The extent of consumer approval for lamb is intimately connected to meat quality standards. Within this context, the distinctive ‘mutton taint’ serves as a critical benchmark for assessment, a characteristic that is largely governed by the concentrations of three fundamental branched-chain fatty acids (KBCFA), specifically 4-methyloctanoic acid (MOA), 4-ethyloctanoic acid (EOA), and 4-methylnonanoic acid (MNA). While Allium mongolicum Regel (AMR)—an Allium species prevalent in arid Asian regions known for its abundant bioactive constituents—is known to improve meat quality and mitigate these off-flavors, the potential mediating role of the rumen fluid in this process remains unclear. This study investigated whether rumen fluid transplantation (RFT) from AMR-fed donors could mimic the impacts of directly adding AMR to the diet on KBCFA accumulation and meat attributes. Thirty male lambs (23 ± 2 kg BW) were allocated at random into three distinct treatments (n = 10): a control set (CON), a dietary supplementation group administered 15 g/d of AMR (AMG), along with a rumen fluid transplantation treatment (RTG) inoculated with rumen fluid from AMR-fed donors. The carcass traits, physicochemical properties, and makeup of amino acids, as well as the fatty acid constitution of the longissimus thoracis muscle, were subjected to analysis. Data revealed that the levels of KBCFAs associated with off-flavors were markedly lowered in both the AMG and RTG. Specifically, decreases ranging from 49% to 64% were observed in MOA, EOA, and MNA concentrations (p < 0.05). Relative to the control group, drip loss and cooking loss were reduced in the treatment groups (p < 0.05), whereas ash (p = 0.047) and crude protein (p = 0.001) were increased. Moreover, the interventions improved the composition of essential amino acids (EAA), flavor-enhancing amino acids, and polyunsaturated fatty acids (PUFAs). In conclusion, rumen fluid transplantation effectively replicates the beneficial effects of dietary AMR on meat quality, particularly in reducing taint-related KBCFA. Such outcomes imply that rumen microbial communities likely act as a crucial mediator in controlling meat flavor.

Deposition of three key 4-alkyl branched-chain fatty acids (KBCFA), including 4-methyloctanoic acid (MOA), 4-ethyloctanoic acid (EOA), and 4-methylnonanoic acid (MNA), causes the gamey flavor in sheep meat. This study integrated metagenomics and metabolomics to evaluate how Allium mongolicum Regel (AMR) supplementation (15 g/d) and rumen fluid transplantation (RFT) modulate rumen microbiota and hepatic metabolism to reduce KBCFA in lamb longissimus thoracis muscle. The experiment consisted of two phases. In Phase I, twelve 3-month-old male Dorper × Small Tailed Han sheep (25 ± 1 kg) were selected as the rumen donor group. These sheep were supplemented with 15 g/d/head of AMR powder in their basal diet until the end of the experiment. In Phase II, thirty 3-month-old male Dorper × Small Tailed Han sheep (23 ± 2 kg) were randomly assigned to one of three groups (n = 10 per group): the control group (STG), which was fed the basal diet and received a physiological saline transplant; the AMR group, which was fed the basal diet supplemented with 15 g/d/head of AMR powder and received a physiological saline transplant; and the rumen fluid transplant group (RTG), which was fed the basal diet and received a rumen fluid transplant from the donor group. Compared to the STG, results showed that the MOA, EOA, and MNA in the AMG decreased by 64.51%, 54.72%, and 49.34%, respectively. Similarly, the MOA, EOA, and MNA in the RTG were reduced by 63.13%, 56.17%, and 49.60%, respectively (p < 0.001). For the rumen metagenome, AMR enriched the genus Prevotella, while RFT increased Butyrivibrio. Hepatic metabolomics revealed a distinct shift where AMR elevated amino acid derivatives and RFT enhanced carnitine-related metabolites. These alterations indicate a potential metabolic shift associated with amino acid metabolism and mitochondrial β-oxidation, rather than lipid elongation. We postulate that this coordinated regulation across the rumen–liver–muscle axis may alter the availability of lipogenic precursors for KBCFA synthesis, ultimately contributing to improved meat flavor.