Membrane Lipid Remodeling Strategies Regulate Fluidity for Acute Temperature Adaptation in Oysters

Extreme climatic temperature stress induced by global warming poses a severe threat to the survival of marine invertebrates. The plasma membrane functions as a natural barrier and serves as the first responder to ambient temperature through dynamic modulation of its fluidity. However, the adaptive mechanisms of membrane lipid remodeling in response to temperature fluctuations remain poorly understood in marine organisms. Oysters, the most widely cultivated shellfish globally, hold significant economic and ecological importance. We characterized the changes in plasma membrane lipid composition of two congeneric oyster species-the northern/cold-adapted <i>Crassostrea gigas</i> and the southern/warm-adapted <i>Crassostrea angulata</i>-under short-term acute heat and cold stress, including changes in lipid subclass content, glycerophospholipid acyl chain length, and glycerophospholipid unsaturation. Our results revealed sphingolipids and sterol lipids content may play a more critical role in short-term temperature adaptation, while glycerophospholipid alterations may prioritize dynamic lipid modifications over abundance changes. Notably, the relatively cold tolerant <i>C. gigas</i> exhibited higher lipid unsaturation and shorter acyl chain lengths, with a preferential modulation of glycerophospholipid acyl chain length, while the heat tolerant <i>C. angulata</i> regulated fatty acid unsaturation to maintain membrane fluidity for temperature adaptation. Divergent membrane lipid remodeling strategies in two congeneric oysters provide new insights into the adaptation mechanisms of membrane fluidity in marine organisms, informing risk assessment for aquaculture industries under global warming. The identification of key components such as phosphatidylethanolamine, sphingosine, ceramide phosphates, and cold and heat adapted lipid molecules provides important biomarkers for predicting the adaptive potential of marine organisms to future extreme climate.