Comparative metagenomic and metatranscriptomic analyses reveal the role of the gayal rumen and hindgut microbiome in high-efficiency lignocellulose degradation

BACKGROUND: The gayal (Bos frontalis), a semi-domesticated bovine species, demonstrates exceptional adaptability to lignocellulose-rich diets dominated by bamboo, suggesting the presence of a specialized gastrointestinal microbiome. However, the functional mechanisms underlying this host-microbiome interaction remain poorly understood. Here, we conducted integrated metagenomic and metatranscriptomic analyses of rumen, cecum, and colon digesta from yellow cattle and gayal raised on the same bamboo-based high-fiber diet. RESULTS: The results showed that gayal exhibited superior fiber-degrading capacity relative to yellow cattle, evidenced by significantly higher (P < 0.05) fiber digestibility, cellulase and xylanase activities, and increased volatile fatty acids production despite identical feed intake. Microbial community analysis revealed distinct composition in both the rumen and hindgut of gayal compared to yellow cattle, with notable enrichment of taxa specialized in lignocellulose degradation. Metatranscriptomic profiling further identified upregulation of key lignin-modification enzymes, particularly AA6, AA2, and AA3, primarily encoded by Prevotella, Cryptobacteroides, Limimorpha, and Ventricola. These enzymes are known to modify lignin structure to increase polysaccharide accessibility. These results demonstrate that gayal hosts a unique and metabolically active gastrointestinal microbiome capable of efficient lignocellulose deconstruction through a coordinated enzymatic cascade, especially effective in dismantling lignin barriers. CONCLUSIONS: This study provides novel insights into host-microbiome co-adaptation to fibrous feeds and highlights the potential of gayal-derived microbial consortia and enzymes for improving roughage utilization in ruminant agriculture.