The extensive transgenerational transcriptomic effects of ocean acidification on the olfactory epithelium of a marine fish are associated with a better viral resistance

• Published in: BMC Genomics
• Main Authors: Cohen-Rengifo, Mishal, Danion, Morgane, Gonzalez, Anne-Alicia, Bégout, Marie-Laure, Cormier, Alexandre, Noel, Cyril, Cabon, Joëlle, Vitré, Thomas, Mark, Félix, Mazurais, David
• Other Authors: Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), Laboratoire de Ploufragan-Plouzané-Niort ANSES, Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail (ANSES), BioCampus (BCM), Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), MARine Biodiversity Exploitation and Conservation (UMR MARBEC), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM), Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Alfred Wegener Institute for Polar and Marine Research (AWI), The is study was supported by the AWI-MARUM-IFREMER AMI Partnership Programme (DEADLY TRIO project), LabexMer (ANR-10LABX-0019, OASYS project), the Ministry of Ecological and Solidarity Transition and the Foundation for Biodiversity Research (Ocean Acidification Program, PACIO project), the Deutsche Forschungsgemeinschaft, PE 1157/8–1, MA4271/3–1 (the FITNESS project) and France Génomique National infrastructure, funded as part of “Investissement d’Avenir” program managed by Agence Nationale pour la Recherche (contract ANR-10-INBS-09). Open Access funding enabled and organized by Projekt DEAL., ANR-10-INBS-0009,France-Génomique,Organisation et montée en puissance d'une Infrastructure Nationale de Génomique(2010), ANR-10-LABX-0019,LabexMER,LabexMER Marine Excellence Research: a changing ocean(2010)
• Format: Article in Journal/Newspaper
• Language: English
• Published: HAL CCSD 2022
• Subjects: Metabolism; teleost fish; Climate change; Transcriptomics; European sea bass; mass mortalities; Betanodavirus; Anti-viral immunity; carbon-dioxide; double-stranded-rna; immune-response; induced mx proteins; interferon-stimulated genes; Long-term transgenerational ocean acidification; mhc class-i; Neuro-sensory system; nod-like receptor; Olfactory epithelium; reared sea-bass; [SDE.BE]Environmental Sciences/Biodiversity and Ecology; [SDE.MCG]Environmental Sciences/Global Changes; Ocean acidification
• Online Access: https://hal.umontpellier.fr/hal-03718439; https://hal.umontpellier.fr/hal-03718439/document; https://hal.umontpellier.fr/hal-03718439/file/s12864-022-08647-w.pdf; https://doi.org/10.1186/s12864-022-08647-w

International audience Background Progressive CO2-induced ocean acidification (OA) impacts marine life in ways that are difficult to predict but are likely to become exacerbated over generations. Although marine fishes can balance acid-base homeostasis efficiently, indirect ionic regulation that alter neurosensory systems can result in behavioural abnormalities. In marine invertebrates, OA can also affect immune system function, but whether this is the case in marine fishes is not fully understood. Farmed fish are highly susceptible to disease outbreak, yet strategies for overcoming such threats in the wake of OA are wanting. Here, we exposed two generations of the European sea bass (Dicentrarchus labrax) to end-of-century predicted pH levels (IPCC RCP8.5), with parents (F1) being exposed for four years and their offspring (F2) for 18 months. Our design included a transcriptomic analysis of the olfactory rosette (collected from the F2) and a viral challenge (exposing F2 to betanodavirus) where we assessed survival rates. Results We discovered transcriptomic trade-offs in both sensory and immune systems after long-term transgenerational exposure to OA. Specifically, RNA-Seq analysis of the olfactory rosette, the peripheral olfactory organ, from 18-months-old F2 revealed extensive regulation in genes involved in ion transport and neuronal signalling, including GABAergic signalling. We also detected OA-induced up-regulation of genes associated with odour transduction, synaptic plasticity, neuron excitability and wiring and down-regulation of genes involved in energy metabolism. Furthermore, OA-exposure induced up-regulation of genes involved in innate antiviral immunity (pathogen recognition receptors and interferon-stimulated genes) in combination with down-regulation of the protein biosynthetic machinery. Consistently, OA-exposed F2 challenged with betanodavirus, which causes damage to the nervous system of marine fish, had acquired improved resistance. Conclusion F2 exposed to long-term transgenerational OA ...