Integrative analysis of gut microbiome and metabolome reveals the growth rate differences in Dezhou donkeys

Average daily gain (ADG) is a key production trait in donkeys; however, substantial variations in ADG occur even under identical nutritional and management conditions. The Gut microbiota is increasingly recognized as a critical regulator of host metabolism and growth. Sixteen male Dezhou donkeys were raised from birth to 18.5 months and classified into slow-growing group (SG, n =8) and fast-growing group (FG, n =8) based on ADG. Fecal microbiome and metabolomic analyses were conducted. The results showed that FG donkeys had higher body weight (BW), weight gain (WG), and ADG than SG donkeys. The FG group donkeys were enriched in fiber-degrading bacteria ( Fibrobacter ), while SG donkeys were enriched in inflammation-associated bacteria ( Campylobacter , Oscillospiraceae_UCG_005 and UCG_002 ). Metabolomics identified 373 differential metabolites, of which 244 were up-regulated in FG. Key pathways in FG included folate, protein, and bile acid metabolism. Growth-promoting metabolites (5-methyltetrahydrofolate, isovaleric acid, L-isoleucine, and L-phenylalanine) correlated positively with fiber-degrading bacteria and ADG, whereas methylmalonic acid was elevated in SG and correlated negatively with growth. These findings indicate the fast-growing donkeys possess a coordinated network of fiber-degrading bacteria and growth-promoting metabolites. While slow-growing donkeys exhibit enrichment of inflammation-associated bacteria and methylmalonic acid, indicating metabolic inefficiency. This study provides potential microbial and metabolic biomarkers for improving growth performance in donkeys.