Influence of host genetics on the functional composition of the rumen metagenome in beef cattle

Cattle rely on the microorganisms in their rumen to break down plant matter into useable nutrients. Studies have demonstrated that the rumen microbiome plays a critical role in economically important traits. One factor that impacts rumen microbial community assembly is the host genome. Previous studies have demonstrated host genetics affect rumen microbial community composition and the association of microbiome features with production traits. However, gaps exist relative to the underlying host genetic influence on functional features of the rumen metagenome. Here we elucidated the relationship between host genetics and functional composition of the rumen metagenome while identifying metagenomic features which may provide targets for genetic selection. Rumen samples were collected via esophageal tubing from 717 beef cattle on four diets and were subjected to shotgun sequencing from which open reading frames (ORFs) were predicted. Animal genotypes were generated from imputation based on low-pass sequencing and array data. The log-transformed relative abundance of 16,350 ORFs were used as phenotypes in linear mixed models with the random effect of host genotype. In this population of 717 animals, approximately 4% of the ORFs had heritability estimates larger than twice their standard error and more than 10% of the ORFs had estimates greater than 0.20. Functions of highly heritable ORFs included aromatic amino acid biosynthesis and genome regulation. Additionally, some ORFs were genetically correlated with production traits. Eleven host genes were associated with more than one ORF. The functionality of these candidate host genes can be generally classified as either immune-related, metabolism-related, or possibly involved in host-microbiome crosstalk. Host genetics influence the rumen microbiome function making genetic selection of the host an avenue to alter rumen microbiome functionality. Associations between host genes and rumen metagenome composition indicate multiple potential biological mechanisms underlie these associations. Moreover, a portion of the highly heritable ORFs are genetically correlated with feed efficiency traits making them potential selection targets to increase productivity. The functions of the candidate host genes show the rumen metagenome is influenced by multiple complex biological systems of the host.