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      Expressed protein profile of a Tectomicrobium and other microbial symbionts in the marine sponge Aplysina aerophoba as evidenced by metaproteomics

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          Abstract

          Aplysina aerophoba is an emerging model marine sponge, with a well-characterized microbial community in terms of diversity and structure. However, little is known about the expressed functional capabilities of its associated microbes. Here, we present the first metaproteomics-based study of the microbiome of A. aerophoba. We found that transport and degradation of halogenated and chloroaromatic compounds are common active processes in the sponge microbiomes. Our data further reveal that the highest number of proteins were affiliated to a sponge-associated Tectomicrobium, presumably from the family Entotheonellaceae, as well as to the well-known symbiont “ Candidatus Synechococcus spongiarium”, suggesting a high metabolic activity of these two microorganisms in situ. Evidence for nitric oxide (NO) conversion to nitrous oxide was consistently observed for Tectomicrobia across replicates, by production of the NorQ protein. Moreover, we found a potential energy-yielding pathway through CO oxidation by putative Chloroflexi bacteria. Finally, we observed expression of enzymes that may be involved in the transformation of chitin, glycoproteins, glycolipids and glucans into smaller molecules, consistent with glycosyl hydrolases predicted from analyses of the genomes of Poribacteria sponge symbionts. Thus, this study provides crucial links between expressed proteins and specific members of the A. aerophoba microbiome.

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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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            Genomic insights into the marine sponge microbiome.

            Marine sponges (phylum Porifera) often contain dense and diverse microbial communities, which can constitute up to 35% of the sponge biomass. The genome of one sponge, Amphimedon queenslandica, was recently sequenced, and this has provided new insights into the origins of animal evolution. Complementary efforts to sequence the genomes of uncultivated sponge symbionts have yielded the first glimpse of how these intimate partnerships are formed. The remarkable microbial and chemical diversity of the sponge-microorganism association, coupled with its postulated antiquity, makes sponges important model systems for the study of metazoan host-microorganism interactions, and their evolution, as well as for enabling access to biotechnologically important symbiont-derived natural products. In this Review, we discuss our current understanding of the interactions between marine sponges and their microbial symbiotic consortia, and highlight recent insights into these relationships from genomic studies.
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              An environmental bacterial taxon with a large and distinct metabolic repertoire.

              Cultivated bacteria such as actinomycetes are a highly useful source of biomedically important natural products. However, such 'talented' producers represent only a minute fraction of the entire, mostly uncultivated, prokaryotic diversity. The uncultured majority is generally perceived as a large, untapped resource of new drug candidates, but so far it is unknown whether taxa containing talented bacteria indeed exist. Here we report the single-cell- and metagenomics-based discovery of such producers. Two phylotypes of the candidate genus 'Entotheonella' with genomes of greater than 9 megabases and multiple, distinct biosynthetic gene clusters co-inhabit the chemically and microbially rich marine sponge Theonella swinhoei. Almost all bioactive polyketides and peptides known from this animal were attributed to a single phylotype. 'Entotheonella' spp. are widely distributed in sponges and belong to an environmental taxon proposed here as candidate phylum 'Tectomicrobia'. The pronounced bioactivities and chemical uniqueness of 'Entotheonella' compounds provide significant opportunities for ecological studies and drug discovery.
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                Author and article information

                Contributors
                m.chaib.de.mares@rug.nl
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                7 August 2018
                7 August 2018
                2018
                : 8
                : 11795
                Affiliations
                [1 ]ISNI 0000 0004 0407 1981, GRID grid.4830.f, Microbial Ecology Cluster, Groningen Institute for Evolutionary Life Sciences (GELIFES), , University of Groningen, ; Nijenborgh 7, 9747 AG Groningen, The Netherlands
                [2 ]ISNI 0000000419370714, GRID grid.7247.6, Department of Biological Sciences, , Universidad de los Andes, ; Bogotá, Colombia
                [3 ]ISNI 0000 0001 0791 5666, GRID grid.4818.5, Laboratory of Microbiology, , Wageningen University, ; Wageningen, The Netherlands
                [4 ]ISNI 0000 0001 2295 9843, GRID grid.16008.3f, Luxembourg Centre for Systems Biomedicine, , University of Luxembourg, ; Esch-sur-Alzette, Luxembourg
                [5 ]ISNI 0000 0001 2157 9291, GRID grid.11843.3f, Department of Microbiology, Genomics and the Environment, UMR 7156 UNISTRA – CNRS, , Université de Strasbourg, ; Strasbourg, France
                Author information
                http://orcid.org/0000-0002-3359-3258
                http://orcid.org/0000-0002-9339-6520
                Article
                30134
                10.1038/s41598-018-30134-0
                6081418
                30087358
                f3844da5-0a93-4d00-8a89-73c6af8ae0fb
                © 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
                : 4 April 2018
                : 23 July 2018
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100004963, EC | Seventh Framework Programme (European Union Seventh Framework Programme);
                Award ID: 607786
                Award ID: 607786
                Award ID: 607786
                Award ID: 607786
                Award Recipient :
                Funded by: N/A
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