Comparison of rumen and liver lipid metabolism in grazing vs. indoor-feeding lambs: Insights into 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 weights were assigned to two groups: one fed pellets and hay in separate pens (AF) and the other grazing exclusively on artificial pasture (AG) for 90 d. The results showed significantly higher serum glucose and triglyceride concentrations and significantly lower serum lipase activity 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 Malic enzyme 1 (ME1), fatty acid-binding protein 1 (FABP1), hydroxyacyl-CoA dehydrogenase alpha subunit (HADHA), Perilipin-2 (PLIN2), and acetyl CoA acyltransferase 2 (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 acid in muscle, rumen, and liver were 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, this study systematically revealed the lipid metabolism mechanisms in lambs under different feeding patterns, which are influenced by comprehensive factors such as diet and environment. These findings contribute to the goals of high-quality grazing lamb production and efficient grassland productivity.