IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38500-x.html
   My bibliography  Save this article

Diversity of the Pacific Ocean coral reef microbiome

Author

Listed:
  • Pierre E. Galand

    (Sorbonne Université, CNRS, Laboratoire d’Ecogéochimie des Environnements Benthiques (LECOB), Observatoire Océanologique de Banyuls
    Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022 GOSEE)

  • Hans-Joachim Ruscheweyh

    (Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zürich)

  • Guillem Salazar

    (Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zürich)

  • Corentin Hochart

    (Sorbonne Université, CNRS, Laboratoire d’Ecogéochimie des Environnements Benthiques (LECOB), Observatoire Océanologique de Banyuls)

  • Nicolas Henry

    (Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022 GOSEE
    Sorbonne Université, CNRS, Station Biologique de Roscoff, AD2M, UMR 7144, ECOMAP)

  • Benjamin C. C. Hume

    (University of Konstanz)

  • Pedro H. Oliveira

    (Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022 GOSEE
    Université Paris-Saclay)

  • Aude Perdereau

    (Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022 GOSEE
    Université Paris-Saclay)

  • Karine Labadie

    (Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022 GOSEE
    Université Paris-Saclay)

  • Caroline Belser

    (Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022 GOSEE
    Université Paris-Saclay)

  • Emilie Boissin

    (Université de Perpignan)

  • Sarah Romac

    (Sorbonne Université, CNRS, Station Biologique de Roscoff, AD2M, UMR 7144, ECOMAP)

  • Julie Poulain

    (Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022 GOSEE
    Université Paris-Saclay)

  • Guillaume Bourdin

    (University of Maine)

  • Guillaume Iwankow

    (Université de Perpignan)

  • Clémentine Moulin

    (Fondation Tara Océan)

  • Eric J. Armstrong

    (Université de Perpignan)

  • David A. Paz-García

    (Centro de Investigaciones Biológicas del Noroeste (CIBNOR))

  • Maren Ziegler

    (Justus Liebig University Giessen)

  • Sylvain Agostini

    (University of Tsukuba)

  • Bernard Banaigs

    (Université de Perpignan)

  • Emmanuel Boss

    (University of Maine)

  • Chris Bowler

    (Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022 GOSEE
    Université PSL)

  • Colomban Vargas

    (Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022 GOSEE
    Sorbonne Université, CNRS, Station Biologique de Roscoff, AD2M, UMR 7144, ECOMAP)

  • Eric Douville

    (Université Paris-Saclay)

  • Michel Flores

    (Weizmann Institute of Science, Department of Earth and Planetary Sciences)

  • Didier Forcioli

    (Université Côte d’Azur, CNRS, INSERM, IRCAN, Medical School
    LIA ROPSE, Laboratoire International Associé Université Côte d’Azur-Centre Scientifique de Monaco)

  • Paola Furla

    (Université Côte d’Azur, CNRS, INSERM, IRCAN, Medical School
    LIA ROPSE, Laboratoire International Associé Université Côte d’Azur-Centre Scientifique de Monaco)

  • Eric Gilson

    (Université Côte d’Azur, CNRS, INSERM, IRCAN, Medical School
    LIA ROPSE, Laboratoire International Associé Université Côte d’Azur-Centre Scientifique de Monaco
    Department of Medical Genetics, CHU of Nice)

  • Fabien Lombard

    (Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022 GOSEE
    Sorbonne Université, Institut de la Mer de Villefranche sur mer, Laboratoire d’Océanographie de Villefranche
    Institut Universitaire de France)

  • Stéphane Pesant

    (European Bioinformatics Institute, Wellcome Genome Campus, Hinxton)

  • Stéphanie Reynaud

    (LIA ROPSE, Laboratoire International Associé Université Côte d’Azur-Centre Scientifique de Monaco
    Centre Scientifique de Monaco)

  • Olivier P. Thomas

    (School of Biological and Chemical Sciences, Ryan Institute, University of Galway)

  • Romain Troublé

    (Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022 GOSEE
    Fondation Tara Océan)

  • Didier Zoccola

    (LIA ROPSE, Laboratoire International Associé Université Côte d’Azur-Centre Scientifique de Monaco
    Centre Scientifique de Monaco)

  • Christian R. Voolstra

    (University of Konstanz)

  • Rebecca Vega Thurber

    (Oregon State University)

  • Shinichi Sunagawa

    (Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zürich)

  • Patrick Wincker

    (Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022 GOSEE
    Université Paris-Saclay)

  • Denis Allemand

    (LIA ROPSE, Laboratoire International Associé Université Côte d’Azur-Centre Scientifique de Monaco
    Centre Scientifique de Monaco)

  • Serge Planes

    (Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022 GOSEE
    Université de Perpignan)

Abstract

Coral reefs are among the most diverse ecosystems on Earth. They support high biodiversity of multicellular organisms that strongly rely on associated microorganisms for health and nutrition. However, the extent of the coral reef microbiome diversity and its distribution at the oceanic basin-scale remains to be explored. Here, we systematically sampled 3 coral morphotypes, 2 fish species, and planktonic communities in 99 reefs from 32 islands across the Pacific Ocean, to assess reef microbiome composition and biogeography. We show a very large richness of reef microorganisms compared to other environments, which extrapolated to all fishes and corals of the Pacific, approximates the current estimated total prokaryotic diversity for the entire Earth. Microbial communities vary among and within the 3 animal biomes (coral, fish, plankton), and geographically. For corals, the cross-ocean patterns of diversity are different from those known for other multicellular organisms. Within each coral morphotype, community composition is always determined by geographic distance first, both at the island and across ocean scale, and then by environment. Our unprecedented sampling effort of coral reef microbiomes, as part of the Tara Pacific expedition, provides new insight into the global microbial diversity, the factors driving their distribution, and the biocomplexity of reef ecosystems.

Suggested Citation

  • Pierre E. Galand & Hans-Joachim Ruscheweyh & Guillem Salazar & Corentin Hochart & Nicolas Henry & Benjamin C. C. Hume & Pedro H. Oliveira & Aude Perdereau & Karine Labadie & Caroline Belser & Emilie B, 2023. "Diversity of the Pacific Ocean coral reef microbiome," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38500-x
    DOI: 10.1038/s41467-023-38500-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38500-x
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-38500-x?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Terry P. Hughes & Michele L. Barnes & David R. Bellwood & Joshua E. Cinner & Graeme S. Cumming & Jeremy B. C. Jackson & Joanie Kleypas & Ingrid A. van de Leemput & Janice M. Lough & Tiffany H. Morriso, 2017. "Coral reefs in the Anthropocene," Nature, Nature, vol. 546(7656), pages 82-90, June.
    2. Maren Ziegler & Carsten G. B. Grupstra & Marcelle M. Barreto & Martin Eaton & Jaafar BaOmar & Khalid Zubier & Abdulmohsin Al-Sofyani & Adnan J. Turki & Rupert Ormond & Christian R. Voolstra, 2019. "Coral bacterial community structure responds to environmental change in a host-specific manner," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    3. Costanza, Robert & de Groot, Rudolf & Braat, Leon & Kubiszewski, Ida & Fioramonti, Lorenzo & Sutton, Paul & Farber, Steve & Grasso, Monica, 2017. "Twenty years of ecosystem services: How far have we come and how far do we still need to go?," Ecosystem Services, Elsevier, vol. 28(PA), pages 1-16.
    4. Maren Ziegler & Francois O. Seneca & Lauren K. Yum & Stephen R. Palumbi & Christian R. Voolstra, 2017. "Bacterial community dynamics are linked to patterns of coral heat tolerance," Nature Communications, Nature, vol. 8(1), pages 1-8, April.
    5. F. Joseph Pollock & Ryan McMinds & Styles Smith & David G. Bourne & Bette L. Willis & Mónica Medina & Rebecca Vega Thurber & Jesse R. Zaneveld, 2018. "Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. C. E. Dubé & M. Ziegler & A. Mercière & E. Boissin & S. Planes & C. A. -F. Bourmaud & C. R. Voolstra, 2021. "Naturally occurring fire coral clones demonstrate a genetic and environmental basis of microbiome composition," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. Corentin Hochart & Lucas Paoli & Hans-Joachim Ruscheweyh & Guillem Salazar & Emilie Boissin & Sarah Romac & Julie Poulain & Guillaume Bourdin & Guillaume Iwankow & Clémentine Moulin & Maren Ziegler & , 2023. "Ecology of Endozoicomonadaceae in three coral genera across the Pacific Ocean," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    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. Buckwell, Andrew & Fleming, Christopher & Smart, James & Mackey, Brendan & Ware, Daniel & Hallgren, Willow & Sahin, Oz & Nalau, Johanna, 2018. "Valuing aggregated ecosystem services at a national and regional scale for Vanuatu using a remotely operable, rapid assessment methodology," 2018 Conference (62nd), February 7-9, 2018, Adelaide, Australia 273524, Australian Agricultural and Resource Economics Society.
    5. Eric J. Armstrong & Julie Lê-Hoang & Quentin Carradec & Jean-Marc Aury & Benjamin Noel & Benjamin C. C. Hume & Christian R. Voolstra & Julie Poulain & Caroline Belser & David A. Paz-García & Corinne C, 2023. "Host transcriptomic plasticity and photosymbiotic fidelity underpin Pocillopora acclimatization across thermal regimes in the Pacific Ocean," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    6. Aryal, Kishor & Maraseni, Tek & Apan, Armando, 2023. "Examining policy−institution−program (PIP) responses against the drivers of ecosystem dynamics. A chronological review (1960–2020) from Nepal," Land Use Policy, Elsevier, vol. 132(C).
    7. Liu, Duan & Tang, Runcheng & Xie, Jun & Tian, Jingjing & Shi, Rui & Zhang, Kai, 2020. "Valuation of ecosystem services of rice–fish coculture systems in Ruyuan County, China," Ecosystem Services, Elsevier, vol. 41(C).
    8. Yajing Shao & Xuefeng Yuan & Chaoqun Ma & Ruifang Ma & Zhaoxia Ren, 2020. "Quantifying the Spatial Association between Land Use Change and Ecosystem Services Value: A Case Study in Xi’an, China," Sustainability, MDPI, vol. 12(11), pages 1-20, May.
    9. Pietrzyk-Kaszyńska, Agata & Olszańska, Agnieszka & Rechciński, Marcin & Tusznio, Joanna & Grodzińska-Jurczak, Małgorzata, 2022. "Divergent or convergent? Prioritization and spatial representation of ecosystem services as perceived by conservation professionals and local leaders," Land Use Policy, Elsevier, vol. 119(C).
    10. Robbie Maris & Mark Holmes, 2023. "Economic Growth Theory and Natural Resource Constraints: A Stocktake and Critical Assessment," Australian Economic Review, The University of Melbourne, Melbourne Institute of Applied Economic and Social Research, vol. 56(2), pages 255-268, June.
    11. van der Hoff, Richard & Nascimento, Nathália & Fabrício-Neto, Ailton & Jaramillo-Giraldo, Carolina & Ambrosio, Geanderson & Arieira, Julia & Afonso Nobre, Carlos & Rajão, Raoni, 2022. "Policy-oriented ecosystem services research on tropical forests in South America: A systematic literature review," Ecosystem Services, Elsevier, vol. 56(C).
    12. Joel C. Creed & Laura Sol Aranda & Júlia Gomes de Sousa & Caio Barros Brito do Bem & Beatriz Sant’Anna Vasconcelos Marafiga Dutra & Marianna Lanari & Virgínia Eduarda de Sousa & Karine M. Magalhães & , 2023. "A Synthesis of Provision and Impact in Seagrass Ecosystem Services in the Brazilian Southwest Atlantic," Sustainability, MDPI, vol. 15(20), pages 1-19, October.
    13. Wanxu Chen & Guangqing Chi & Jiangfeng Li, 2020. "Ecosystem Services and Their Driving Forces in the Middle Reaches of the Yangtze River Urban Agglomerations, China," IJERPH, MDPI, vol. 17(10), pages 1-19, May.
    14. O'Sullivan, Jane N., 2020. "The social and environmental influences of population growth rate and demographic pressure deserve greater attention in ecological economics," Ecological Economics, Elsevier, vol. 172(C).
    15. Nicolás Ruiz, Néstor & Suárez Alonso, María Luisa & Vidal-Abarca, María Rosario, 2021. "Contributions of dry rivers to human well-being: A global review for future research," Ecosystem Services, Elsevier, vol. 50(C).
    16. Moreno-Llorca, R. & Vaz, A.S. & Herrero, J. & Millares, A. & Bonet-García, F.J. & Alcaraz-Segura, D., 2020. "Multi-scale evolution of ecosystem services’ supply in Sierra Nevada (Spain): An assessment over the last half-century," Ecosystem Services, Elsevier, vol. 46(C).
    17. Xiaoyu Li & Shudan Gong & Qingdong Shi & Yuan Fang, 2023. "A Review of Ecosystem Services Based on Bibliometric Analysis: Progress, Challenges, and Future Directions," Sustainability, MDPI, vol. 15(23), pages 1-18, November.
    18. Daniels, Silvie & Bellmore, J. Ryan & Benjamin, Joseph R. & Witters, Nele & Vangronsveld, Jaco & Van Passel, Steven, 2018. "Quantification of the Indirect Use Value of Functional Group Diversity Based on the Ecological Role of Species in the Ecosystem," Ecological Economics, Elsevier, vol. 153(C), pages 181-194.
    19. Lau, Jacqueline D. & Hicks, Christina C. & Gurney, Georgina G. & Cinner, Joshua E., 2018. "Disaggregating ecosystem service values and priorities by wealth, age, and education," Ecosystem Services, Elsevier, vol. 29(PA), pages 91-98.
    20. Shujun Liu & Xinzhuan Yao & Degang Zhao & Litang Lu, 2021. "Evaluation of the ecological benefits of tea gardens in Meitan County, China, using the InVEST model," Environment, Development and Sustainability: A Multidisciplinary Approach to the Theory and Practice of Sustainable Development, Springer, vol. 23(5), pages 7140-7155, May.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38500-x. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.