A study on the hepatic response to heat stress in Gymnocypris eckloni through an approach combining metabolomic and transcriptomic profiling

Gymnocypris eckloni, an economically important cold-water fish widely cultivated in southwest China, is at increased risk of prolonged exposure to heat stress owing to persistent high temperatures in summer, extreme climate changes, and expansion of factory farming. In this study, G. eckloni was sub...

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Main Authors: Chaowei Zhou, Yuting Duan, Junting Li, Suxing Fu, Shuhao Bai, Yutong Zhuang, Shidong Liu, Hejiao Li, Yinhua Zhou, Qiming Wang, Jian Shen, Rongzhu Zhou, Luo Lei, Haiping Liu
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Aquaculture Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352513424004800
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author Chaowei Zhou
Yuting Duan
Junting Li
Suxing Fu
Shuhao Bai
Yutong Zhuang
Shidong Liu
Hejiao Li
Yinhua Zhou
Qiming Wang
Jian Shen
Rongzhu Zhou
Luo Lei
Haiping Liu
author_facet Chaowei Zhou
Yuting Duan
Junting Li
Suxing Fu
Shuhao Bai
Yutong Zhuang
Shidong Liu
Hejiao Li
Yinhua Zhou
Qiming Wang
Jian Shen
Rongzhu Zhou
Luo Lei
Haiping Liu
author_sort Chaowei Zhou
collection DOAJ
description Gymnocypris eckloni, an economically important cold-water fish widely cultivated in southwest China, is at increased risk of prolonged exposure to heat stress owing to persistent high temperatures in summer, extreme climate changes, and expansion of factory farming. In this study, G. eckloni was subjected to both chronic and acute heat stress, with subsequent analysis focusing on changes in the pathological and physiological characteristics and transcriptomic and metabolic responses of the liver to high temperature. The results revealed heat stress-induced damage to liver tissues, lipid accumulation and mitochondrial abnormalities in hepatocytes, and an increased number of apoptotic cells, with the damage being more severe under acute heat stress conditions. Assessment of biochemical indices showed that the antioxidant enzyme catalase (CAT) was activated in response to oxidative stress and energy demands increased following heat stress. Transcriptomic analysis showed significant enrichment in the protein processing in the endoplasmic reticulum pathway, along with upregulation of key genes associated with protein degradation (hsp40, hsp70, hsp90, ero1l, and pdia4) and activation of the unfolded protein response (UPR), which effectively reduces or clears the accumulation of misfolded proteins to combat stress. Most identified differential metabolites were associated with amino acid and lipid metabolism under heat stress. Notably, integrated transcriptomic and metabolomic analysis suggested that tryptophan metabolism played an important role in the adaptation of G. eckloni to chronic heat stress. These findings improve the understanding of the mechanisms through which G. eckloni adapts to high temperatures, providing a valuable foundation and novel avenues for developing strategies to alleviate the effects of heat stress and improve the outcomes of aquaculture.
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spelling doaj-art-473b2ca8145540c0a46d60011b6dca352025-08-20T02:51:30ZengElsevierAquaculture Reports2352-51342024-12-013910239210.1016/j.aqrep.2024.102392A study on the hepatic response to heat stress in Gymnocypris eckloni through an approach combining metabolomic and transcriptomic profilingChaowei Zhou0Yuting Duan1Junting Li2Suxing Fu3Shuhao Bai4Yutong Zhuang5Shidong Liu6Hejiao Li7Yinhua Zhou8Qiming Wang9Jian Shen10Rongzhu Zhou11Luo Lei12Haiping Liu13Integrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City & Southwest University, Chongqing, China; College of Fisheries, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City & Southwest University, Chongqing, China; College of Fisheries, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City & Southwest University, Chongqing, China; College of Fisheries, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City & Southwest University, Chongqing, China; College of Fisheries, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City & Southwest University, Chongqing, China; College of Fisheries, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City & Southwest University, Chongqing, China; College of Fisheries, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City & Southwest University, Chongqing, China; College of Fisheries, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City & Southwest University, Chongqing, China; College of Fisheries, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City & Southwest University, Chongqing, China; College of Fisheries, Southwest University, Chongqing 400715, ChinaDepartment of Agriculture and Rural Affairs of the Xizang Autonomous Region, Xizang 850000, ChinaHuadian Xizang Energy Co., Ltd., Xizang 851414, ChinaNational Animal Husbandry Services, Beijin 100125, China; Correspondence to: College of Fisheries, Southwest University, Chongqing, China.Integrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City & Southwest University, Chongqing, China; College of Fisheries, Southwest University, Chongqing 400715, China; Correspondence to: College of Fisheries, Southwest University, Chongqing, China.Integrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City & Southwest University, Chongqing, China; Correspondence to: College of Fisheries, Southwest University, Chongqing, China.Gymnocypris eckloni, an economically important cold-water fish widely cultivated in southwest China, is at increased risk of prolonged exposure to heat stress owing to persistent high temperatures in summer, extreme climate changes, and expansion of factory farming. In this study, G. eckloni was subjected to both chronic and acute heat stress, with subsequent analysis focusing on changes in the pathological and physiological characteristics and transcriptomic and metabolic responses of the liver to high temperature. The results revealed heat stress-induced damage to liver tissues, lipid accumulation and mitochondrial abnormalities in hepatocytes, and an increased number of apoptotic cells, with the damage being more severe under acute heat stress conditions. Assessment of biochemical indices showed that the antioxidant enzyme catalase (CAT) was activated in response to oxidative stress and energy demands increased following heat stress. Transcriptomic analysis showed significant enrichment in the protein processing in the endoplasmic reticulum pathway, along with upregulation of key genes associated with protein degradation (hsp40, hsp70, hsp90, ero1l, and pdia4) and activation of the unfolded protein response (UPR), which effectively reduces or clears the accumulation of misfolded proteins to combat stress. Most identified differential metabolites were associated with amino acid and lipid metabolism under heat stress. Notably, integrated transcriptomic and metabolomic analysis suggested that tryptophan metabolism played an important role in the adaptation of G. eckloni to chronic heat stress. These findings improve the understanding of the mechanisms through which G. eckloni adapts to high temperatures, providing a valuable foundation and novel avenues for developing strategies to alleviate the effects of heat stress and improve the outcomes of aquaculture.http://www.sciencedirect.com/science/article/pii/S2352513424004800Gymnocypris eckloniHeat stressTranscriptome analysisMetabolome analysis
spellingShingle Chaowei Zhou
Yuting Duan
Junting Li
Suxing Fu
Shuhao Bai
Yutong Zhuang
Shidong Liu
Hejiao Li
Yinhua Zhou
Qiming Wang
Jian Shen
Rongzhu Zhou
Luo Lei
Haiping Liu
A study on the hepatic response to heat stress in Gymnocypris eckloni through an approach combining metabolomic and transcriptomic profiling
Aquaculture Reports
Gymnocypris eckloni
Heat stress
Transcriptome analysis
Metabolome analysis
title A study on the hepatic response to heat stress in Gymnocypris eckloni through an approach combining metabolomic and transcriptomic profiling
title_full A study on the hepatic response to heat stress in Gymnocypris eckloni through an approach combining metabolomic and transcriptomic profiling
title_fullStr A study on the hepatic response to heat stress in Gymnocypris eckloni through an approach combining metabolomic and transcriptomic profiling
title_full_unstemmed A study on the hepatic response to heat stress in Gymnocypris eckloni through an approach combining metabolomic and transcriptomic profiling
title_short A study on the hepatic response to heat stress in Gymnocypris eckloni through an approach combining metabolomic and transcriptomic profiling
title_sort study on the hepatic response to heat stress in gymnocypris eckloni through an approach combining metabolomic and transcriptomic profiling
topic Gymnocypris eckloni
Heat stress
Transcriptome analysis
Metabolome analysis
url http://www.sciencedirect.com/science/article/pii/S2352513424004800
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