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      Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny

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          Abstract

          Scleractinian corals’ microbial symbionts influence host health, yet how coral microbiomes assembled over evolution is not well understood. We survey bacterial and archaeal communities in phylogenetically diverse Australian corals representing more than 425 million years of diversification. We show that coral microbiomes are anatomically compartmentalized in both modern microbial ecology and evolutionary assembly. Coral mucus, tissue, and skeleton microbiomes differ in microbial community composition, richness, and response to host vs. environmental drivers. We also find evidence of coral-microbe phylosymbiosis, in which coral microbiome composition and richness reflect coral phylogeny. Surprisingly, the coral skeleton represents the most biodiverse coral microbiome, and also shows the strongest evidence of phylosymbiosis. Interactions between bacterial and coral phylogeny significantly influence the abundance of four groups of bacteria–including Endozoicomonas-like bacteria, which divide into host-generalist and host-specific subclades. Together these results trace microbial symbiosis across anatomy during the evolution of a basal animal lineage.

          Abstract

          Associations between corals and symbiotic microorganisms could be driven by the environment or shared evolutionary history. Here, the authors examine relationships between coral phylogenies and associated microbiomes, finding evidence of phylosymbiosis in microbes from coral skeleton and tissue, but not mucus.

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          Most cited references28

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          The Coevolutionary Process

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            Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences

            We present a performance-optimized algorithm, subsampled open-reference OTU picking, for assigning marker gene (e.g., 16S rRNA) sequences generated on next-generation sequencing platforms to operational taxonomic units (OTUs) for microbial community analysis. This algorithm provides benefits over de novo OTU picking (clustering can be performed largely in parallel, reducing runtime) and closed-reference OTU picking (all reads are clustered, not only those that match a reference database sequence with high similarity). Because more of our algorithm can be run in parallel relative to “classic” open-reference OTU picking, it makes open-reference OTU picking tractable on massive amplicon sequence data sets (though on smaller data sets, “classic” open-reference OTU clustering is often faster). We illustrate that here by applying it to the first 15,000 samples sequenced for the Earth Microbiome Project (1.3 billion V4 16S rRNA amplicons). To the best of our knowledge, this is the largest OTU picking run ever performed, and we estimate that our new algorithm runs in less than 1/5 the time than would be required of “classic” open reference OTU picking. We show that subsampled open-reference OTU picking yields results that are highly correlated with those generated by “classic” open-reference OTU picking through comparisons on three well-studied datasets. An implementation of this algorithm is provided in the popular QIIME software package, which uses uclust for read clustering. All analyses were performed using QIIME’s uclust wrappers, though we provide details (aided by the open-source code in our GitHub repository) that will allow implementation of subsampled open-reference OTU picking independently of QIIME (e.g., in a compiled programming language, where runtimes should be further reduced). Our analyses should generalize to other implementations of these OTU picking algorithms. Finally, we present a comparison of parameter settings in QIIME’s OTU picking workflows and make recommendations on settings for these free parameters to optimize runtime without reducing the quality of the results. These optimized parameters can vastly decrease the runtime of uclust-based OTU picking in QIIME.
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              Diversity, structure and convergent evolution of the global sponge microbiome

              Sponges (phylum Porifera) are early-diverging metazoa renowned for establishing complex microbial symbioses. Here we present a global Porifera microbiome survey, set out to establish the ecological and evolutionary drivers of these host–microbe interactions. We show that sponges are a reservoir of exceptional microbial diversity and major contributors to the total microbial diversity of the world's oceans. Little commonality in species composition or structure is evident across the phylum, although symbiont communities are characterized by specialists and generalists rather than opportunists. Core sponge microbiomes are stable and characterized by generalist symbionts exhibiting amensal and/or commensal interactions. Symbionts that are phylogenetically unique to sponges do not disproportionally contribute to the core microbiome, and host phylogeny impacts complexity rather than composition of the symbiont community. Our findings support a model of independent assembly and evolution in symbiont communities across the entire host phylum, with convergent forces resulting in analogous community organization and interactions.
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                Author and article information

                Contributors
                zaneveld@gmail.com
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                22 November 2018
                22 November 2018
                2018
                : 9
                : 4921
                Affiliations
                [1 ]ISNI 0000 0001 2097 4281, GRID grid.29857.31, Department of Biology, , Pennsylvania State University, ; 208 Mueller Lab, University Park, State College, PA 16802 USA
                [2 ]ISNI 0000 0001 2112 1969, GRID grid.4391.f, Department of Microbiology, , Oregon State University, ; 226 Nash Hall, Corvallis, OR 97331 USA
                [3 ]ISNI 0000 0004 0474 1797, GRID grid.1011.1, College of Science and Engineering, , James Cook University, ; Townsville, QLD 4811 Australia
                [4 ]ISNI 0000 0001 0328 1619, GRID grid.1046.3, Australian Institute of Marine Science, ; Townsville, QLD 4810 Australia
                [5 ]ISNI 0000 0004 0474 1797, GRID grid.1011.1, ARC Centre of Excellence for Coral Reef Studies, , James Cook University, ; Townsville, QLD 4811 Australia
                [6 ]GRID grid.430355.4, Smithsonian Tropical Research Institute, Smithsonian Institution, ; 9100 Panama City PL, Washington, DC 20521 USA
                [7 ]ISNI 0000000122986657, GRID grid.34477.33, Division of Biological Sciences, Bothell, School of Science, Technology, Engineering, and Mathematics, , University of Washington, ; UWBB-277, Bothell, WA 98011 USA
                Author information
                http://orcid.org/0000-0001-6333-6845
                http://orcid.org/0000-0001-8367-0293
                Article
                7275
                10.1038/s41467-018-07275-x
                6250698
                30467310
                3827bdd0-1d66-4d44-8672-1eb02d4f0f4e
                © The Author(s) 2018

                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
                : 10 December 2017
                : 19 October 2018
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