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

Temperature adaptations of the thermophilic snail Echinolittorina malaccana: insights from metabolomic analysis
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嗜热蜗牛 Echinolittorina malaccana 的温度适应:代谢组学分析的见解

DOI:
10.1242/jeb.238659
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发表时间:
2021-03-01
影响因子:
2.8
通讯作者:
Dong, Yun-wei
Dong, Yun-wei
中科院分区:
生物学2区
文献类型:
--
作者:
Chen, Ya-qi;Wang, Jie;Dong, Yun-wei

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长春花螺Echinolittorina Malaccana的最高致死温度接近55摄氏度,是已知的最耐热的真核生物之一。我们进行了一项多层次的研究,包括心脏生理学、酶活性以及定向和非定向代谢分析-阐明了这种有机体对极端高温的一系列适应。所有被检查的系统都显示出依赖于热强度的响应。在中度热应激(37-45摄氏度)下,蜗牛心脏活动受到抑制,进入代谢抑制状态。整体代谢学和酶分析表明,在低迷的代谢状态下产生的代谢产物是ATP生成的氧不依赖途径的特征代谢物(乳酸和琥珀酸),这表明在热应激(37-52℃)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摄氏度)下甘油磷脂代谢的变化,这可能反映了维持膜结构的适应性变化。小分子有机渗透物质(甘氨酸甜菜碱、胆碱和肉碱)呈现复杂的浓度变化,这与这些稳定蛋白质的溶质在热胁迫下保护蛋白质组的作用是一致的。因此,这种嗜热物种可以部署广泛的适应策略,以适应极高的温度。
The periwinkle snail Echinolittorina malaccana, for which the upper lethal temperature is near 55 degrees 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 degrees 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 degrees C). The metabolomic analyses also revealed alterations in glycerophospholipid metabolism under extreme heat stress (52 degrees 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.