Integrated analysis of biochemical, transcriptomic, and metabolomic response mechanisms in Ussuri catfish (Pseudobagrus ussuriensis) under acute heat stress

Fish metabolism, growth, development, and physiological conditions are highly sensitive to fluctuations in water temperature. The Ussuri catfish (Pseudobagrus ussuriensis) is an important native economic species in China. However, research on heat stress in P. ussuriensis, particularly concerning ge...

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Main Authors: Qing Liu, Yang Cao, Ruyi Hu, Libo Gu, Lirong Yang, Yu Liu, Weiwei Wang, Liang Xiao, Bugao Li
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651324016397
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author Qing Liu
Yang Cao
Ruyi Hu
Libo Gu
Lirong Yang
Yu Liu
Weiwei Wang
Liang Xiao
Bugao Li
author_facet Qing Liu
Yang Cao
Ruyi Hu
Libo Gu
Lirong Yang
Yu Liu
Weiwei Wang
Liang Xiao
Bugao Li
author_sort Qing Liu
collection DOAJ
description Fish metabolism, growth, development, and physiological conditions are highly sensitive to fluctuations in water temperature. The Ussuri catfish (Pseudobagrus ussuriensis) is an important native economic species in China. However, research on heat stress in P. ussuriensis, particularly concerning gene expression and metabolites, remains limited. In this study, we conducted histological observations, biochemical measurements, transcriptomic analysis, and metabolomic analysis on liver tissue from a control group (22 ℃), an acute heat stress group (34 ℃, with samples taken at 0, 3, 6, 12, and 24 h), and a recovery group (sampled 24 h after recovery to 22 ℃). Histopathological analysis showed that liver damage worsened with the duration of heat stress. Biochemical results indicated that acute heat stress significantly impacted the activities of superoxide dismutase, catalase, and alanine aminotransferase, as well as the levels of glutathione, malondialdehyde, and total antioxidant capacity, with alterations remaining even after temperature recovery. Transcriptomic and metabolomic analyses revealed that compared to the control group, 3482, 800, 980, and 1479 differentially expressed genes (DEGs) were detected at 0, 6, and 24 h of acute heat stress and at 24 h post-recovery, respectively. Similarly, 114, 151, 365, and 326 differentially expressed metabolites (DEMs), respectively, were detected at the same time points. Furthermore, when comparing 24 h of heat stress with 24 h of recovery, 1279 DEGs and 157 DEMs were identified. Functional enrichment analysis revealed that these DEGs and DEMs were significantly enriched in key pathways, such as endoplasmic reticulum protein processing and glutathione metabolism, with significant changes continuing into the recovery phase. Additionally, substantial alterations in the expression levels of amino acids, sugars, and lipids were observed during heat stress. These findings provide valuable insights into the defense mechanisms of fish under high-temperature stress and lay a theoretical foundation for breeding heat-resistant P. ussuriensis strains, as well as improving sustainable aquaculture management.
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spelling doaj-art-de8df819b53b450da2dd9666cb863bf22025-02-12T05:29:47ZengElsevierEcotoxicology and Environmental Safety0147-65132025-01-01290117563Integrated analysis of biochemical, transcriptomic, and metabolomic response mechanisms in Ussuri catfish (Pseudobagrus ussuriensis) under acute heat stressQing Liu0Yang Cao1Ruyi Hu2Libo Gu3Lirong Yang4Yu Liu5Weiwei Wang6Liang Xiao7Bugao Li8College of Animal Science, Shanxi Agricultural University, Jinzhong 030800, China; Shanxi Key Laboratory of Animal Genetics Resource Utilization and Breeding, Jinzhong 030800, China; Corresponding authors at: College of Animal Science, Shanxi Agricultural University, Jinzhong 030800, China.College of Animal Science, Shanxi Agricultural University, Jinzhong 030800, China; Shanxi Key Laboratory of Animal Genetics Resource Utilization and Breeding, Jinzhong 030800, ChinaCollege of Animal Science, Shanxi Agricultural University, Jinzhong 030800, China; Shanxi Key Laboratory of Animal Genetics Resource Utilization and Breeding, Jinzhong 030800, ChinaCollege of Animal Science, Shanxi Agricultural University, Jinzhong 030800, China; Shanxi Key Laboratory of Animal Genetics Resource Utilization and Breeding, Jinzhong 030800, ChinaCollege of Animal Science, Shanxi Agricultural University, Jinzhong 030800, China; Shanxi Key Laboratory of Animal Genetics Resource Utilization and Breeding, Jinzhong 030800, ChinaCollege of Animal Science, Shanxi Agricultural University, Jinzhong 030800, China; Shanxi Key Laboratory of Animal Genetics Resource Utilization and Breeding, Jinzhong 030800, ChinaCollege of Animal Science, Shanxi Agricultural University, Jinzhong 030800, ChinaFaculty of Naval Medicine, Naval Medical University, Shanghai 200433, China; Corresponding author.College of Animal Science, Shanxi Agricultural University, Jinzhong 030800, China; Shanxi Key Laboratory of Animal Genetics Resource Utilization and Breeding, Jinzhong 030800, China; Corresponding authors at: College of Animal Science, Shanxi Agricultural University, Jinzhong 030800, China.Fish metabolism, growth, development, and physiological conditions are highly sensitive to fluctuations in water temperature. The Ussuri catfish (Pseudobagrus ussuriensis) is an important native economic species in China. However, research on heat stress in P. ussuriensis, particularly concerning gene expression and metabolites, remains limited. In this study, we conducted histological observations, biochemical measurements, transcriptomic analysis, and metabolomic analysis on liver tissue from a control group (22 ℃), an acute heat stress group (34 ℃, with samples taken at 0, 3, 6, 12, and 24 h), and a recovery group (sampled 24 h after recovery to 22 ℃). Histopathological analysis showed that liver damage worsened with the duration of heat stress. Biochemical results indicated that acute heat stress significantly impacted the activities of superoxide dismutase, catalase, and alanine aminotransferase, as well as the levels of glutathione, malondialdehyde, and total antioxidant capacity, with alterations remaining even after temperature recovery. Transcriptomic and metabolomic analyses revealed that compared to the control group, 3482, 800, 980, and 1479 differentially expressed genes (DEGs) were detected at 0, 6, and 24 h of acute heat stress and at 24 h post-recovery, respectively. Similarly, 114, 151, 365, and 326 differentially expressed metabolites (DEMs), respectively, were detected at the same time points. Furthermore, when comparing 24 h of heat stress with 24 h of recovery, 1279 DEGs and 157 DEMs were identified. Functional enrichment analysis revealed that these DEGs and DEMs were significantly enriched in key pathways, such as endoplasmic reticulum protein processing and glutathione metabolism, with significant changes continuing into the recovery phase. Additionally, substantial alterations in the expression levels of amino acids, sugars, and lipids were observed during heat stress. These findings provide valuable insights into the defense mechanisms of fish under high-temperature stress and lay a theoretical foundation for breeding heat-resistant P. ussuriensis strains, as well as improving sustainable aquaculture management.http://www.sciencedirect.com/science/article/pii/S0147651324016397Ussuri catfish (Pseudobagrus ussuriensis)Acute heat stressLiver diseaseHeat shock protein (HSP)Energy metabolism
spellingShingle Qing Liu
Yang Cao
Ruyi Hu
Libo Gu
Lirong Yang
Yu Liu
Weiwei Wang
Liang Xiao
Bugao Li
Integrated analysis of biochemical, transcriptomic, and metabolomic response mechanisms in Ussuri catfish (Pseudobagrus ussuriensis) under acute heat stress
Ecotoxicology and Environmental Safety
Ussuri catfish (Pseudobagrus ussuriensis)
Acute heat stress
Liver disease
Heat shock protein (HSP)
Energy metabolism
title Integrated analysis of biochemical, transcriptomic, and metabolomic response mechanisms in Ussuri catfish (Pseudobagrus ussuriensis) under acute heat stress
title_full Integrated analysis of biochemical, transcriptomic, and metabolomic response mechanisms in Ussuri catfish (Pseudobagrus ussuriensis) under acute heat stress
title_fullStr Integrated analysis of biochemical, transcriptomic, and metabolomic response mechanisms in Ussuri catfish (Pseudobagrus ussuriensis) under acute heat stress
title_full_unstemmed Integrated analysis of biochemical, transcriptomic, and metabolomic response mechanisms in Ussuri catfish (Pseudobagrus ussuriensis) under acute heat stress
title_short Integrated analysis of biochemical, transcriptomic, and metabolomic response mechanisms in Ussuri catfish (Pseudobagrus ussuriensis) under acute heat stress
title_sort integrated analysis of biochemical transcriptomic and metabolomic response mechanisms in ussuri catfish pseudobagrus ussuriensis under acute heat stress
topic Ussuri catfish (Pseudobagrus ussuriensis)
Acute heat stress
Liver disease
Heat shock protein (HSP)
Energy metabolism
url http://www.sciencedirect.com/science/article/pii/S0147651324016397
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