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, Noël, Cyril, Cabon, Joëlle, Vitré, Thomas, Mark, Felix C., Mazurais, David
• Format: Article in Journal/Newspaper
• Language: English
• Published: Springer Science and Business Media LLC 2022
• Subjects: Anti-viral immunity; Betanodavirus; Climate change; European sea bass; Long-term transgenerational ocean acidification; Metabolism; Neuro-sensory system; Olfactory epithelium; Transcriptomics; Ocean acidification
• Online Access: https://archimer.ifremer.fr/doc/00777/88898/94499.pdf; https://archimer.ifremer.fr/doc/00777/88898/94500.zip; https://archimer.ifremer.fr/doc/00777/88898/102864.pdf; https://doi.org/10.1186/s12864-022-08647-w; https://archimer.ifremer.fr/doc/00777/88898/

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 ...