Bovine Host Genetic Variation Influences Rumen Microbial Methane Production with Best Selection Criterion for Low Methane Emitting and Efficiently Feed Converting Hosts Based on Metagenomic Gene Abundance

Abstract

Methane produced by methanogenic archaea in ruminants contributes significantly to anthropogenic greenhouse gas emissions. The host genetic link controlling microbial methane production is unknown and appropriate genetic selection strategies are not developed. We used sire progeny group differences to estimate the host genetic influence on rumen microbial methane production in a factorial experiment consisting of crossbred breed types and diets. Rumen metagenomic profiling was undertaken to investigate links between microbial genes and methane emissions or feed conversion efficiency. Sire progeny groups differed significantly in their methane emissions measured in respiration chambers. Ranking of the sire progeny groups based on methane emissions or relative archaeal abundance was consistent overall and within diet, suggesting that archaeal abundance in ruminal digesta is under host genetic control and can be used to genetically select animals without measuring methane directly. In the metagenomic analysis of rumen contents, we identified 3970 microbial genes of which 20 and 49 genes were significantly associated with methane emissions and feed conversion efficiency respectively. These explained 81% and 86% of the respective variation and were clustered in distinct functional gene networks. Methanogenesis genes (e.g. mcrA and fmdB) were associated with methane emissions, whilst host-microbiome cross talk genes (e.g. TSTA3 and FucI) were associated with feed conversion efficiency. These results strengthen the idea that the host animal controls its own microbiota to a significant extent and open up the implementation of effective breeding strategies using rumen microbial gene abundance as a predictor for difficult-to-measure traits on a large number of hosts. Generally, the results provide a proof of principle to use the relative abundance of microbial genes in the gastrointestinal tract of different species to predict their influence on traits e.g. human metabolism, health and behaviour, as well as to understand the genetic link between host and microbiome.

Author Summary

Methane is a highly potent greenhouse gas and ruminants are the major source of methane emissions from anthropogenic activities. Here we show in an experiment with cattle that genetic selection of low-emitting animals is a viable option based on a newly developed selection criterion. The experimental data provided a comprehensive insight into the host additive genetic influence on the microbiome, the impact of nutrition on genetics and the microbiome, and the effect of metagenomic microbial genes on the analysed traits. We developed a selection criterion to change those traits by evaluation of hosts based on the relative abundance of microbial genes. This criterion is shown to be highly informative and it is therefore suggested to be used in studies analysing different traits and species. This study provides a proof of principle that there is an additive genetic influence of the host on its microbiome and that selection for the desired host can be based on the abundance of a suite of genes in the ruminal metagenome associated with the trait. The use of this criterion will allow genetic analysis on a large number of hosts, previously a significant barrier to determination of host genetic effects on such traits.