Transcriptional responses of Mediterranean mussels (Mytilus galloprovincialis) under the 2022 Marine Heatwave: a trade-off of physiological regulation between metabolism, stress response, and shell biomineralization in a mixed exposure scenario

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There has been a notable increase in occurrence and intensity of marine heatwaves (MHWs) over the past decades, with a consequent remarkable risk to vulnerable species as marine bivalves. This study examines the responses of farmed Mytilus galloprovincialis to the 2022 MHW that impacted the Northwestern (NW) Adriatic Sea. Expression of key transcripts involved in functions of digestive glands and mantles were investigated to explore the putative acclimatory processes contributing to mussel fitness. The 2022 MHW was characterized by persistent sea temperature anomalies, elevated salinity, and dramatically low chlorophyll-a levels. Despite the temporal trends of pH and the extreme seawater temperatures reached in July and August, the carbonate system never reached the undersaturation state, being favourable for bivalve biomineralization. Transcriptional profiles in digestive glands and mantles displayed a two-step temporal response. In digestive glands, metabolism and lysosomal response functional categories showed an initial decrease (late May), and a recovery in late August. Antioxidant and cytoprotective related gene products showed a February to August increased expression, with strong up-regulations in August. In mantles, transcripts involved in shell biomineralization were prompted in the initial stage of the MHW, likely to withstand the abrupt changes of seawater parameters and to maintain bivalve growth. At high MHW intensities, energy was diverted towards the strong stress response activation in digestive glands, with a relative decrease of mRNA levels for shell biomineralization transcripts. Results showed that a trade-off between core physiological processes may contribute to the acclimatory response of mussels to cope with the adverse conditions of the 2022 MHW in the NW Adriatic Sea. • Gene transcription in digestive glands and mantles of M. galloprovincialis is reported. • Investigations were performed during the 2022 marine heatwave (MHW). • At early MHW, metabolism and lysosomal responses (digestive glands) were reduced, shell biomineralization (mantles) prompted. • At late MHW, energy was diverted to stress responses (digestive glands), with decreased shell biomineralization transcripts. • A trade-off between core physiological processes contributes to mussel acclimatory responses to the 2022 MHW.