The Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China.
College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi, China.
Mol Biol Evol. 2023 Mar 4;40(3). doi: 10.1093/molbev/msad040.
Freeze tolerance, the ability of an organism to survive internal ice formation, is a striking survival strategy employed by some ectotherms living in cold environments. However, the genetic bases of this remarkable adaptation are largely unknown. The Amur sleeper (Perccottus glenii), the only known freeze-tolerant fish species, can overwinter with its entire body frozen in ice. Here, we sequenced the chromosome-level genome of the Amur sleeper and performed comparative genomic, transcriptomic, and metabolomic analyses to investigate its strategies for surviving freezing. Evolutionary analysis suggested that the Amur sleeper diverged from its closest non-cold-hardy relative about 15.07 million years ago and has experienced a high rate of protein evolution. Transcriptomic and metabolomic data identified a coordinated and tissue-specific regulation of genes and metabolites involved in hypometabolism, cellular stress response, and cryoprotectant accumulation involved in freezing and thawing. Several genes show evidence of accelerated protein sequence evolution or family size expansion were found as adaptive responses to freezing-induced stresses. Specifically, genetic changes associated with cytoskeleton stability, cryoprotectant synthesis, transmembrane transport, and neuroprotective adaptations were identified as potentially key innovations that aid in freezing survival. Our work provides valuable resources and opportunities to unveil the molecular adaptations supporting freeze tolerance in ectothermic vertebrates.
抗冻性，即生物体耐受内部冰晶形成的能力，是一些生活在寒冷环境中的变温动物所采用的一种显著的生存策略。然而，这种非凡适应的遗传基础在很大程度上尚不清楚。亚东鲑（Perccottus glenii）是已知的唯一具有抗冻性的鱼类物种，它可以在整个身体被冰冻在冰中的情况下越冬。在这里，我们对亚东鲑的染色体水平基因组进行了测序，并进行了比较基因组、转录组和代谢组学分析，以研究其抗冻结的生存策略。进化分析表明，亚东鲑与最接近的非耐寒相关物种大约在 1507 万年前分化，并经历了较高的蛋白质进化速率。转录组和代谢组数据鉴定了涉及低代谢、细胞应激反应和冷冻和解冻过程中冷冻保护剂积累的基因和代谢物的协调和组织特异性调节。一些基因显示出加速蛋白质序列进化或家族大小扩张的证据，这是对冷冻诱导应激的适应性反应。具体而言，与细胞骨架稳定性、冷冻保护剂合成、跨膜运输和神经保护适应相关的遗传变化被认为是有助于冷冻生存的潜在关键创新。我们的工作提供了有价值的资源和机会，以揭示支持变温脊椎动物抗冻性的分子适应。
