Olfactory specialization in the Senegalese sole (Solea senegalensis): CO2 acidified water triggers nostril-specific immune processes

Increased carbon dioxide (CO₂) in the ocean is changing seawater chemistry. Behavioural alterations in CO₂ exposed fish have been linked to changes in the central nervous system (CNS). However, we hypothesise that receptor cells in direct contact with the environment are more susceptible to changes in water chemistry than the CNS. Electrophysiology, histology, and transcriptomics were used to explore the effect of exposure to CO₂ acidified water on the olfactory epithelium (OE) of the Senegalese sole (Solea senegalensis). The upper and lower OE of this flatfish detect different odorants and are in contact with different environments. Acute exposure to acidified water decreased olfactory sensitivity more in the upper than in the lower OE. After chronic exposure to high CO₂ there were no histological changes in the upper OE; however, in the lower OE, there was a massive infiltration of melanomacrophage (MMC) and tissue disorganization. In addition, in the upper OE, differential expressed gene transcripts (DETs) were related to inflammation and innate immune processes whereas in the lower OE, DETs were related to the adaptative immune response. Differential regulation of genes related to neurogenesis and plasticity occurred in both epithelia. The effects of ocean acidification in sole OE depends on the nostril; however, the occurrence of an exacerbated immune response, OE remodelling and reduced sensitivity indicate that ocean acidification is likely to have significant and unpredictable consequences for behaviour.