Effects of gut bacterial community on differential growth of sea cucumber (Apostichopus japonicus): Molecular mechanisms based on host-gut microbiome co-metabolism

Abstract

Background Gut microbiome and their metabolites are increasingly recognized for their pivotal role in regulating the health and growth of the host. The mechanism by which the host-gut microbiome co-metabolism affects the growth rate of sea cucumber (Apostichopus japonicus) remains unclear. In this study, the intestinal wall tissues of fast-growing (FG) and slow-growing (SG) A. japonicus were collected from the full-sib family for 16S amplicon sequencing, metagenomics, metabolomics, and transcriptomics analyses. Results The results showed a marked variation in the gut bacterial community of A. japonicus with different growth rates. Compared with SG group, FG A. japonicus had a higher abundance of Bacteroidetes. Many of these bacteria were associated with the degradation of polysaccharides, which could potentially affect growth performance. The abundance of Proteobacteria, however, was found to be higher in SG A. japonicus, thereby increasing the potential risk of disease. The metabolome results were further supported by the predicated KEGG functions of the gut microbiomes, lots of metabolites related to the metabolism and biosynthesis of fructose 6-phosphate, arachidonic acid, oleic acid, and dihydroxyacetone phosphate were upregulated in the FG A. japonicus. Furthermore, the genes (IGF1, HK, PK, PCK1) were significantly upregulated in the FG A. japonicus, which were mainly enriched in the metabolic pathways of lipids, amino acids, and carbohydrates. Conclusions Gut bacterial community via their unique metabolic pathways, which in turn affected the metabolic phenotypes of the organism and eventually led to differences in growth performance of A. japonicus. These findings might help understand the molecular mechanisms of growth gap in sea cucumber, thereby increasing the mariculture production.