Multi-omics analysis reveals the toxic mechanism of ammonia-enhanced Microcystis aeruginosa exposure causing liver fat deposition and muscle nutrient loss in zebrafish

Microcystis aeruginosa and ammonia pollution are two important environmental stress factors in water eutrophication. Herein, we simulated environmental conditions to investigate the effects of chronic exposure (single and combined) to M. aeruginosa and total ammonia nitrogen (TAN) on lipid metabolis...

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Published inJournal of hazardous materials Vol. 461; p. 132631
Main Authors Ou-Yang, Kang, Kuang, Yu, Yang, Hui, He, Ya, Wang, Liangmou, Wang, Xinyu, Li, Dapeng, Li, Li
Format Journal Article
LanguageEnglish
Published Elsevier B.V 05.01.2024
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Online AccessGet full text
ISSN0304-3894
1873-3336
1873-3336
DOI10.1016/j.jhazmat.2023.132631

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Abstract Microcystis aeruginosa and ammonia pollution are two important environmental stress factors in water eutrophication. Herein, we simulated environmental conditions to investigate the effects of chronic exposure (single and combined) to M. aeruginosa and total ammonia nitrogen (TAN) on lipid metabolism and muscle quality in zebrafish. Our results showed that M. aeruginosa and TAN significantly induced lipid deposition and tissue damage in the liver of zebrafish. Liver transcriptomic analysis revealed that M. aeruginosa and TAN disrupted the balance in lipid synthesis, decomposition, and transport, ultimately leading to hepatic lipid accumulation. Moreover, exposure to M. aeruginosa or TAN alone resulted in decreased crude protein content and increased lipid content in muscle, as well as disrupted muscle fatty acid composition. Metabolomic analysis of muscle revealed significant alterations in metabolites such as glycerolipids, glycerophospholipids and fatty acids. The co-exposure of M. aeruginosa and TAN had a more significant effect on liver lipid dysfunction and muscle quality deterioration in zebrafish. These findings provide valuable insights into the potential risks and hazards of M. aeruginosa and TAN in eutrophic water bodies subject to Microcystis blooms, and can help inform effective strategies for monitoring and managing these toxins in aquatic ecosystems. This current work uncovers new dangers of eutrophic water environments: M. aeruginosa exposure in the presence of ammonia can lead to increased liver lipid deposition and deteriorated muscle quality in zebrafish according to a multi-omics analysis. The study also identifies key genes (ppap2d and dgat2) responsible for the deterioration of muscle quality caused by liver lipid accumulation. These findings provide valuable insights into the potential risks and hazards of M. aeruginosa and ammonia in eutrophic water bodies subject to Microcystis blooms, and can help inform effective strategies for monitoring and managing these toxins in aquatic ecosystems. [Display omitted] •M. aeruginosa and ammonia disrupted the balance of lipid metabolism, leading to hepatic steatosis.•M. aeruginosa and ammonia deteriorated zebrafish muscle quality.•Ammonia enhances M. aeruginosa-induced lipid dysfunction and muscle quality deterioration.•Potential synergistic health impacts of MC-LR and ammonia should not be underestimated.
AbstractList Microcystis aeruginosa and ammonia pollution are two important environmental stress factors in water eutrophication. Herein, we simulated environmental conditions to investigate the effects of chronic exposure (single and combined) to M. aeruginosa and total ammonia nitrogen (TAN) on lipid metabolism and muscle quality in zebrafish. Our results showed that M. aeruginosa and TAN significantly induced lipid deposition and tissue damage in the liver of zebrafish. Liver transcriptomic analysis revealed that M. aeruginosa and TAN disrupted the balance in lipid synthesis, decomposition, and transport, ultimately leading to hepatic lipid accumulation. Moreover, exposure to M. aeruginosa or TAN alone resulted in decreased crude protein content and increased lipid content in muscle, as well as disrupted muscle fatty acid composition. Metabolomic analysis of muscle revealed significant alterations in metabolites such as glycerolipids, glycerophospholipids and fatty acids. The co-exposure of M. aeruginosa and TAN had a more significant effect on liver lipid dysfunction and muscle quality deterioration in zebrafish. These findings provide valuable insights into the potential risks and hazards of M. aeruginosa and TAN in eutrophic water bodies subject to Microcystis blooms, and can help inform effective strategies for monitoring and managing these toxins in aquatic ecosystems.Microcystis aeruginosa and ammonia pollution are two important environmental stress factors in water eutrophication. Herein, we simulated environmental conditions to investigate the effects of chronic exposure (single and combined) to M. aeruginosa and total ammonia nitrogen (TAN) on lipid metabolism and muscle quality in zebrafish. Our results showed that M. aeruginosa and TAN significantly induced lipid deposition and tissue damage in the liver of zebrafish. Liver transcriptomic analysis revealed that M. aeruginosa and TAN disrupted the balance in lipid synthesis, decomposition, and transport, ultimately leading to hepatic lipid accumulation. Moreover, exposure to M. aeruginosa or TAN alone resulted in decreased crude protein content and increased lipid content in muscle, as well as disrupted muscle fatty acid composition. Metabolomic analysis of muscle revealed significant alterations in metabolites such as glycerolipids, glycerophospholipids and fatty acids. The co-exposure of M. aeruginosa and TAN had a more significant effect on liver lipid dysfunction and muscle quality deterioration in zebrafish. These findings provide valuable insights into the potential risks and hazards of M. aeruginosa and TAN in eutrophic water bodies subject to Microcystis blooms, and can help inform effective strategies for monitoring and managing these toxins in aquatic ecosystems.
Microcystis aeruginosa and ammonia pollution are two important environmental stress factors in water eutrophication. Herein, we simulated environmental conditions to investigate the effects of chronic exposure (single and combined) to M. aeruginosa and total ammonia nitrogen (TAN) on lipid metabolism and muscle quality in zebrafish. Our results showed that M. aeruginosa and TAN significantly induced lipid deposition and tissue damage in the liver of zebrafish. Liver transcriptomic analysis revealed that M. aeruginosa and TAN disrupted the balance in lipid synthesis, decomposition, and transport, ultimately leading to hepatic lipid accumulation. Moreover, exposure to M. aeruginosa or TAN alone resulted in decreased crude protein content and increased lipid content in muscle, as well as disrupted muscle fatty acid composition. Metabolomic analysis of muscle revealed significant alterations in metabolites such as glycerolipids, glycerophospholipids and fatty acids. The co-exposure of M. aeruginosa and TAN had a more significant effect on liver lipid dysfunction and muscle quality deterioration in zebrafish. These findings provide valuable insights into the potential risks and hazards of M. aeruginosa and TAN in eutrophic water bodies subject to Microcystis blooms, and can help inform effective strategies for monitoring and managing these toxins in aquatic ecosystems. This current work uncovers new dangers of eutrophic water environments: M. aeruginosa exposure in the presence of ammonia can lead to increased liver lipid deposition and deteriorated muscle quality in zebrafish according to a multi-omics analysis. The study also identifies key genes (ppap2d and dgat2) responsible for the deterioration of muscle quality caused by liver lipid accumulation. These findings provide valuable insights into the potential risks and hazards of M. aeruginosa and ammonia in eutrophic water bodies subject to Microcystis blooms, and can help inform effective strategies for monitoring and managing these toxins in aquatic ecosystems. [Display omitted] •M. aeruginosa and ammonia disrupted the balance of lipid metabolism, leading to hepatic steatosis.•M. aeruginosa and ammonia deteriorated zebrafish muscle quality.•Ammonia enhances M. aeruginosa-induced lipid dysfunction and muscle quality deterioration.•Potential synergistic health impacts of MC-LR and ammonia should not be underestimated.
Microcystis aeruginosa and ammonia pollution are two important environmental stress factors in water eutrophication. Herein, we simulated environmental conditions to investigate the effects of chronic exposure (single and combined) to M. aeruginosa and total ammonia nitrogen (TAN) on lipid metabolism and muscle quality in zebrafish. Our results showed that M. aeruginosa and TAN significantly induced lipid deposition and tissue damage in the liver of zebrafish. Liver transcriptomic analysis revealed that M. aeruginosa and TAN disrupted the balance in lipid synthesis, decomposition, and transport, ultimately leading to hepatic lipid accumulation. Moreover, exposure to M. aeruginosa or TAN alone resulted in decreased crude protein content and increased lipid content in muscle, as well as disrupted muscle fatty acid composition. Metabolomic analysis of muscle revealed significant alterations in metabolites such as glycerolipids, glycerophospholipids and fatty acids. The co-exposure of M. aeruginosa and TAN had a more significant effect on liver lipid dysfunction and muscle quality deterioration in zebrafish. These findings provide valuable insights into the potential risks and hazards of M. aeruginosa and TAN in eutrophic water bodies subject to Microcystis blooms, and can help inform effective strategies for monitoring and managing these toxins in aquatic ecosystems.
ArticleNumber 132631
Author Li, Li
Ou-Yang, Kang
Li, Dapeng
Wang, Xinyu
Kuang, Yu
He, Ya
Wang, Liangmou
Yang, Hui
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  email: foreverlili78@mail.hzau.edu.cn
  organization: College of Fisheries, Huazhong Agricultural University, Wuhan 430070, P.R. China
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Keywords Ammonia
Microcystis aeruginosa
Lipid metabolism
Multi-omics analysis
Muscle quality
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Snippet Microcystis aeruginosa and ammonia pollution are two important environmental stress factors in water eutrophication. Herein, we simulated environmental...
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SubjectTerms Ammonia
ammonium nitrogen
chronic exposure
crude protein
Danio rerio
eutrophication
fatty acid composition
glycerophospholipids
lipid content
Lipid metabolism
liver
metabolites
metabolomics
Microcystis aeruginosa
Multi-omics analysis
multiomics
Muscle quality
muscles
pollution
toxicity
transcriptomics
Title Multi-omics analysis reveals the toxic mechanism of ammonia-enhanced Microcystis aeruginosa exposure causing liver fat deposition and muscle nutrient loss in zebrafish
URI https://dx.doi.org/10.1016/j.jhazmat.2023.132631
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