Comparison of rumen and liver lipid metabolism in grazing vs. indoor-feeding lambs: insights into optimizing muscle fatty acid composition

• Grazing mainly affects the biosynthesis of unsaturated fatty acids in the rumen and liver. • Grazing inhibits fatty acid oxidation and lipid synthesis in the liver. • The reduction of oleic acid, palmitic acid, and stearic acid in the rumen and liver helps decrease their deposition in the muscle, thus optimizing muscle fatty acid composition. Grassland resources are the foundation of the sheep industry, and the development of artificial pastures provides a solution for alleviating the livestock-carrying pressure on natural grasslands. Based on the impact of lipid metabolism on muscle fatty acid composition, studying the differences in rumen and liver lipid metabolism between grazing and indoor feeding lambs helps to analyze the causes of high-quality grazing lamb meat and to improve the productivity of artificial pasture-based grazing systems. A total of 22 weaned lambs with similar weight were assigned to two groups; fed pellets and hay in separate pens (AF) or grazed exclusively on artificial pasture (AG) for 90 days. The results showed a significantly higher value in serum glucose and triglyceride concentrations and a significantly lower value in serum lipase in the AF vs AG group ( P < 0.05). The metabolome revealed that crucial differential metabolites (DFMs) participating in lipid metabolism, oleic acid and palmitic acid, were down-regulated in the rumen of the AG group. In the liver, oleic acid, α-linolenic acid, and stearic acid were down-regulated in the AG group, while linoleic acid was up-regulated. Meanwhile, rumen hydroxypropanoate and liver succinic acid, enriched in propionate metabolism processes, were down-regulated in grazing lambs. Subsequently, liver transcriptome sequencing revealed that grazing inhibited fatty acid oxidation and lipid synthesis by down-regulating ME1 , FABP1 , HADHA , PLIN2 , and ACAA2 . The significant correlation between CYP4A6 and propionate metabolites suggested a potential regulatory role of propionate metabolism in liver lipid metabolism. Moreover, oleic acid, palmitic acid and stearic acids in muscle, rumen and liver were also closely correlated, revealing an essential contribution of rumen and liver lipid metabolism to muscle fatty acid deposition. Through the multi-omics assessment of the rumen and liver, our research systematically revealed the lipid metabolism mechanisms in lambs under different feeding patterns, which were caused by comprehensive factors such as diet and environment. It has made contributions to the goals of high-quality grazing lamb production and efficient grassland productivity.