Metabolic response of longitudinal muscles to acute hypoxia in sea cucumber Apostichopus japonicus (Selenka): A metabolome integrated analysis

Abstract

Hypoxia is a severe problem in aquatic environments worldwide and has caused mass mortality of sea cucumbers (& other species) for decades, seriously affecting the sustainable development of aquaculture. Investigations of the metabolic disruptions and biochemical responses associated with acute hypoxia stress in sea cucumbers can provide a theoretical basis and guidance for improving aquaculture. A metabolomics approach to characterize changes in the profiles of endogenous small molecules in response to acute hypoxia can help to identify the main underlying causes of metabolic damage and potentially suggest solutions to alleviate to improve viability. The current study uses liquid chromatography-mass spectrometry (LC-MS) and multivariate analysis methods to evaluate the metabolic profile of longitudinal muscles from A. japonicus exposed to acute hypoxia stress (by bubbling the aquaria water with nitrogen aeration to decrease dissolved oxygen to 2 mg/L in 2 min) for 6 or 24 h (experimental groups EG6 or EG24) and control group (CG, n = 10, respectively). The results showed that 29 and 62 metabolites were influenced significantly in EG6 and EG24, respectively, mainly including lipids, glycosides and their derivatives. Levels of most lipids (fatty acids, glycerolipids, glycerophospholipids, sphingolipids and sterols) were elevated in both experimental groups, and increased with elongation of hypoxia, implying that the homeostasis of synthesis and degradation of lipids and their derivatives was strongly affected by hypoxia stress. Pathway enrichment analysis was performed to further assess the importance of differential metabolite expression to the development of the A. japonicus response to hypoxia, showing that 4 (fatty acid biosynthesis, d-glutamine and d-glutamate metabolism, glycolysis/gluconeogenesis, glyoxylate and dicarboxylate metabolism) and 2 (steroid biosynthesis, longevity regulating pathway) pathways were markedly enriched in EG6 and EG24, respectively. These results suggested that fatty acid synthesis was strengthened significantly in both treatment groups, and the degree was higher in EG24 than in EG6, providing valuable information towards understanding the special adaptive mechanism of A. japonicus to hypoxia stress.

Keywords: Apostichopus japonicus; Dissolved oxygen; Fatty acids; Hypoxia; LC-MS; Lipid metabolism; Metabolomics.