Effects of Dietary Starch and Dextrin on Growth and Hypoxia Tolerance in Tiger Puffer (Takifugu rubripes)

Fish meal and fish oil are important sources of protein and lipid in feeds. The lack of fish meal and fish oil supply has become an important limiting factor for the aquaculture industry. The proportion of fish oil and fish meal used in commercial feeds for farmed fish and crustaceans is continually decreasing, while the carbohydrate content is increasing. Carbohydrates are one of the three major nutrients that provide energy for the body. They have a much lower production price than protein and fat. Starch is a polymeric carbohydrate made from glucose molecules; it is the most commonly used in aquatic feeds and can replace fish meal and fish oil to reduce feed cost. Therefore, it is important to fully explore the nutritional function of carbohydrates for aquaculture. Hypoxia is a common stress in aquaculture, and acute hypoxia may lead to massive mortality of cultured fish in a short period of time resulting in serious economic losses to aquaculture. Therefore, it is crucial to find ways to improve the acute hypoxia tolerance of fish. Fish mainly use glucose for energy under acute hypoxia. Hypoxia inhibits oxidative phosphorylation in mitochondria and activates the anaerobic glycolysis pathway. Glucose degrades to produce lactate and ATP. Carnivorous fishes have limited absorption and utilization capacities to feed carbohydrates, unlike omnivorous fishes. Dextrin is an intermediate starch hydrolysis product, with a molecular weight between starch and glucose; it has good adhesion properties and is more easily digested and absorbed than starch. Therefore, we hypothesized that the use of easily digestible carbohydrate in the feed is an effective way to improve the acute hypoxia tolerance of fish. Takifugu rubripes is loved by Japanese and Korean consumers owing to its delicious taste and high nutritional value. It is a characteristic species of Chinese mariculture fish. It is mainly cultured in a high-density factory, and the dissolved oxygen in the water often relies on water exchange and an oxygenation pump; its gill cover is degraded and is at risk of acute hypoxia. This study determined the effect of the addition of corn starch or dextrin (corn starch hydrolysate) to the feed on growth performance, acute hypoxia survival rate, metabolite content, and the hypoxia inducible factor (HIF) signaling pathway of T. rubripes after 8 weeks of feeding. There were no significant differences in weight gain, feed conversion ratio, hepatosomatic index, viscerosomatic index, condition factor, and body composition between the starch group and the dextrin group (P > 0.05). However, the survival rate during acute hypoxia of the dextrin group was significantly higher than that of the starch group (P < 0.05). There were no significant differences in the liver glycogen and lactate contents, and lactate dehydrogenase A4 (ldha) gene expression between the starch group and dextrin group (P > 0.05) during normoxia. However, the lactate content and ldha gene expression were significantly higher in the liver of the dextrin group than those in the starch group (P < 0.05) during hypoxia. This indicated that feeding dextrin strongly activated anaerobic glycolysis to provide more energy under hypoxia. The serum triglyceride (TG) content significantly increased in the dextrin group compared with the normoxia groups, although the TG content in the serum and liver significantly decreased in the starch group after acute hypoxia (P < 0.05). This suggested that feeding starch promoted lipid catabolism and oxygen consumption. There was no significant difference in the total soluble protein content of the muscle between the starch group and the dextrin group (P > 0.05) during normoxia. However, the total soluble protein content of the muscle decreased in the dextrin group compared with the starch group (P < 0.05) after acute hypoxia. Meanwhile, the total muscle soluble protein content, and the gene expression of liver v-akt murine thymoma viral oncogene homolog 1 (akt1), and mechanistic target of rapamycin kinase (mtor) significantly decreased in the dextrin group after hypoxia compared with the normoxia group. However, the liver mtor gene expression significantly increased in the starch group after hypoxia (P < 0.05). This data demonstrated that protein synthesis was inhibited in the dextrin group under hypoxia. Hypoxia inducible factor (HIF) is the most critical transcription factor in cellular response to hypoxic stress. The dextrin group had higher hypoxia inducible factor 1 subunit alpha like (hif-3α) gene expression in the liver and lower hypoxia inducible factor 1 subunit alpha a (hif-1α) gene expression in the muscle (P < 0.05) compared with the starch group during normoxia. The gene expression of liver hif-1α and hif-3α and muscle hif-1α and vascular endothelial growth factor A (vegfa) significantly increased in the dextrin group compared with the starch group (P < 0.05) during hypoxia. This proved that feeding dextrin strongly activated the HIF signaling pathway under hypoxia. In summary, replacing starch with easily digestible dextrin in the feed did not affect the growth performance. Instead, it activated the HIF signaling pathway and anaerobic glycolysis to provide more energy for fish. Meanwhile, feeding dextrin inhibited lipid catabolism and protein synthesis, and reduced oxygen consumption to improve the acute hypoxia tolerance of T. rubripes. The study provides important guidance for the formulation design of hypoxia-tolerant feed and healthy development of aquaculture.