Integrated physiological, transcriptome and metabolome analyses of the hepatopancreas of the female swimming crab Portunus trituberculatus under ammonia exposure

Ammonia is a common environmental pollutant in aquatic ecosystem and is also a significant concern in closed aquaculture systems. The threat of ammonia has been increasing with rising anthropogenic activities including intensified aquaculture. In this study, we aimed to investigate ammonia toxicity...

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Autores principales: Xianliang Meng, Nishad Jayasundara, Jingyan Zhang, Xianyun Ren, Baoquan Gao, Jian Li, Ping Liu
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Publicado: Elsevier 2021
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spelling oai:doaj.org-article:d5b2ce68bfdf453b8404de82d96a022a2021-11-26T04:23:35ZIntegrated physiological, transcriptome and metabolome analyses of the hepatopancreas of the female swimming crab Portunus trituberculatus under ammonia exposure0147-651310.1016/j.ecoenv.2021.113026https://doaj.org/article/d5b2ce68bfdf453b8404de82d96a022a2021-12-01T00:00:00Zhttp://www.sciencedirect.com/science/article/pii/S0147651321011386https://doaj.org/toc/0147-6513Ammonia is a common environmental pollutant in aquatic ecosystem and is also a significant concern in closed aquaculture systems. The threat of ammonia has been increasing with rising anthropogenic activities including intensified aquaculture. In this study, we aimed to investigate ammonia toxicity and metabolism mechanisms in the hepatopancreas, a major organ for Vitellogenin (Vtg) synthesis and defending against ammonia stress, of female swimming crab Portunus trituberculatus which is an important fishery and aquaculture species, by integrating physiological, transcriptome and metabolome analyses. The results revealed that ammonia exposure (10 mg/L, an environmentally relevant concentration) resulted in a remarkable reduction in vtg expression and depression of multiple signaling pathways for reproductive regulators including methyl farnesoate, ecdysone and neuroparsin, demonstrating for the first time that ammonia impairs swimming crab female reproduction. In addition, a number of important genes and metabolites in glycolysis, the Krebs cycle, fatty acid β-oxidation and synthesis were significantly downregulated, indicating that changes in ammonia levels lead to a general depression of energy metabolism in hepatopancreas. After ammonia exposure, an increased level of urea and a reduction of amino acid catabolism were observed in hepatopancreas, suggesting that urea cycle was utilized to biotransform ammonia, and amino acid catabolism was decreased to reduce endogenous ammonia generation. Furthermore, antioxidant systems were altered following ammonia exposure, which was accompanied by proteins and lipid oxidations, as well as cellular apoptosis. These results indicate that ammonia leads to metabolic suppression, oxidative stress and apoptosis in P. trituberculatus hepatopancreas. The findings improve the understanding for the mechanisms of ammonia toxicity and metabolism in P. trituberculatus, and provide valuable information for assessing potential ecological risk of environmental ammonia and improving aquaculture management.Xianliang MengNishad JayasundaraJingyan ZhangXianyun RenBaoquan GaoJian LiPing LiuElsevierarticleAmmoniaCrabTranscriptomeMetabolomePhysiologyVitellogenesisEnvironmental pollutionTD172-193.5Environmental sciencesGE1-350ENEcotoxicology and Environmental Safety, Vol 228, Iss , Pp 113026- (2021)
institution DOAJ
collection DOAJ
language EN
topic Ammonia
Crab
Transcriptome
Metabolome
Physiology
Vitellogenesis
Environmental pollution
TD172-193.5
Environmental sciences
GE1-350
spellingShingle Ammonia
Crab
Transcriptome
Metabolome
Physiology
Vitellogenesis
Environmental pollution
TD172-193.5
Environmental sciences
GE1-350
Xianliang Meng
Nishad Jayasundara
Jingyan Zhang
Xianyun Ren
Baoquan Gao
Jian Li
Ping Liu
Integrated physiological, transcriptome and metabolome analyses of the hepatopancreas of the female swimming crab Portunus trituberculatus under ammonia exposure
description Ammonia is a common environmental pollutant in aquatic ecosystem and is also a significant concern in closed aquaculture systems. The threat of ammonia has been increasing with rising anthropogenic activities including intensified aquaculture. In this study, we aimed to investigate ammonia toxicity and metabolism mechanisms in the hepatopancreas, a major organ for Vitellogenin (Vtg) synthesis and defending against ammonia stress, of female swimming crab Portunus trituberculatus which is an important fishery and aquaculture species, by integrating physiological, transcriptome and metabolome analyses. The results revealed that ammonia exposure (10 mg/L, an environmentally relevant concentration) resulted in a remarkable reduction in vtg expression and depression of multiple signaling pathways for reproductive regulators including methyl farnesoate, ecdysone and neuroparsin, demonstrating for the first time that ammonia impairs swimming crab female reproduction. In addition, a number of important genes and metabolites in glycolysis, the Krebs cycle, fatty acid β-oxidation and synthesis were significantly downregulated, indicating that changes in ammonia levels lead to a general depression of energy metabolism in hepatopancreas. After ammonia exposure, an increased level of urea and a reduction of amino acid catabolism were observed in hepatopancreas, suggesting that urea cycle was utilized to biotransform ammonia, and amino acid catabolism was decreased to reduce endogenous ammonia generation. Furthermore, antioxidant systems were altered following ammonia exposure, which was accompanied by proteins and lipid oxidations, as well as cellular apoptosis. These results indicate that ammonia leads to metabolic suppression, oxidative stress and apoptosis in P. trituberculatus hepatopancreas. The findings improve the understanding for the mechanisms of ammonia toxicity and metabolism in P. trituberculatus, and provide valuable information for assessing potential ecological risk of environmental ammonia and improving aquaculture management.
format article
author Xianliang Meng
Nishad Jayasundara
Jingyan Zhang
Xianyun Ren
Baoquan Gao
Jian Li
Ping Liu
author_facet Xianliang Meng
Nishad Jayasundara
Jingyan Zhang
Xianyun Ren
Baoquan Gao
Jian Li
Ping Liu
author_sort Xianliang Meng
title Integrated physiological, transcriptome and metabolome analyses of the hepatopancreas of the female swimming crab Portunus trituberculatus under ammonia exposure
title_short Integrated physiological, transcriptome and metabolome analyses of the hepatopancreas of the female swimming crab Portunus trituberculatus under ammonia exposure
title_full Integrated physiological, transcriptome and metabolome analyses of the hepatopancreas of the female swimming crab Portunus trituberculatus under ammonia exposure
title_fullStr Integrated physiological, transcriptome and metabolome analyses of the hepatopancreas of the female swimming crab Portunus trituberculatus under ammonia exposure
title_full_unstemmed Integrated physiological, transcriptome and metabolome analyses of the hepatopancreas of the female swimming crab Portunus trituberculatus under ammonia exposure
title_sort integrated physiological, transcriptome and metabolome analyses of the hepatopancreas of the female swimming crab portunus trituberculatus under ammonia exposure
publisher Elsevier
publishDate 2021
url https://doaj.org/article/d5b2ce68bfdf453b8404de82d96a022a
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