Food ration affects mRNA processing, translation, proteostasis, and cytoskeletal responses during heat shock in Mytilus californianus

Despite a likely role in setting stress tolerance limits, food ration has received limited attention as an ecological factor affecting the cellular stress response (CSR). To study the interactive effects of food and temperature on the proteomic heat shock response, we acclimated intertidal mussels (Mytilus californianus) to four combinations of nearshore (low) and aquaculture (high) phytoplankton levels, combined with low (20 °C) and high (30 °C) aerial temperatures during daytime low tides. Mussels were then exposed to an acute (6 h), aerial heat stress (33 °C) and allowed to recover for 1 h and 25 h in pre-exposure conditions. Proteomic changes in the gill before and after heat shock were measured using label-free liquid-chromatography-mass spectrometry. Compared to other acclimation treatments, low-food-low-temperature (LTLF) mussels modified more splicing factors, heterogeneous nuclear ribonucleoproteins, ribosomal proteins, and translation initiation and elongation factors, suggesting systemic changes to RNA processing, selection, and translation. LTLF mussels also increased chaperones of the actin- and microtubule-associated cytoskeleton and proteins that mature along the endoplasmic reticulum to Golgi secretory pathway. Simultaneously, actin stress fiber formation at focal adhesions and the extracellular matrix, along with anchoring of microtubule-associated cilia, indicate a possible system-wide mechanical breakdown of the cytoskeleton. Signaling proteins causing cytoskeletal changes varied mainly in LTLF mussels and suggest a food-dependent role for prostaglandin synthesis. Overall, the acclimation-dependent proteomic changes show how thermal conditioning and food ration together will shape the CSR of mussels during heat waves.