Gene expression plasticity and frontloading promote thermotolerance in Pocillopora corals

Ecosystems worldwide are suffering from climate change. Coral reef ecosystems are globally threatened by increasing sea surface temperatures. However, gene expression plasticity provides the potential for organisms to respond rapidly and effectively to environmental changes, and would be favored in...

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Main Authors: Brener-Raffalli, Kelly, Vidal-Dupiol, Jeremie, Adjeroud, Mehdi, Rey, Olivier, Romans, Pascal, Bonhomme, François, Pratlong, Marine, Haguenauer, Anne, Pillot, Rémi, Feuillassier, Lionel, Claereboudt, Michel, Magalon, Hélène, Gélin, Pauline, Pontarotti, Pierre, Aurelle, Didier, Mitta, Guillaume, Toulza, Eve
Format: Article
Language:English
Published: Peer Community In 2022-02-01
Series:Peer Community Journal
Online Access:https://peercommunityjournal.org/articles/10.24072/pcjournal.79/
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author Brener-Raffalli, Kelly
Vidal-Dupiol, Jeremie
Adjeroud, Mehdi
Rey, Olivier
Romans, Pascal
Bonhomme, François
Pratlong, Marine
Haguenauer, Anne
Pillot, Rémi
Feuillassier, Lionel
Claereboudt, Michel
Magalon, Hélène
Gélin, Pauline
Pontarotti, Pierre
Aurelle, Didier
Mitta, Guillaume
Toulza, Eve
author_facet Brener-Raffalli, Kelly
Vidal-Dupiol, Jeremie
Adjeroud, Mehdi
Rey, Olivier
Romans, Pascal
Bonhomme, François
Pratlong, Marine
Haguenauer, Anne
Pillot, Rémi
Feuillassier, Lionel
Claereboudt, Michel
Magalon, Hélène
Gélin, Pauline
Pontarotti, Pierre
Aurelle, Didier
Mitta, Guillaume
Toulza, Eve
author_sort Brener-Raffalli, Kelly
collection DOAJ
description Ecosystems worldwide are suffering from climate change. Coral reef ecosystems are globally threatened by increasing sea surface temperatures. However, gene expression plasticity provides the potential for organisms to respond rapidly and effectively to environmental changes, and would be favored in variable environments. In this study, we investigated the thermal stress response in Pocillopora coral colonies from two contrasting environments by exposing them to heat stress. We compared the physiological state, bacterial and Symbiodiniaceae communities (using 16S and ITS2 metabarcoding), and gene expression levels (using RNA-Seq) between control conditions and heat stress (the temperature just below the first signs of compromised health). Colonies from both thermal regimes remained apparently normal and presented open and colored polyps during heat stress, with no change in bacterial and Symbiodiniaceae community composition. In contrast, they differed in their transcriptomic responses. The colonies from Oman displayed a more plastic transcriptome, but some genes had a higher basal expression level (frontloading) compared to the less thermotolerant colonies from New Caledonia. In terms of biological functions, we observed an increase in the expression of stress response genes (including induction of tumor necrosis factor receptors, heat shock proteins, and detoxification of reactive oxygen species), together with a decrease in the expression of genes involved in morpho-anatomical functions. Gene regulation (transcription factors, mobile elements, histone modifications and DNA methylation) appeared to be overrepresented in the Oman colonies, indicating possible epigenetic regulation. These results show that transcriptomic plasticity and frontloading can be co-occurring processes in corals confronted with highly variable thermal regimes.
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spelling doaj.art-ebefdf2b03a541ffb63a193cd1e502ae2023-10-24T14:38:36ZengPeer Community InPeer Community Journal2804-38712022-02-01210.24072/pcjournal.7910.24072/pcjournal.79Gene expression plasticity and frontloading promote thermotolerance in Pocillopora coralsBrener-Raffalli, Kelly0Vidal-Dupiol, Jeremie1https://orcid.org/0000-0002-0577-2953Adjeroud, Mehdi2https://orcid.org/0000-0002-6825-8759Rey, Olivier3https://orcid.org/0000-0003-3699-7204Romans, Pascal4Bonhomme, François5https://orcid.org/0000-0002-8792-9239Pratlong, Marine6Haguenauer, Anne7https://orcid.org/0000-0003-2332-2929Pillot, Rémi8Feuillassier, Lionel9Claereboudt, Michel10https://orcid.org/0000-0003-0868-338XMagalon, Hélène11https://orcid.org/0000-0002-7061-955XGélin, Pauline12Pontarotti, Pierre13https://orcid.org/0000-0001-7202-3648Aurelle, Didier14https://orcid.org/0000-0002-3922-7291Mitta, Guillaume15https://orcid.org/0000-0003-1188-1467Toulza, Eve16https://orcid.org/0000-0003-2049-2279IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan via Domitia, Perpignan FranceIHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan via Domitia, Montpellier FranceENTROPIE, IRD, Université de la Réunion, CNRS, IFREMER, Université de la Nouvelle-Calédonie, Perpignan, France; Laboratoire d’Excellence “CORAIL”, Paris, France; PSL Université Paris, USR 3278 CRIOBE EPHE-UPVD-CNRS, Perpignan, FranceIHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan via Domitia, Perpignan FranceObservatoire Océanologique de Banyuls, Sorbonne Université-CNRS, FR3724, Avenue Pierre Fabre, 66650 Banyuls-sur-Mer, FranceInstitut des Sciences de l'Évolution, Univ. Montpellier, CNRS, IRD, EPHE, Montpellier, France. Aix Marseille Univ, CNRS, Centrale Marseille, I2M, Marseille, France, Equipe Evolution Biologique et Modélisation, Marseille, France; Aix Marseille Univ, Université de Toulon, CNRS, IRD, MIO, Marseille, FranceAix-Marseille Université, Avignon Université, CNRS, IRD, IMBE, Marseille, FranceObservatoire Océanologique de Banyuls, Sorbonne Université-CNRS, FR3724, Avenue Pierre Fabre, 66650 Banyuls-sur-Mer, FranceObservatoire Océanologique de Banyuls, Sorbonne Université-CNRS, FR3724, Avenue Pierre Fabre, 66650 Banyuls-sur-Mer, FranceDepartment of Marine Science and Fisheries, College of Agricultural and Marine Sciences, Sultan Qaboos University, Al-Khod, 123, Sultanate of OmanENTROPIE, IRD, Université de la Réunion, CNRS, IFREMER, Université de la Nouvelle-Calédonie, Perpignan, France; Laboratoire d’Excellence “CORAIL”, Paris, France; PSL Université Paris, USR 3278 CRIOBE EPHE-UPVD-CNRS, Perpignan, FranceENTROPIE, IRD, Université de la Réunion, CNRS, IFREMER, Université de la Nouvelle-Calédonie, Perpignan, France; Laboratoire d’Excellence “CORAIL”, Paris, France; PSL Université Paris, USR 3278 CRIOBE EPHE-UPVD-CNRS, Perpignan, FranceAix Marseille Univ, IRD, APHM, Microbe, Evolution, PHylogénie, Infection, IHU Méditerranée Infection, Marseille France. Evolutionary Biology team; CNRS SNC5039Aix Marseille Univ, Université de Toulon, CNRS, IRD, MIO, Marseille, France; Aix-Marseille Université, Avignon Université, CNRS, IRD, IMBE, Marseille, France; Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, EPHE, 57 rue Cuvier, 75005 Paris, FranceIHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan via Domitia, Perpignan France; Univ Polynesie Francaise, ILM, IRD, Ifremer, F-98719 Tahiti, French Polynesia, FranceIHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan via Domitia, Perpignan FranceEcosystems worldwide are suffering from climate change. Coral reef ecosystems are globally threatened by increasing sea surface temperatures. However, gene expression plasticity provides the potential for organisms to respond rapidly and effectively to environmental changes, and would be favored in variable environments. In this study, we investigated the thermal stress response in Pocillopora coral colonies from two contrasting environments by exposing them to heat stress. We compared the physiological state, bacterial and Symbiodiniaceae communities (using 16S and ITS2 metabarcoding), and gene expression levels (using RNA-Seq) between control conditions and heat stress (the temperature just below the first signs of compromised health). Colonies from both thermal regimes remained apparently normal and presented open and colored polyps during heat stress, with no change in bacterial and Symbiodiniaceae community composition. In contrast, they differed in their transcriptomic responses. The colonies from Oman displayed a more plastic transcriptome, but some genes had a higher basal expression level (frontloading) compared to the less thermotolerant colonies from New Caledonia. In terms of biological functions, we observed an increase in the expression of stress response genes (including induction of tumor necrosis factor receptors, heat shock proteins, and detoxification of reactive oxygen species), together with a decrease in the expression of genes involved in morpho-anatomical functions. Gene regulation (transcription factors, mobile elements, histone modifications and DNA methylation) appeared to be overrepresented in the Oman colonies, indicating possible epigenetic regulation. These results show that transcriptomic plasticity and frontloading can be co-occurring processes in corals confronted with highly variable thermal regimes.https://peercommunityjournal.org/articles/10.24072/pcjournal.79/
spellingShingle Brener-Raffalli, Kelly
Vidal-Dupiol, Jeremie
Adjeroud, Mehdi
Rey, Olivier
Romans, Pascal
Bonhomme, François
Pratlong, Marine
Haguenauer, Anne
Pillot, Rémi
Feuillassier, Lionel
Claereboudt, Michel
Magalon, Hélène
Gélin, Pauline
Pontarotti, Pierre
Aurelle, Didier
Mitta, Guillaume
Toulza, Eve
Gene expression plasticity and frontloading promote thermotolerance in Pocillopora corals
Peer Community Journal
title Gene expression plasticity and frontloading promote thermotolerance in Pocillopora corals
title_full Gene expression plasticity and frontloading promote thermotolerance in Pocillopora corals
title_fullStr Gene expression plasticity and frontloading promote thermotolerance in Pocillopora corals
title_full_unstemmed Gene expression plasticity and frontloading promote thermotolerance in Pocillopora corals
title_short Gene expression plasticity and frontloading promote thermotolerance in Pocillopora corals
title_sort gene expression plasticity and frontloading promote thermotolerance in pocillopora corals
url https://peercommunityjournal.org/articles/10.24072/pcjournal.79/
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