Multiomics insights into rumen microbiome and function in grazing lambs: implications for nutrient absorption and grassland sustainability.

BACKGROUND: The center of sustainable development of grassland husbandry is the balance between forage intake and growth characteristics of animals, and one of the keys to restricting the conversion efficiency of forage intake is the digestibility of forage produced by rumen microorganisms. Thus, the interaction between grass intake and rumen microbial fermentation is a key driver of both ruminant productivity and grassland ecosystem health. However, interactions between grass species, supplementary feeding, rumen microbiome, and rumen epithelium function, remain poorly understood. RESULTS: We employed metagenomic and metatranscriptomic analyses, coupled with single-cell RNA sequencing (scRNA-seq) of rumen wall and serum metabolomics, to investigate how the rumen microbiome regulates grass intake and host metabolism. In a two-factor (grazing intensity and concentrate supplementation) experiment with 72 lambs, supplementary feeding under moderate grazing increased dry matter intake but decreased grass consumption of Artemisia tanacetifolia. These shifts correlated with contrasting trends between metagenomic and metatranscriptomic profiles of Lachnospiraceae. scRNA-seq revealed an increased abundance of basal cells (BCs), terminally differentiated keratinocytes (TDKs), and differentiated keratinocytes (DKs) in the supplemented group, with solute carrier genes (e.g., SLC16A1) involved in short chain fatty acids (SCFAs) transport enriched in basal cells. We also identified interactions between the rumen microbiome and host epithelial cells, influencing gene expression and localization, which in turn mediated the animal serum nutrient metabolism, particularly in B vitamin, bile acids, and amino acids. CONCLUSIONS: Our study identified key microbiome and epithelial cell subtypes involved in grass digestion and SCFAs metabolism in the rumen. This novel link between ruminal microbial function, epithelial cell cluster-based genes, and host metabolism provides critical insights into mechanisms underlying the interaction between grass intake and supplementary feeding for optimizing ruminant management strategies in sustainable grazing systems. Video Abstract.