The extensive transgenerational transcriptomic effects of ocean acidification on the olfactory epithelium of a marine fish are associated with a better viral resistance
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 alt...
Published in: | BMC Genomics |
---|---|
Main Authors: | , , , , , , , , , |
Other Authors: | , , , , , , , , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
Published: |
HAL CCSD
2022
|
Subjects: | |
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 |
id |
ftunimontpellier:oai:HAL:hal-03718439v1 |
---|---|
record_format |
openpolar |
institution |
Open Polar |
collection |
Université de Montpellier: HAL |
op_collection_id |
ftunimontpellier |
language |
English |
topic |
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 |
spellingShingle |
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 Cohen-Rengifo, Mishal Danion, Morgane Gonzalez, Anne-Alicia Bégout, Marie-Laure Cormier, Alexandre Noel, Cyril Cabon, Joëlle Vitré, Thomas Mark, Félix, C. Mazurais, David The extensive transgenerational transcriptomic effects of ocean acidification on the olfactory epithelium of a marine fish are associated with a better viral resistance |
topic_facet |
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 |
description |
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 ... |
author2 |
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 - MARBEC (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 |
author |
Cohen-Rengifo, Mishal Danion, Morgane Gonzalez, Anne-Alicia Bégout, Marie-Laure Cormier, Alexandre Noel, Cyril Cabon, Joëlle Vitré, Thomas Mark, Félix, C. Mazurais, David |
author_facet |
Cohen-Rengifo, Mishal Danion, Morgane Gonzalez, Anne-Alicia Bégout, Marie-Laure Cormier, Alexandre Noel, Cyril Cabon, Joëlle Vitré, Thomas Mark, Félix, C. Mazurais, David |
author_sort |
Cohen-Rengifo, Mishal |
title |
The extensive transgenerational transcriptomic effects of ocean acidification on the olfactory epithelium of a marine fish are associated with a better viral resistance |
title_short |
The extensive transgenerational transcriptomic effects of ocean acidification on the olfactory epithelium of a marine fish are associated with a better viral resistance |
title_full |
The extensive transgenerational transcriptomic effects of ocean acidification on the olfactory epithelium of a marine fish are associated with a better viral resistance |
title_fullStr |
The extensive transgenerational transcriptomic effects of ocean acidification on the olfactory epithelium of a marine fish are associated with a better viral resistance |
title_full_unstemmed |
The extensive transgenerational transcriptomic effects of ocean acidification on the olfactory epithelium of a marine fish are associated with a better viral resistance |
title_sort |
extensive transgenerational transcriptomic effects of ocean acidification on the olfactory epithelium of a marine fish are associated with a better viral resistance |
publisher |
HAL CCSD |
publishDate |
2022 |
url |
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 |
genre |
Ocean acidification |
genre_facet |
Ocean acidification |
op_source |
ISSN: 1471-2164 BMC Genomics https://hal.umontpellier.fr/hal-03718439 BMC Genomics, 2022, 23 (1), pp.448. ⟨10.1186/s12864-022-08647-w⟩ https://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-022-08647-w |
op_relation |
info:eu-repo/semantics/altIdentifier/doi/10.1186/s12864-022-08647-w info:eu-repo/semantics/altIdentifier/pmid/35710351 hal-03718439 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 doi:10.1186/s12864-022-08647-w PUBMED: 35710351 PUBMEDCENTRAL: PMC9204966 WOS: 000812249800001 |
op_rights |
http://creativecommons.org/licenses/by/ info:eu-repo/semantics/OpenAccess |
op_doi |
https://doi.org/10.1186/s12864-022-08647-w |
container_title |
BMC Genomics |
container_volume |
23 |
container_issue |
1 |
_version_ |
1809933082952728576 |
spelling |
ftunimontpellier:oai:HAL:hal-03718439v1 2024-09-09T20:01:17+00:00 The extensive transgenerational transcriptomic effects of ocean acidification on the olfactory epithelium of a marine fish are associated with a better viral resistance Cohen-Rengifo, Mishal Danion, Morgane Gonzalez, Anne-Alicia Bégout, Marie-Laure Cormier, Alexandre Noel, Cyril Cabon, Joëlle Vitré, Thomas Mark, Félix, C. Mazurais, David 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 - MARBEC (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) 2022-06-17 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 en eng HAL CCSD BioMed Central info:eu-repo/semantics/altIdentifier/doi/10.1186/s12864-022-08647-w info:eu-repo/semantics/altIdentifier/pmid/35710351 hal-03718439 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 doi:10.1186/s12864-022-08647-w PUBMED: 35710351 PUBMEDCENTRAL: PMC9204966 WOS: 000812249800001 http://creativecommons.org/licenses/by/ info:eu-repo/semantics/OpenAccess ISSN: 1471-2164 BMC Genomics https://hal.umontpellier.fr/hal-03718439 BMC Genomics, 2022, 23 (1), pp.448. ⟨10.1186/s12864-022-08647-w⟩ https://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-022-08647-w 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 info:eu-repo/semantics/article Journal articles 2022 ftunimontpellier https://doi.org/10.1186/s12864-022-08647-w 2024-06-17T14:21:32Z 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 ... Article in Journal/Newspaper Ocean acidification Université de Montpellier: HAL BMC Genomics 23 1 |