Sporosarcina aquimarina MS4 is a microecological preparation for overwintering Apostichopus japonicus, which has an immune regulation function, but its role in the nutritional regulation of A. japonicus is not clear. This study aimed to describe the effects of S. aquimarina MS4 on the growth, digestion, and body wall nutrition of A. japonicus through feeding experiments and to discuss the potential mechanism of S. aquimarina MS4 regulating gut function through the detection of gut microbiota and metabolites. After 60 days of culture, the growth performance of A. japonicus fed S. aquimarina MS4 (108 cfu/g) significantly improved, and the content of polysaccharide, leucine, phenylalanine, lysine, and docosahexaenoic acid in the body wall significantly increased. Gut microbiota analysis showed that although Proteobacteria, Verrucomicrobia, Firmicutes, and Bacteroidetes were the predominant phyla in all the sea cucumbers, Haloferula and Rubritalea showed significant difference between the group fed with or without S. aquimarina MS4. Metabolomics analysis showed that differential metabolites in the gut were mainly enriched in amino acid metabolism and lipid metabolism. The association analysis of differential metabolites and microbiota showed that the production of some differential metabolites was significantly related to differential microorganisms, which improved the understanding of the function of microorganisms and their roles in the gut of A. japonicus. This study reveals the life activities such as growth and metabolism of A. japonicus, and it provides support for the functional study of the gut microbiome of A. japonicus.

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