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高温胁迫反应:利用多组学方法深入了解美洲西鲱(Alosa sapidissima)的分子调控

High-temperature stress response: Insights into the molecular regulation of American shad (Alosa sapidissima) using a multi-omics approach.

作者信息

Luo Mingkun, Zhu Wenbin, Liang Zhengyuan, Feng Bingbing, Xie Xudong, Li Yulin, Liu Ying, Shi Xiulan, Fu Jianjun, Miao Linghong, Dong Zaijie

机构信息

Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Freshwater Fisheries Research Center of Chinese Academy of Fishery Sciences, Ministry of Agriculture and Rural Affairs, Wuxi, Jiangsu, China.

Wuxi Fisheries College, Nanjing Agricultural University, Wuxi, Jiangsu, China.

出版信息

Sci Total Environ. 2024 Mar 15;916:170329. doi: 10.1016/j.scitotenv.2024.170329. Epub 2024 Jan 26.

DOI:10.1016/j.scitotenv.2024.170329
PMID:38280591
Abstract

High temperature is an important abiotic stressor that limits the survival and growth of aquatic organisms. American shad (Alosa sapidissima), a migratory fish suitable for culturing at low temperatures, is known for its delicious taste and thus has high economic value. Studies concerning changes in A. sapidissima under high temperature are limited, especially at the gene expression and protein levels. High-temperature stress significantly reduced the survival rates and increased vacuolar degeneration and inflammatory infiltration in the gills and liver. High temperature increased the activities of SOD, CAT, and cortisol, with a trend of initial increase followed by decreases in MDA, ALP, and LDH, and irregular changes in T-AOC and Na-K-ATPase. Comprehensive analysis of the transcriptome, proteome, and metabolome of gills from fish treated with different culture temperatures (24, 27, and 30 °C) revealed that differentially expressed genes, proteins, and metabolites were highly enriched in pathways involved in protein digestion and absorption, protein processing in endoplasmic reticulum, metabolic pathways, and purine metabolism. Gene expression and protein profiles indicated that genes coding for antioxidants (i.e., cat and alpl) and members of the heat shock protein (i.e., HSP70, HSP90AA1, and HSP5) were significantly upregulated. Additionally, a conjoint analysis revealed that several key enzymes, including nucleoside diphosphate kinase 2, adenosine deaminase, and ectonucleoside triphosphate diphosphohydrolase 5/6 were altered, thereby affecting the metabolism of guanosine, guanine, and inosine. An interaction network further confirmed that levels of the essential amino acids DL-arginine and L-histidine were significantly reduced, and corticosterone levels were significantly increased, suggesting that A. sapidissima may be more dependent on amino acids for energy in vivo. Overall, this work suggests that living in a high-temperature environment leads to differential defense responses in fishes. The results provide novel perspectives for studying the molecular basis of adaptation to climate change in A. sapidissima and for genetic selection.

摘要

高温是一种重要的非生物胁迫因素,限制了水生生物的生存和生长。美洲西鲱(Alosa sapidissima)是一种适合在低温下养殖的洄游鱼类,因其味道鲜美而闻名,因此具有很高的经济价值。关于美洲西鲱在高温下变化的研究有限,尤其是在基因表达和蛋白质水平方面。高温胁迫显著降低了存活率,并增加了鳃和肝脏中的液泡变性和炎症浸润。高温增加了超氧化物歧化酶(SOD)、过氧化氢酶(CAT)和皮质醇的活性,丙二醛(MDA)、碱性磷酸酶(ALP)和乳酸脱氢酶(LDH)呈先升高后降低的趋势,总抗氧化能力(T-AOC)和钠钾ATP酶(Na-K-ATPase)则出现不规则变化。对在不同养殖温度(24、27和30°C)下处理的鱼类鳃的转录组、蛋白质组和代谢组进行综合分析发现,差异表达的基因、蛋白质和代谢物在参与蛋白质消化和吸收、内质网中的蛋白质加工、代谢途径和嘌呤代谢的途径中高度富集。基因表达和蛋白质谱表明,编码抗氧化剂的基因(即cat和alpl)以及热休克蛋白成员(即HSP70、HSP90AA1和HSP5)显著上调。此外,联合分析显示,包括核苷二磷酸激酶2、腺苷脱氨酶和胞外核苷三磷酸二磷酸水解酶5/6在内的几种关键酶发生了改变,从而影响了鸟苷、鸟嘌呤和肌苷的代谢。相互作用网络进一步证实,必需氨基酸DL-精氨酸和L-组氨酸的水平显著降低,皮质酮水平显著升高,这表明美洲西鲱在体内可能更依赖氨基酸获取能量。总体而言,这项研究表明生活在高温环境中会导致鱼类产生不同的防御反应。这些结果为研究美洲西鲱适应气候变化的分子基础以及遗传选择提供了新的视角。

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