Based on the Metabolomic Approach the Energy Metabolism Responses of Oriental River Prawn Macrobrachium nipponense Hepatopancreas to Acute Hypoxia and Reoxygenation

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.

Respiratory Metabolism Responses of Chinese Mitten Crab, Eriocheir sinensis and Chinese Grass Shrimp, Palaemonetes sinensis, Subjected to Environmental Hypoxia Stress

“…In general, SDH activity is used as an important indicator to measure the aerobic capacity of the body ( Simon and Robin, 1971 ). These results showed that significantly lower SDH activity occurred in E. sinensis and P. sinensis after environmental hypoxia, indicating a lower level of aerobic metabolism, similar to a previous study of Macrobrachium nipponense ( Sun et al, 2018 ). LDH is a key regulatory enzyme in anaerobic glycolysis.…”

“…Much research has focused on the negative effects of environmental hypoxia on crustaceans. For example, environmental hypoxia causes abnormal breathing and metabolic disorders in crustaceans, which leads to a decline in feeding and efficiency of food transformation and retarded growth ( Han et al, 2017 ; Sun et al, 2018 ). Environmental hypoxia even affects the behavior, morphological characteristics, immunity, and reproduction of crustaceans ( De Lima et al, 2015 ; Lara et al, 2017 ; Peruzza et al, 2018 .).…”

Metabolomics investigation of molecular responses of whiteleg shrimp (Penaeus vannamei) to hypoxia

“…In shrimp, accumulation of lactic acid has been recorded during out of water storage stress [45] and elevated temperatures [46]. Interestingly, increases of lactic acid due to hypoxia have been recently reported in M. nipponense [29] and P. vannamei [6,7,47,48]. In addition to lactic acid, other metabolites, such as succinic acid, alanine and volatile fatty acids are also anaerobic end-products in invertebrates [49][50][51].…”

“…These studies cover diverse topics, including diet and nutrient [13][14][15], immunology and disease [16][17][18], environmental stress [18][19][20], eco-toxicology [21,22], and post-harvest handling [23,24]. Several studies have also employed metabolomics techniques to explore hypoxic effects in molluscan species, such as sea cucumbers [19,20], abalone [25,26], mussels [27,28] and prawn [29]. In general, these studies have reported changes in metabolites from different tissues of the host under hypoxic stress conditions compared to controls.…”

Molecular Cloning and Expression Analysis of Lactate Dehydrogenase from the Oriental River Prawn Macrobrachium nipponense in Response to Hypoxia

“…Thus, in prawn production, hypoxia may cause large economic losses because of increased mortality and decreased growth rate. Our previous studies have focused on energy metabolic mechanism for prawns in response to hypoxia stress [ 15 , 16 ]. However, little information is available on expression and regulation of LDH, a key enzyme of anaerobic metabolism, in M. nipponense .…”