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      Diversity, structure and convergent evolution of the global sponge microbiome

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          Abstract

          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.

          Abstract

          Sponges are early-diverging marine organisms that establish complex symbioses with microorganisms. Here, Thomas et al. analyse the microbial communities associated with 81 species of sponges from around the world, shedding light on the ecological and evolutionary drivers of these host-microbe associations.

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          Most cited references26

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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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            The architecture of mutualistic networks minimizes competition and increases biodiversity.

            The main theories of biodiversity either neglect species interactions or assume that species interact randomly with each other. However, recent empirical work has revealed that ecological networks are highly structured, and the lack of a theory that takes into account the structure of interactions precludes further assessment of the implications of such network patterns for biodiversity. Here we use a combination of analytical and empirical approaches to quantify the influence of network architecture on the number of coexisting species. As a case study we consider mutualistic networks between plants and their animal pollinators or seed dispersers. These networks have been found to be highly nested, with the more specialist species interacting only with proper subsets of the species that interact with the more generalist. We show that nestedness reduces effective interspecific competition and enhances the number of coexisting species. Furthermore, we show that a nested network will naturally emerge if new species are more likely to enter the community where they have minimal competitive load. Nested networks seem to occur in many biological and social contexts, suggesting that our results are relevant in a wide range of fields.
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              Ecological networks and their fragility.

              Darwin used the metaphor of a 'tangled bank' to describe the complex interactions between species. Those interactions are varied: they can be antagonistic ones involving predation, herbivory and parasitism, or mutualistic ones, such as those involving the pollination of flowers by insects. Moreover, the metaphor hints that the interactions may be complex to the point of being impossible to understand. All interactions can be visualized as ecological networks, in which species are linked together, either directly or indirectly through intermediate species. Ecological networks, although complex, have well defined patterns that both illuminate the ecological mechanisms underlying them and promise a better understanding of the relationship between complexity and ecological stability.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                16 June 2016
                2016
                : 7
                : 11870
                Affiliations
                [1 ] School of Biological, Earth and Environmental Sciences, Centre for Marine Bio-Innovation and School of Biotechnology and Biomolecular Sciences, University of New South Wales , Sydney, New South Wales 2052, Australia
                [2 ]The Environment Institute and School of Biological Sciences, University of Adelaide , Adelaide, South Australia 5005, Australia
                [3 ]Ecological Networks and Global Change Group, Experimental and Theoretical Ecology Station, Centre National de la Recherche Scientifique , Moulis 09200, France
                [4 ]Institute of Marine Sciences, CSIC , 08003 Barcelona, Spain
                [5 ]Department of Biology, University of Alabama at Birmingham , Birmingham, Alabama 35487, USA
                [6 ]School of Biological Sciences, University of Auckland , Auckland 1010, New Zealand
                [7 ]Department of Biological Sciences, University of Alabama , Tuscaloosa, Alabama 35487, USA
                [8 ]Department of Biology and Marine Biology, and Center for Marine Science. University of North Carolina Wilmington , 5600 Marvin K. Moss Lane, Wilmington, North Carolina 28409, USA
                [9 ]NAMRA and the Research Institute for the Environment and Livelihoods, Charles Darwin University , Darwin, Northern Territory 0810, Australia
                [10 ]Halmos College of Natural Sciences and Oceanography, Guy Harvey Oceanographic Center, Nova Southeastern University , Dania Beach, Florida 33004, USA
                [11 ]Microbial Ecology and Evolution Research Group, Centre of Marine Sciences, Algarve University , 8005-139 Faro, Portugal
                [12 ]Institute of Chemistry and Biology of the Marine Environment, ICBM, University of Oldenburg , Oldenburg 26111, Germany
                [13 ]Department of Marine Biology, Leon Charney School of Marine Sciences, University of Haifa , Haifa 3498838, Israel
                [14 ]Department of Earth and Environmental Sciences and GeoBio-CenterLMU, Ludwig-Maximilians-Universität , Munich 80539, Germany
                [15 ]Department of Ecology and Evolution, Department of Surgery, University of Chicago , Chicago, Illinois 60637, USA
                [16 ]Argonne National Laboratory , Argonne, Illinois 60439, USA
                [17 ]Departments of Pediatrics and Computer Science and Engineering and Center for Microbiome Innovation, University of California at San Diego, 9500 Gilman Drive , La Jolla, California 92093, USA
                [18 ]Department of Ecology and Evolution, Stony Brook University , Stony Brook, New York 11794, USA
                [19 ]GEOMAR Helmholtz Centre for Ocean Research Kiel , Kiel 24105, Germany
                [20 ]Australian Institute of Marine Science , Townsville, Queensland 4816, Australia
                Author notes
                Author information
                http://orcid.org/0000-0002-5932-4101
                http://orcid.org/0000-0002-0975-9019
                http://orcid.org/0000-0002-9654-0073
                http://orcid.org/0000-0002-4753-5278
                Article
                ncomms11870
                10.1038/ncomms11870
                4912640
                27306690
                c73b8071-1f99-47b7-a4f6-fbc1493df070
                Copyright © 2016, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 01 November 2015
                : 09 May 2016
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