Effects of a High-Fat Diet on Intestinal and Gonadal Metabolism in Female and Male Sea Cucumber Apostichopus japonicus

SIMPLE SUMMARY: The sea cucumber Apostichopus japonicus is an important aquatic invertebrate in the aquaculture industry. It has high nutritional and medicinal value and is popular with consumers, in particular in Asia. The high demand for the species has led to declines in wild populations and A. japonicus is listed as an endangered species by IUCN. Aquaculture of sea cucumber is important to safeguard the conservation of the species in the wild, and its successful reproduction in captivity is a prerequisite for industrial production. It is known that parental nutrient reserves, in particular of lipids, are directly related to the reproductive performance of sea cucumbers. In this study, we investigated the impact of a high-fat diet on the intestinal and gonadal metabolism of male and female A. japonicus. Diet lipid content significantly affected the intestinal microbiome and metabolite profile, and also interfered with gonadal metabolites. Dietary lipid supplementation enhanced the dominance of Proteobacteria in the intestines. Other microbes in the intestines responded to a high-fat diet, which may contribute to maintain intestinal homeostasis. The physiological and metabolic responses of sea cucumbers to a high-fat diet showed sex differences. Interestingly, a correlation between intestinal and gonadal tissue levels of polyunsaturated fatty acid was found. The results of this study indicate that the lipid content in diets can be differentially adjusted for male and female sea cucumbers to improve nutrition and promote reproduction. This data also contributes to a better understanding of the reproductive biology and sex differences of sea cucumbers. ABSTRACT: Parental nutrient reserves are directly related to reproductive performance in sea cucumbers. This study focused on the lipid requirements of male and female sea cucumbers Apostichopus japonicus during the reproductive stage and analyzed their physiological responses to a high-fat diet (HFD). The intestinal lipid metabolites and microbiome profile changed significantly in animals fed with the HFD, as given by an upregulation of metabolites related to lipid metabolism and an increase in the predominance of Proteobacteria in the microbiome, respectively. The metabolic responses of male and female sea cucumbers to the HFD differed, which in turn could have triggered sex-related differences in the intestinal microbiome. These results suggest that the lipid content in diets can be differentially adjusted for male and female sea cucumbers to improve nutrition and promote reproduction. This data contributes to a better understanding of the reproductive biology and sex differences of sea cucumbers.