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

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.

Cross-talk between tissues is critical for intergenerational acclimation to environmental change

“…While neural plasticity could facilitate increased flexibility to environmental changes (Ebbesson & Braithwaite, 2012), it could result in behavioural alterations that have been observed in fish exposed to OA conditions (Schunter et al, 2019). Increased GABAergic signaling is a commonly observed within-generation response to elevated CO2 in A. polyacanthus (Schunter et al, 2018) and a similar increase in neural signaling pathways was found in the olfactory epithelium of European seabass (D. labrax) even after prolonged transgenerational OA exposure for two generations (Cohen-Rengifo et al 2022). The restoration of OA induced changes in neural signaling processes with previous parental exposure to elevated CO2 could indicate elevated intergenerational plasticity of A. polyacanthus.…”

Juvenile zebrafish (Danio rerio) are able to recover from lordosis

“…From the extracted RNA samples, five from each group were selected based on the quality of the RNA and they were sent for transcriptome analysis via RNA sequencing at GenomiX (MGX, Montpellier, France) following the procedure described by Cohen-Rengifo et al 66 Total RNA was quantified on Fragment Analyzer (Agilent Technologies, Santa Clara, CA, USA) using the standard sensitivity RNA kit (DNF-471-0500). Libraries were constructed using Stranded mRNA Prep Ligation kit (Illumina, San Diego, CA,USA) according to the manufacturer’s instructions.…”

When Trauma is Passed on through Generations

“…A recent study just demonstrated that exposure to chemicals in plastic products resulted in epigenetic changes in marine fish, which was passed on to both their offspring (F1) and the subsequent generation of marine fish (F2) (Cohen-Rengifo et al, 2022). Interestingly, this epigenetic change led to greater viral resistance to the chemicals (along with changes to their metabolism and scent detection).…”