Abstract
Hypoxia represents a major physiological challenge for prawns and is a problem in aquaculture. Therefore, an understanding of the metabolic response mechanism of economically important prawn species to hypoxia and re-oxygenation is essential. However, little is known about the intrinsic mechanisms by which the oriental river prawn Macrobrachium nipponense copes with hypoxia at the metabolic level. In this study, we conducted gas chromatography-mass spectrometry-based metabolomics studies and assays of energy metabolism-related parameters to investigate the metabolic mechanisms in the hepatopancreas of M. nipponense in response to 2.0 O2/L hypoxia for 6 and 24 h, and reoxygenation for 6 h following hypoxia for 24 h. Prawns under hypoxic stress displayed higher glycolysis-related enzyme activities and lower mRNA expression levels of aerobic respiratory enzymes than those in the normoxic control group, and those parameters returned to control levels in the reoxygenated group. Our results showed that hypoxia induced significant metabolomic alterations in the prawn hepatopancreas within 24 h. The main metabolic alterations were depletion of amino acids and 2-hydroxybutanoic acid and accumulation of lactate. Further, the findings indicated that hypoxia disturbed energy metabolism and induced antioxidant defense regulation in prawns. Surprisingly, recovery from hypoxia (i.e., reoxygenation) significantly affected 25 metabolites. Some amino acids (valine, leucine, isoleucine, lysine, glutamate, and methionine) were markedly decreased compared to the control group, suggesting that increased degradation of amino acids occurred to provide energy in prawns at reoxygenation conditions. This study describes the acute metabolomic alterations that occur in prawns in response to hypoxia and demonstrates the potential of the altered metabolites as biomarkers of hypoxia.
Highlights
The level of dissolved oxygen is a key indicator of water quality, and partially determines the intensity of crustacean aquaculture
Crustaceans often exposed to hypoxia show a complex and highly integrated series of metabolic responses to maintain cellular homeostasis, and ATP synthesis/hydrolysis is crucial in the process of hypoxia-induced stress
We observed no significant changes in ATPα and ATPβ mRNA expression in prawns during hypoxia or subsequent reoxygenation; this is not consistent with previous findings in the L. vannamei (Martinez-Cruz et al, 2011) where mRNA level of ATPβ increased in response to hypoxia and a subsequent decreased when L. vannamei were re-oxygenated
Summary
The level of dissolved oxygen is a key indicator of water quality, and partially determines the intensity of crustacean aquaculture. Several analytical techniques have been well established and are frequently applied in metabolomics studies (Luo et al, 2007; Nudi et al, 2008; Shao et al, 2015; Li et al, 2017), such as liquid chromatography–mass spectrometry (LC–MS), nuclear magnetic resonance (NMR), high-performance liquid chromatography (HPLC), and gas chromatography–mass spectrometry (GC–MS). Among these analytical techniques, GC-MS is frequently used in metabolomics studies and is highly sensitive and reproducible (Ruan et al, 2013; Ren et al, 2015). Their work confirmed the applicability of GC-MS-based metabolomics analysis to characterize the biological effects of environmental stressors in crustaceans
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