Negative synergistic impacts of ocean warming and acidification on the survival and proteome of the commercial sea bream, Sparus aurata

Global change is impacting aquatic ecosystems, with high risks for food production. However, the molecular underpinnings of organismal tolerance to both ocean warming and acidification are largely unknown. Here we tested the effect of warming and acidification in a 42-day experiment on a commercial temperate fish, the gilt-head seabream Sparus aurata. Juvenile fish were exposed to control (C 18 °C pH 8), ocean warming (OW 22 °C pH 8), ocean acidification (OA 18 °C pH 7.5) and ocean warming and acidification (OWA 22 °C pH 7.5). Proxies of fitness (mortality; condition index) and muscle proteome changes were assessed; bioinformatics tools (Cytoscape, STRAP, STRING) were used for functional analyses. While there was no mortality in fish under OW, fish exposed to OA and both OWA showed 17% and 50% mortality, respectively. Condition index remained constant in all treatments. OW alone induced small proteome adjustments (up-regulation of 2 proteins) related to epigenetic gene regulation and cytoskeletal remodeling. OA and both OWA induced greater proteome changes (12 and 8 regulated proteins, respectively) when compared to OW alone, suggesting that pH is central to proteome modulation. OA exposure led to increased glycogen degradation, glycolysis, lipid metabolism, anion homeostasis, cytoskeletal remodeling, immune processes and redox based signaling while decreasing ADP metabolic process. OWA led to increased lipid metabolism, glycogen degradation, glycolysis, cytoskeleton remodeling and decreased muscle filament sliding and intermediate filament organization. Moreover, as rates of change in temperature and acidification depend on region we tested as proof of concept an (i) acidification effect in a hot ocean (22 °C pH 8 vs 22 °C pH 7.5) which led to the regulation of 7 proteins, the novelty being in a boost of anaerobic metabolism and impairment of proteasomal degradation; and (ii) warming effect in an acidified ocean (18 °C pH 7.5 vs 22 °C pH 7.5) which led to the regulation of 5 proteins, with an emphasis on anaerobic metabolism and transcriptional regulation. The negative synergistic effects of ocean warming and acidification on fish survival coupled to the mobilization of storage compounds, enhancement in anaerobic pathways and impaired proteasomal degradation could pose a serious threat to the viability of sea bream populations.