Integrative analysis of microbiome and metabolome reveals the linkage between gut microbiota and carp growth

Abstract

Gut microbiota and their metabolites are increasingly recognized for their crucial role in regulating the health and growth of the host. The mechanism by which the gut microbiome affects the growth rate of fish (Cyprinus carpio) in the rice-fish coculture system, however, remains unclear. In this study, the gut contents of the fast-growing and slow-growing (FG and SG) carp were collected from the rice-fish coculture system for both the fish gut microbiome and metabolome analyses. High throughput 16 S rRNA gene sequencing showed that the overall gut microbiota of FG group was distinct from that of SG group. For example, the cyanobacteria were highly enriched in the guts of SG carp (18.61%), in contrast, they only represented a minor fraction of gut microbiota for FG group (<0.20%). The liquid chromatography-mass spectrometry (LC-MS)-based metabolomics analysis revealed that 191 identified metabolites mostly located in 18 KEGG pathways were differentially present between the two groups, of which more than 50% of these metabolites were involved in lipid and amino acids metabolism. Compared with the FG group, the gut microbiota of SG group significantly enriched the metabolic pathways involved in the steroid (hormone) biosynthesis, whereas reducing those associated with beta-alanine metabolism, biosynthesis of unsaturated fatty acids and bile secretion. The enrichment and depletion of these metabolic pathways resulted in an increase in steroid metabolites and a decrease in the concentration of spermidine, which may have a major impact on the growth rate of carp. The metabolome results were further supported by the predicated KEGG functions of the gut microbiomes of the two groups, pointing out that the gut microbiota could substantially affect the growth of fish via their unique metabolic functions. Together, our integrated fish gut microbiome and metabolome analysis has substantial implications for the development of engineered microbiome technologies in aquaculture.

Keywords: Growth performance; Gut microbiota; Metabolome; Rice-fish coculture system.