Influence of host genetics on the functional composition of the rumen metagenome in beef cattle1.

内容摘要

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. The rumen contains microorganisms which break down plant matter and supply nutrients to the host animal. Each microorganism has its own set of genes with specific functions. All the genetic information of these rumen microorganisms is collectively known as the rumen metagenome. The composition of the rumen metagenome is known to affect economically important traits like feed intake and gain. The goal of this study was to investigate the influence of the host genome on the composition of the rumen metagenome and identify features of the rumen metagenome that might be useful candidates for future genetic selection. Using data from 717 animals, we focused on 16,350 rumen metagenome features. Of these, 92 features were highly heritable. The composition of the rumen metagenome is affected by multiple host genes. These host genes may affect the rumen metagenome through metabolism or immune processes or even host-microbiome crosstalk. Several features of the rumen metagenome are genetically correlated with production traits. The relative abundance of one feature, the aroD gene, was negatively correlated with average daily dry matter intake and positively correlated with average daily gain making it a possible candidate for the genetic selection of feed efficiency.