The gut microbiota mediate lipid metabolism to regulate the growth rate of mandarin fish (Siniperca chuatsi)

Mandarin fish ( Siniperca chuatsi ) is an important freshwater aquaculture species in China, enhancing its growth performance is crucial for shortening culture cycles and optimizing industrial benefits. Gut microbiota, as an important participant in host growth regulation, has not yet been clearly linked to growth rate of S.chuatsi . In this study, five fast-growthing (FG) and five slow-growthing (SG) S.chuatsi reared in the same cage were used as targets. Using 16S rRNA gene sequencing combined with untargeted metabolomics, we analyzed the intestinal microbial composition, metabolite profiles, and their interaction patterns. Microbiome structure analysis revealed that Firmicutes and Proteobacteria were the core dominant phyla in the intestine of S.chuatsi . LEfSe analysis identified Fusobacteria as significantly enriched in the FG group (LDA > 3.0, P < 0.05). At the genus level, relative abundances of potential probiotics Cetobacterium and Leuconostoc were 11.7-fold and 1.0-fold higher in the FG group than in the SG group, respectively (LDA > 3.0, P < 0.05). Partial least squares discriminant analysis (PLS-DA) showed significant differentiation in metabolites between groups (R²Y = 0.992, Q² = 0.727). A total of 150 differential metabolites were identified ( P < 0.05, VIP > 1.0, |FC= > 1.0), with 123 upregulated in the FG group, mainly annotated as fatty acids, glycerophospholipids and sterols. KEGG pathway enrichment revealed that the FG group significantly enriched lipid metabolism pathways such as glycerophospholipid metabolism (ko00564), unsaturated fatty acid biosynthesis (ko01040), and steroid hormone biosynthesis (ko00140), while the SG group showed specifically enriched Foxo signaling pathway (ko04810). Spearman correlation analysis showed that Cetobacterium was significantly positively correlated with phosphatidylglycerol (PG, 22:5/18:0) and phosphatidylcholine (PC, 18:1E/2:0) (r > 0.65, P < 0.05). Leuconostoc exhibited a positive correlation with eicosapentaenoic acid (EPA, r = 0.62, P < 0.05) and a significant negative correlation with adenosine diphosphate (ADP, r = -0.71, P < 0.01). These findings suggest that dominant probiotics Cetobacterium and Leuconostoc may synergistically enhance host nutrient absorption and energy utilization efficiency by regulating membrane lipid structure, promoting fatty acid metabolism and steroid hormone synthesis, while inhibiting energy metabolism loss mediated by the Foxo pathway. This study provides new insights into the microbiota-metabolite interaction mechanisms regulating growth in mandarin fish, and offers a theoretical basis for the targeted development of growth-promoting probiotic formulations in aquatic animals. • Firmicutes and Proteobacteria were the core dominant phyla in the intestine of Siniperca chuatsi. • The dominant probiotics Cetobacterium and Leuconostoc may synergistically enhance host nutrient absorption and energy utilization efficiency by regulating membrane lipid structure, promoting fatty acid metabolism and steroid hormone synthesis, while inhibiting energy metabolism loss mediated by the Foxo pathway. • Provides new insights into the interaction mechanisms between microbiota and metabolites in the growth regulation of mandarin fish.