Long-term thermal acclimation enhances heat resistance of Hong Kong catfish (Clarias fuscus) by modulating gill tissue structure, antioxidant capacity and immune metabolic pathways

Cunyu Duan; Dayan Zhou; Ruiqing Feng; Xiaolong Li; Lei Yang; Xinyi Li; Guangli Li; Huapu Chen; Yu Liao; Changxu Tian

Ecotoxicology and Environmental Safety (Oct 2024)

Long-term thermal acclimation enhances heat resistance of Hong Kong catfish (Clarias fuscus) by modulating gill tissue structure, antioxidant capacity and immune metabolic pathways

Cunyu Duan,
Dayan Zhou,
Ruiqing Feng,
Xiaolong Li,
Lei Yang,
Xinyi Li,
Guangli Li,
Huapu Chen,
Yu Liao,
Changxu Tian

Affiliations

Cunyu Duan: Fisheries College, Guangdong Ocean University, Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Guangdong Provincial Engineering Laboratory for Mariculture Organism Breeding, Guangdong Provincial Key Lab of Pathogenic Biology and Epidemiology for Aquatic Economic Animals, Zhanjiang 524088, China
Dayan Zhou: Guangxi Introduction and Breeding Center of Aquaculture, Nanning 530001, China
Ruiqing Feng: Fisheries College, Guangdong Ocean University, Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Guangdong Provincial Engineering Laboratory for Mariculture Organism Breeding, Guangdong Provincial Key Lab of Pathogenic Biology and Epidemiology for Aquatic Economic Animals, Zhanjiang 524088, China
Xiaolong Li: Fisheries College, Guangdong Ocean University, Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Guangdong Provincial Engineering Laboratory for Mariculture Organism Breeding, Guangdong Provincial Key Lab of Pathogenic Biology and Epidemiology for Aquatic Economic Animals, Zhanjiang 524088, China
Lei Yang: Fisheries College, Guangdong Ocean University, Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Guangdong Provincial Engineering Laboratory for Mariculture Organism Breeding, Guangdong Provincial Key Lab of Pathogenic Biology and Epidemiology for Aquatic Economic Animals, Zhanjiang 524088, China
Xinyi Li: Fisheries College, Guangdong Ocean University, Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Guangdong Provincial Engineering Laboratory for Mariculture Organism Breeding, Guangdong Provincial Key Lab of Pathogenic Biology and Epidemiology for Aquatic Economic Animals, Zhanjiang 524088, China
Guangli Li: Fisheries College, Guangdong Ocean University, Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Guangdong Provincial Engineering Laboratory for Mariculture Organism Breeding, Guangdong Provincial Key Lab of Pathogenic Biology and Epidemiology for Aquatic Economic Animals, Zhanjiang 524088, China
Huapu Chen: Fisheries College, Guangdong Ocean University, Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Guangdong Provincial Engineering Laboratory for Mariculture Organism Breeding, Guangdong Provincial Key Lab of Pathogenic Biology and Epidemiology for Aquatic Economic Animals, Zhanjiang 524088, China
Yu Liao: Guangxi Introduction and Breeding Center of Aquaculture, Nanning 530001, China
Changxu Tian: Fisheries College, Guangdong Ocean University, Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Guangdong Provincial Engineering Laboratory for Mariculture Organism Breeding, Guangdong Provincial Key Lab of Pathogenic Biology and Epidemiology for Aquatic Economic Animals, Zhanjiang 524088, China; Correspondence to: Fisheries College, Guangdong Ocean University, Zhanjiang 524088, China.

Journal volume & issue: Vol. 284
p. 116930

Abstract

Read online

The rapid temperature changes caused by global warming significantly challenge fish survival by affecting various biological processes. Fish generally mitigate stress through physiological plasticity, but when temperature changes exceed their tolerance limits, even adaptable species like Siluriformes can experience internal disruptions. This study investigates the effects of extreme thermal climate on Hong Kong catfish (Clarias fuscus), native to tropical and subtropical regions. C. fuscus were exposed to normal temperature (NT, 26 ℃) or high temperature (HT, 34 ℃) condition for 90 days. Subsequently, histological, biochemical, and transcriptomic changes in gill tissue were observed after exposure to acute high temperatures (34 ℃) and subsequent temperature recovery (26 ℃). Histological analysis revealed that C. fuscus in the HT group exhibited less impact from sudden temperature shifts compared to the NT group, as they adapted by reducing the interlamellar cell mass (ILCM) and lamellae thickness (LT) of gill tissue, thereby mitigating the aftermath of acute heat shock. Biochemical analysis showed that catalase (CAT) activity in the high temperature group continued to increase, while malondialdehyde (MDA) levels decreased, suggesting establishment of a new oxidative balance and enhanced environmental adaptability. Transcriptome analysis identified 520 and 463 differentially expressed genes in the NT and HT groups, respectively, in response to acute temperature changes. Enrichment analysis highlighted that in response to acute temperature changes, the NT group inhibited apoptosis and ferroptosis by regulating the activity of alox12, gclc, and hmox1a, thereby attenuating the adverse effects of heat stress. Conversely, the HT group increased the activity of pfkma and pkma to provide sufficient energy for tissue repair. The higher degree of heat shock protein (Hsp) response in NT group also indicated more severe heat stress injury. These findings demonstrate alterations in gill tissue structure, regulation of oxidative balance, and the response of immune metabolic pathways to acute temperature fluctuations in C. fuscus following thermal exposure, suggesting potential avenues for further exploration into the thermal tolerance plasticity of fish adapting to global warming.

Published in Ecotoxicology and Environmental Safety

ISSN: 0147-6513 (Print); 1090-2414 (Online)
Publisher: Elsevier
Country of publisher: United States
LCC subjects: Technology: Environmental technology. Sanitary engineering: Environmental pollution; Geography. Anthropology. Recreation: Environmental sciences
Website: https://www.journals.elsevier.com/ecotoxicology-and-environmental-safety

About the journal

Abstract

Keywords