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Host biology, ecology and the environment influence microbial biomass and diversity in 101 marine fish species

Author

Listed:
  • Jeremiah J. Minich

    (The Salk Institute for Biological Studies)

  • Andreas Härer

    (University of California San Diego)

  • Joseph Vechinski

    (University of California San Diego)

  • Benjamin W. Frable

    (University of California San Diego)

  • Zachary R. Skelton

    (University of California San Diego)

  • Emily Kunselman

    (University of California San Diego)

  • Michael A. Shane

    (Hubbs-SeaWorld Research Institute)

  • Daniela S. Perry

    (University of California, San Diego
    University of California, San Diego)

  • Antonio Gonzalez

    (University of California, San Diego)

  • Daniel McDonald

    (University of California, San Diego)

  • Rob Knight

    (University of California, San Diego
    University of California, San Diego
    University of San Diego, California
    University of California, San Diego)

  • Todd P. Michael

    (The Salk Institute for Biological Studies)

  • Eric E. Allen

    (University of California San Diego
    University of California San Diego
    University of San Diego, California
    University of California San Diego)

Abstract

Fish are the most diverse and widely distributed vertebrates, yet little is known about the microbial ecology of fishes nor the biological and environmental factors that influence fish microbiota. To identify factors that explain microbial diversity patterns in a geographical subset of marine fish, we analyzed the microbiota (gill tissue, skin mucus, midgut digesta and hindgut digesta) from 101 species of Southern California marine fishes, spanning 22 orders, 55 families and 83 genera, representing ~25% of local marine fish diversity. We compare alpha, beta and gamma diversity while establishing a method to estimate microbial biomass associated with these host surfaces. We show that body site is the strongest driver of microbial diversity while microbial biomass and diversity is lowest in the gill of larger, pelagic fishes. Patterns of phylosymbiosis are observed across the gill, skin and hindgut. In a quantitative synthesis of vertebrate hindguts (569 species), we also show that mammals have the highest gamma diversity when controlling for host species number while fishes have the highest percent of unique microbial taxa. The composite dataset will be useful to vertebrate microbiota researchers and fish biologists interested in microbial ecology, with applications in aquaculture and fisheries management.

Suggested Citation

  • Jeremiah J. Minich & Andreas Härer & Joseph Vechinski & Benjamin W. Frable & Zachary R. Skelton & Emily Kunselman & Michael A. Shane & Daniela S. Perry & Antonio Gonzalez & Daniel McDonald & Rob Knigh, 2022. "Host biology, ecology and the environment influence microbial biomass and diversity in 101 marine fish species," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34557-2
    DOI: 10.1038/s41467-022-34557-2
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    References listed on IDEAS

    as
    1. Mathieu Groussin & Florent Mazel & Jon G. Sanders & Chris S. Smillie & Sébastien Lavergne & Wilfried Thuiller & Eric J. Alm, 2017. "Unraveling the processes shaping mammalian gut microbiomes over evolutionary time," Nature Communications, Nature, vol. 8(1), pages 1-12, April.
    2. Daniel L. Rabosky & Jonathan Chang & Pascal O. Title & Peter F. Cowman & Lauren Sallan & Matt Friedman & Kristin Kaschner & Cristina Garilao & Thomas J. Near & Marta Coll & Michael E. Alfaro, 2018. "An inverse latitudinal gradient in speciation rate for marine fishes," Nature, Nature, vol. 559(7714), pages 392-395, July.
    3. Nicholas D. Youngblut & Georg H. Reischer & William Walters & Nathalie Schuster & Chris Walzer & Gabrielle Stalder & Ruth E. Ley & Andreas H. Farnleitner, 2019. "Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    4. James T. Morton & Clarisse Marotz & Alex Washburne & Justin Silverman & Livia S. Zaramela & Anna Edlund & Karsten Zengler & Rob Knight, 2019. "Establishing microbial composition measurement standards with reference frames," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
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