Dynamic Remodeling of Membrane Proteins for Temperature Adaptation in Oysters

Rising ocean temperatures due to global warming pose severe threats to marine organism survival. Membrane proteins perform important biological functions and serve as sensitive environmental stress sensors. However, the characterization of membrane protein content in response to temperature adaptation remains poorly understood in marine organisms. Here, we performed reciprocal transplantation experiments between the northern/cold and southern/warm natural habitats of two allopatric but closely related oyster species, Crassostrea gigas and C. angulata. Comparative membrane proteomics combined with transcriptomic analysis revealed ABC transporters, Notch signaling, biosynthesis of unsaturated fatty acids, and aquaporins as key molecular components of temperature adaptation in oysters. ABC transporters and key endoplasmic reticulum enzymes for unsaturated fatty acid synthesis (SCD, FADS2, and ELOVL4) exhibited consistently higher protein abundance in northern environments, indicating their involvement in cold adaptation. The Notch signaling pathway may serve as a crucial mechanism for sensing temperature fluctuations and coordinating regulation of antioxidant defense and apoptosis. Additionally, we identified that aquaporins function as both key heat- and cold-adapted proteins, suggesting their crucial role in temperature fluctuation responses. A nonsynonymous mutation identified in the AQUAPORIN-8 coding region may modulate tetrameric water channel formation, thereby altering transport efficiency and potentially contributing to differential temperature tolerance between the two oyster species. This study is the first to characterize dynamic changes of membrane protein in oysters, which reveals its critical role in ambient temperature adaptation and provides new insights into predicting the adaptability of marine organisms to future climate changes.