Altered intestinal microbiota induced by chronic hypoxia drives the effects on lipid metabolism and the immune response of oriental river prawn Macrobrachium nipponense

Abstract

Feed management and seasonal changes can cause long-term episodes of hypoxia in prawn ponds during aquaculture. Changes to prawn morphology and their intestinal microbiota in response to chronic hypoxia are poorly understood. In the present study, we exposed the oriental river prawn Macrobrachium nipponense to normoxic, moderately hypoxic, and hypoxic conditions for four weeks, and then studied their fatty acid composition, metabolic and immune enzyme activities, and intestinal microbiota. Hypoxia clearly affected the intestinal microbiota and mucosal morphology. Compared with the normoxia and moderate hypoxia groups, the prawns in the hypoxia group had a significantly higher levels of intestinal pathogenic bacteria and a clearly different microbial community structure. Functional prediction revealed that the prawns' adaptation to hypoxia might involve microbiota-induced modulation of lipid metabolic pathways. Furthermore, significant decreases in the levels of intestinal short-chain fatty acids and the levels of hepatic highly unsaturated fatty acids (e.g., eicosapentaenoic acid and eicosapentenoic acid) were observed on prawns in response to hypoxia (P < .05). Hepatic metabolic enzymes activities and haemolymph metabolites were also markedly affected by chronic hypoxia (e.g., fatty acid synthetase, acetyl-CoA carboxylase, lipo-protein lipase, carnitine palmitoyltransferase I, and the free fatty acid content). Hypoxia also significantly reduced intestinal immune enzyme activities in the prawns (e.g., phenoloxidase, alkaline phosphatase, and acid phosphatase) (P < .05). During hypoxia, the prawns' intestinal microbial communities correlated significantly with the intestinal alkaline phosphatase activity (P < .05). The results suggested that chronic hypoxia negatively affected M. nipponense intestinal health by altering the composition of the microbiota, inhibiting the immune response, and decreasing the content of short-chain fatty acids in the intestines.