal of Animal Ecology
                John Wiley and Sons Inc. (Hoboken )
                0021-8790
                1365-2656
                03 September 2019
                November 2019
                : 88
                : 11 ( doiID: 10.1111/jane.v88.11 )
                : 1684-1695
                Affiliations
                [ 1 ] Ecology and Environment Research Centre Manchester Metropolitan University Manchester UK
                [ 2 ] School of Environment and Life Sciences University of Salford Salford UK
                [ 3 ] Centre for Genomic Research, Institute of Integrative Biology University of Liverpool Liverpool UK
                [ 4 ] Fisheries and Aquatic Sciences University of Florida Gainesville FL USA
                [ 5 ] Emerging Pathogens Institute University of Florida Gainesville FL USA
                [ 6 ] Department of Biological Sciences Old Dominion University Norfolk VA USA
                Author notes
                [*] [* ] Correspondence

                Sarah M. Griffiths

                Email: griffiths.sarahm@ 123456gmail.com

                Author information
                https://orcid.org/0000-0003-4743-049X
                https://orcid.org/0000-0002-8849-8194
                Article
                JANE13065
                10.1111/1365-2656.13065
                6899969
                31325164
                ed10764d-161b-4d15-b544-b9c87a60b1d6
                © 2019 The Authors. Journal of Animal Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 25 March 2019
                : 09 July 2019
                Page count
                Figures: 3, Tables: 1, Pages: 12, Words: 9464
                Funding
                Funded by: Natural Environment Research Council , open-funder-registry 10.13039/501100000270;
                Funded by: NERC Biomolecular Analysis Facility
                Categories
                Research Article
                Molecular Ecology
                Custom metadata
                2.0
                November 2019
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.2 mode:remove_FC converted:05.12.2019

                Ecology
                bacteria,core microbiome,eco‐evolutionary dynamics,genetic diversity,host–microbe interactions,microsatellites,porifera

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