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

Type Article
Date 2022-06
Language English
Author(s) Cohen-Rengifo Mishal1, Danion Morgane2, Gonzalez Anne-Alicia3, Bégout Marie-LaureORCID4, Cormier AlexandreORCID5, Noël CyrilORCID5, Cabon Joëlle2, Vitré Thomas1, Mark Felix C.6, Mazurais DavidORCID1
Affiliation(s) 1 : IFREMER, PFOM-ARN, 29280, Plouzané, France
2 : Ploufragan-Plouzané Laboratory, Fish Viral Pathology Unit, French Agency for Food, Environmental and Occupational Health and Safety (ANSES), Technopôle Brest-Iroise, 29280, Plouzané, France
3 : MGX, CNRS, INSERM, University of Montpellier, Biocampus Montpellier, Montpellier, France
4 : MARBEC, University of Montpellier, CNRS, IFREMER, 34250, Palavas-les-Flots, IRD, France
5 : IFREMER, SEBIMER, 29280, Plouzané, France
6 : Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research (AWI), Department of Integrative Ecophysiology, 27570, Bremerhaven, Germany
Source Bmc Genomics (1471-2164) (Springer Science and Business Media LLC), 2022-06 , Vol. 23 , N. 1 , P. 48 (18p.)
DOI 10.1186/s12864-022-08647-w
WOS© Times Cited 5
Keyword(s) Anti-viral immunity, Betanodavirus, Climate change, European sea bass, Long-term transgenerational ocean acidification, Metabolism, Neuro-sensory system, Olfactory epithelium, Transcriptomics

Abstract 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 acclimation showed superior viral resistance, though as their metabolic and odour transduction programs were altered, odour-mediated behaviours might be consequently impacted. Although it is difficult to unveil how long-term OA impacts propagated between generations, our results reveal that, across generations, trade-offs in plastic responses is a core feature of the olfactory epithelium transcriptome in OA-exposed F2 offspring, and will have important consequences for how cultured and wild fish interacts with its environment.

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Correction - 10.1186/s12864-023-09299-0 1 727 KB Open access
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Cohen-Rengifo Mishal, Danion Morgane, Gonzalez Anne-Alicia, Bégout Marie-Laure, Cormier Alexandre, Noël Cyril, Cabon Joëlle, Vitré Thomas, Mark Felix C., Mazurais David (2022). The extensive transgenerational transcriptomic effects of ocean acidification on the olfactory epithelium of a marine fish are associated with a better viral resistance. Bmc Genomics, 23(1), 48 (18p.). Publisher's official version : , Open Access version :