State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Science, Xiamen University, Xiamen 361102, China.
The Key Laboratory of Mariculture, Ministry of Education, Fisheries College, Ocean University of China, Qingdao 266003, China.
J Exp Biol. 2021 Mar 15;224(Pt 6):jeb238659. doi: 10.1242/jeb.238659.
The periwinkle snail , for which the 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 analyses - that elucidated a spectrum of adaptations to extreme heat in this organism. All systems examined showed heat intensity-dependent responses. Under moderate heat stress (37-45°C), the snail depressed cardiac activity and entered a state of metabolic depression. The global metabolomic and enzymatic analyses revealed production of metabolites characteristic of oxygen-independent pathways of ATP generation (lactate and succinate) in the depressed metabolic state, which suggests that anaerobic metabolism was the main energy supply pathway under heat stress (37-52°C). The metabolomic analyses also revealed alterations in glycerophospholipid metabolism under extreme heat stress (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 can thus deploy a wide array of adaptive strategies to acclimatize to extremely high temperatures.
堇青石蜗牛的上致死温度接近 55°C，是已知最耐热的真核生物之一。我们进行了多层次的研究——包括心脏生理学、酶活性以及靶向和非靶向代谢组学分析——阐明了该生物对极端高温的一系列适应机制。所有检查的系统都显示出对热强度的依赖性反应。在适度的热应激（37-45°C）下，蜗牛会降低心脏活动并进入代谢抑制状态。全面的代谢组学和酶学分析表明，在代谢抑制状态下产生了具有氧非依赖性 ATP 生成途径特征的代谢物（乳酸盐和琥珀酸盐），这表明在热应激（37-52°C）下，无氧代谢是主要的能量供应途径。代谢组学分析还揭示了在极端热应激（52°C）下甘油磷脂代谢的改变，这可能反映了适应变化以维持膜结构。小分子质量有机渗透物（甜菜碱、胆碱和肉碱）的浓度表现出复杂的变化，这与这些稳定蛋白质的溶质在热应激下保护蛋白质组的作用一致。因此，这种嗜热物种可以部署广泛的适应性策略来适应极高的温度。
