Host transcriptomic plasticity and photosymbiotic fidelity underpin Pocillopora acclimatization across thermal regimes in the Pacific Ocean

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 Cruaud, Karine Labadie, Corinne Da Silva, Clémentine Moulin, Emilie Boissin, Guillaume Bourdin, Guillaume Iwankow, Sarah Romac, Sylvain Agostini, Bernard Banaigs, Emmanuel Boss, Chris Bowler, Colomban de Vargas, Eric Douville, Michel Flores, Didier Forcioli, Paola Furla, Pierre E. Galand, Eric Gilson, Fabien Lombard, Stéphane Pesant, Stéphanie Reynaud, Matthew B. Sullivan, Shinichi Sunagawa, Olivier P. Thomas, Romain Troublé, Rebecca Vega Thurber, Didier Zoccola, Serge Planes, Denis Allemand and Patrick Wincker
Additional contact information
Eric J. Armstrong: Univ Evry, Université Paris-Saclay
Julie Lê-Hoang: Univ Evry, Université Paris-Saclay
Quentin Carradec: Univ Evry, Université Paris-Saclay
Jean-Marc Aury: Univ Evry, Université Paris-Saclay
Benjamin Noel: Univ Evry, Université Paris-Saclay
Benjamin C. C. Hume: University of Konstanz
Christian R. Voolstra: University of Konstanz
Julie Poulain: Univ Evry, Université Paris-Saclay
Caroline Belser: Univ Evry, Université Paris-Saclay
David A. Paz-García: Centro de Investigaciones Biológicas del Noroeste (CIBNOR)
Corinne Cruaud: Université Paris-Saclay
Karine Labadie: Université Paris-Saclay
Corinne Da Silva: Univ Evry, Université Paris-Saclay
Clémentine Moulin: Fondation Tara Océan, Base Tara, 8 rue de Prague
Emilie Boissin: UAR 3278 CRIOBE, Université de Perpignan
Guillaume Bourdin: University of Maine
Guillaume Iwankow: UAR 3278 CRIOBE, Université de Perpignan
Sarah Romac: FR2022/ Tara Oceans-GOSEE
Sylvain Agostini: University of Tsukuba
Bernard Banaigs: UAR 3278 CRIOBE, Université de Perpignan
Emmanuel Boss: University of Maine
Chris Bowler: FR2022/ Tara Oceans-GOSEE
Colomban de Vargas: FR2022/ Tara Oceans-GOSEE
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
Paola Furla: Université Côte d’Azur, CNRS, INSERM, IRCAN, Medical School
Pierre E. Galand: Sorbonne Université, CNRS, Laboratoire d’Ecogéochimie des Environnements Benthiques (LECOB), Observatoire Océanologique de Banyuls
Eric Gilson: Université Côte d’Azur, CNRS, INSERM, IRCAN, Medical School
Fabien Lombard: FR2022/ Tara Oceans-GOSEE
Stéphane Pesant: European Bioinformatics Institute, Wellcome Genome Campus, Hinxton
Stéphanie Reynaud: Laboratoire International Associé Université Côte d’Azur - Centre Scientifique de Monaco
Matthew B. Sullivan: Ohio State University
Shinichi Sunagawa: Institute of Microbiology, Department of Biology
Olivier P. Thomas: University of Galway
Romain Troublé: Fondation Tara Océan, Base Tara, 8 rue de Prague
Rebecca Vega Thurber: Oregon State University, Department of Microbiology
Didier Zoccola: Laboratoire International Associé Université Côte d’Azur - Centre Scientifique de Monaco
Serge Planes: PSL Research University: EPHE-UPVD-CNRS, USR 3278 CRIOBE, Université de Perpignan
Denis Allemand: Laboratoire International Associé Université Côte d’Azur - Centre Scientifique de Monaco
Patrick Wincker: Univ Evry, Université Paris-Saclay

Nature Communications, 2023, vol. 14, issue 1, 1-18

Abstract: Abstract Heat waves are causing declines in coral reefs globally. Coral thermal responses depend on multiple, interacting drivers, such as past thermal exposure, endosymbiont community composition, and host genotype. This makes the understanding of their relative roles in adaptive and/or plastic responses crucial for anticipating impacts of future warming. Here, we extracted DNA and RNA from 102 Pocillopora colonies collected from 32 sites on 11 islands across the Pacific Ocean to characterize host-photosymbiont fidelity and to investigate patterns of gene expression across a historical thermal gradient. We report high host-photosymbiont fidelity and show that coral and microalgal gene expression respond to different drivers. Differences in photosymbiotic association had only weak impacts on host gene expression, which was more strongly correlated with the historical thermal environment, whereas, photosymbiont gene expression was largely determined by microalgal lineage. Overall, our results reveal a three-tiered strategy of thermal acclimatization in Pocillopora underpinned by host-photosymbiont specificity, host transcriptomic plasticity, and differential photosymbiotic association under extreme warming.

Date: 2023
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DOI: 10.1038/s41467-023-38610-6

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