Background

Progressive climate-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 internal acid-base homeostasis efficiently, indirect ionic regulation effects 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 of ecological and commercial importance is not yet 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 CO2 levels (IPCC RCP8.5), with parents being exposed for four years and their offspring for two years. Our design included a transcriptomic analysis of the olfactory rosette (collected from the F1 offspring) and a viral challenge (exposing F1 offspring to betanodavirus) where we assessed survival rates.

Results

We discovered long-term intergenerational molecular trade-offs in both sensory and immune systems. Specifically, RNA-Seq analysis of the olfactory rosette, the peripheral olfactory organ, from two-year-old F1 offspring revealed extensive regulation in genes involved in ion transport and neuronal signalling, including GABAergic signalling. We also detected extensive OA-induced intergenerational up-regulation of genes associated with odour transduction, synaptic plasticity, neuron excitability and wiring and down-regulation of genes involved in energy metabolism. In addition, intergenerational exposure to OA 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 F1 fish challenged with betanodavirus, which causes damage to the nervous system of marine fish, had acquired improved resistance.

Conclusion

F1 exposed to OA-intergenerational acclimation showed superior viral resistance, though as their metabolic and odour transduction programs were altered, odour-mediated behaviours might be consequently altered. Our results reveal that trade-offs in adaptive plastic responses is a core feature of the olfactory epithelium transcriptome in OA-exposed fish, suggesting that intergenerational plasticity propagate with progressive exposure to OA and will have important consequences for how cultured and wild fish interacts with its environment.