Multi-omics reveals that dietary Piper sarmentosum Roxb. extract improves goat meat quality via the microbiota-muscle amino acid metabolic axis.

Abstract

Background: Improving meat quality through nutritional regulation is an important approach in ruminant production. Growing evidence suggests that rumen microbiota influences host metabolism via microbial metabolites, thereby affecting meat quality. However, whether Piper sarmentosum Roxb. extract (PSE), a medicinal and edible plant-derived extract, improves meat quality through rumen microbiota-host metabolic interactions remains unclear. Thirty-six weaned male Hainan black goats (approximately 3 months old) were randomly assigned to four dietary treatments supplemented with 0, 200, 400, or 600 mg/kg PSE (dry matter basis), respectively. After a 90-day feeding trial, goats were fasted for 12 h before slaughter, and rumen and longissimus lumborum muscle samples were collected for subsequent analyses.

Results: Supplementation with 600 mg/kg PSE significantly enhanced meat quality traits, including higher ultimate pH, improved color stability, and increased water-holding capacity, without affecting growth performance or carcass traits. Transcriptomic and metabolomic analyses revealed that PSE supplementation was associated with remodeling of amino acid and energy metabolism in muscle, particularly glutamate-related pathways. These metabolic changes were accompanied by increased expression of key metabolic genes, including BCAT2, IDH1, and IDH3A, alongside alterations in energy-related metabolites, such as the downregulation of carnitine and upregulation of creatinine. Concomitant shifts in rumen microbial composition were observed, with PSE supplementation increasing the abundance of genera like Weissella and Ruminococcus, while reducing potentially opportunistic genera, such as Acinetobacter and Klebsiella. Weissella showed strong positive correlations with elevated rumen metabolites like serine, threonine, choline, and hypoxanthine. Metagenome-assembled genome analysis of Weissella cibaria revealed an enrichment of genes related to amino acid metabolism and glycosyltransferase families. Correlation and mediation analyses further revealed associations among Weissella abundance, rumen metabolites, and muscle metabolic traits, supporting a potential microbiota-metabolite-host metabolic relationship.

Conclusions: Collectively, this study provides new insights into the association network linking PSE-induced alterations in rumen microbiota, microbial metabolites, and host muscle metabolism in relation to goat meat quality. These findings suggest that PSE supplementation may improve meat quality through coordinated changes in rumen microbial ecology and muscle metabolic profiles.