Comparative analysis of functional diversity of rumen microbiome in bison and beef heifers

Abstract

ABSTRACT Enhancing crop residue digestibility can boost the available energy for growth and milk yield and improve the sustainability of ruminant production systems. As the natural diet of bison is high in lignocellulose, bison have developed a microbiome that efficiently digests cellulose and hemicellulose. This study compared the rumen metatranscriptomes of bison and beef heifers and investigated the effects of inoculating heifers with bison rumen contents. Gene Ontology, molecular function, and Kyoto Encyclopedia of Genes and Genomes orthology terms identified through gene set enrichment analysis successfully captured differences in gene expression of rumen microbiome between heifers and bison fed different diets. Specifically, differences in nitrogen metabolism was detected between heifers and bison rumen microbiomes. Heifer rumen microbiomes demonstrated a higher dissimilatory nitrate reduction, while bison microbiomes tended to suppress this pathway. In contrast, bison microbiomes expressed higher levels of glutamate dehydrogenase 2 (GDH2) genes. However, glutamate dehydrogenase gene expression was observed to be strictly regulated in heifers, as inoculation with bison rumen contents had no effect on expression. Moreover, the transfer of bison rumen contents led to a persistent downregulation of microbial nitrogen metabolism in heifers after 27 days of transfer. In addition, gene set enrichment analysis also identified the crucial regulatory role of serine/threonine kinase in heifer rumen microbial metabolism and differences in ion transport between heifers and bison. These findings provide valuable insights into the complex interplay between diet and the rumen microbiome. IMPORTANCE Ruminants play a key role in the conversion of cellulolytic plant material into high-quality meat and milk protein for humans. The rumen microbiome is the driver of this conversion, yet there is little information on how gene expression within the microbiome impacts the efficiency of this conversion process. The current study investigates gene expression in the rumen microbiome of beef heifers and bison and how transplantation of ruminal contents from bison to heifers alters gene expression. Understanding interactions between the host and the rumen microbiome is the key to developing informed approaches to rumen programming that will enhance production efficiency in ruminants.