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Diversity, structure and convergent evolution of the global sponge microbiome

Author

Listed:
  • Torsten Thomas

    (School of Biological, Earth and Environmental Sciences, Centre for Marine Bio-Innovation and School of Biotechnology and Biomolecular Sciences, University of New South Wales)

  • Lucas Moitinho-Silva

    (School of Biological, Earth and Environmental Sciences, Centre for Marine Bio-Innovation and School of Biotechnology and Biomolecular Sciences, University of New South Wales)

  • Miguel Lurgi

    (The Environment Institute and School of Biological Sciences, University of Adelaide)

  • Johannes R. Björk

    (Ecological Networks and Global Change Group, Experimental and Theoretical Ecology Station, Centre National de la Recherche Scientifique
    Institute of Marine Sciences, CSIC)

  • Cole Easson

    (University of Alabama at Birmingham)

  • Carmen Astudillo-García

    (School of Biological Sciences, University of Auckland)

  • Julie B. Olson

    (University of Alabama)

  • Patrick M. Erwin

    (and Center for Marine Science. University of North Carolina Wilmington)

  • Susanna López-Legentil

    (and Center for Marine Science. University of North Carolina Wilmington)

  • Heidi Luter

    (NAMRA and the Research Institute for the Environment and Livelihoods, Charles Darwin University)

  • Andia Chaves-Fonnegra

    (Halmos College of Natural Sciences and Oceanography, Guy Harvey Oceanographic Center, Nova Southeastern University)

  • Rodrigo Costa

    (Microbial Ecology and Evolution Research Group, Centre of Marine Sciences, Algarve University)

  • Peter J. Schupp

    (Institute of Chemistry and Biology of the Marine Environment, ICBM, University of Oldenburg)

  • Laura Steindler

    (Leon Charney School of Marine Sciences, University of Haifa)

  • Dirk Erpenbeck

    (Ludwig-Maximilians-Universität)

  • Jack Gilbert

    (University of Chicago
    Argonne National Laboratory)

  • Rob Knight

    (University of California at San Diego, 9500 Gilman Drive)

  • Gail Ackermann

    (University of California at San Diego, 9500 Gilman Drive)

  • Jose Victor Lopez

    (Halmos College of Natural Sciences and Oceanography, Guy Harvey Oceanographic Center, Nova Southeastern University)

  • Michael W. Taylor

    (School of Biological Sciences, University of Auckland)

  • Robert W. Thacker

    (Stony Brook University)

  • Jose M. Montoya

    (Ecological Networks and Global Change Group, Experimental and Theoretical Ecology Station, Centre National de la Recherche Scientifique)

  • Ute Hentschel

    (GEOMAR Helmholtz Centre for Ocean Research Kiel)

  • Nicole S. Webster

    (Australian Institute of Marine Science)

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.

Suggested Citation

  • Torsten Thomas & Lucas Moitinho-Silva & Miguel Lurgi & Johannes R. Björk & Cole Easson & Carmen Astudillo-García & Julie B. Olson & Patrick M. Erwin & Susanna López-Legentil & Heidi Luter & Andia Chav, 2016. "Diversity, structure and convergent evolution of the global sponge microbiome," Nature Communications, Nature, vol. 7(1), pages 1-12, September.
  • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms11870
    DOI: 10.1038/ncomms11870
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    Cited by:

    1. Malory O. Brown & Babatunde O. Olagunju & José-Luis Giner & Paula V. Welander, 2023. "Sterol methyltransferases in uncultured bacteria complicate eukaryotic biomarker interpretations," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    2. Gregory A Ellis & Chris S Thomas & Shaurya Chanana & Navid Adnani & Emily Szachowicz & Doug R Braun & Mary Kay Harper & Thomas P Wyche & Tim S Bugni, 2017. "Brackish habitat dictates cultivable Actinobacterial diversity from marine sponges," PLOS ONE, Public Library of Science, vol. 12(7), pages 1-19, July.
    3. M. McCauley & T. L. Goulet & C. R. Jackson & S. Loesgen, 2023. "Systematic review of cnidarian microbiomes reveals insights into the structure, specificity, and fidelity of marine associations," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Wenxiu Wang & Weizhi Song & Marwan E. Majzoub & Xiaoyuan Feng & Bu Xu & Jianchang Tao & Yuanqing Zhu & Zhiyong Li & Pei-Yuan Qian & Nicole S. Webster & Torsten Thomas & Lu Fan, 2024. "Decoupling of strain- and intrastrain-level interactions of microbiomes in a sponge holobiont," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. Kathrin Busch & Beate M. Slaby & Wolfgang Bach & Antje Boetius & Ina Clefsen & Ana Colaço & Marie Creemers & Javier Cristobo & Luisa Federwisch & Andre Franke & Asimenia Gavriilidou & Andrea Hethke & , 2022. "Biodiversity, environmental drivers, and sustainability of the global deep-sea sponge microbiome," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

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