Temperature adaptations of the thermophilic snail Echinolittorina malaccana: insights from metabolomic analysis.

The periwinkle snail Echinolittorina malaccana, whose upper lethal temperature is near 55°C, is one of the most heat-tolerant eukaryotes known. We conducted a multi-level investigation, including cardiac physiology, enzyme activity, and targeted and untargeted metabolomic analysis, that elucidated a spectrum of adaptations to extreme heat. All systems examined showed heat intensity-dependent responses. Under moderate heat stress (from 37 to 45°C) the snail depressed cardiac activity and entered a state of metabolic depression. The global metabolomic analyses and enzymatic analysis showed that the depressed metabolic state under moderate heat stress entailed production of metabolites characteristic of oxygen-independent pathways of ATP generation (lactate and succinate), which suggests that anaerobic metabolism was the main energy supply pathway under heat stress (from 37 to 52°C). The metabolomic analyses also revealed alterations in glycerophospholipid metabolism under extreme heat stress of 52°C, which likely reflected adaptive changes to maintain membrane structure. Small molecular mass organic osmolytes (glycine betaine, choline, and carnitine) showed complex changes in concentration that were consistent with a role of these protein-stabilizing solutes in protection of the proteome under heat stress. This thermophilic species thus can deploy a wide array of adaptive strategies to acclimatize to extremely high temperatures.