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.
Highlights
By 2050, the human population will grow to over 9 billion people, and in the same time frame, global meat consumption is projected to increase by 73% [1]
Methane is a highly potent greenhouse gas and ruminants are the major source of methane emissions from anthropogenic activities
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
Summary
By 2050, the human population will grow to over 9 billion people, and in the same time frame, global meat consumption is projected to increase by 73% [1]. Methane is a greenhouse gas with a global warming potential 28-times that of carbon dioxide [2] and ruminants are the major source of methane emissions from anthropogenic activities. Finding means to mitigate methane emissions is an intractable problem, despite large international research efforts. A fundamental problem is that the ruminal microbiota is able to adapt rapidly to intervention methods that have been tried so far—such as different dietary formulations, chemical and biological feed additives, chemo-genomics and anti-methanogen vaccines [3]. From the environmental and energetic efficiency point of view, there is a disadvantage in that the anaerobic microbial fermentation process can result in excess hydrogen that is used by methanogenic archaea to produce methane and eructed into the atmosphere. The loss of feed gross energy as methane has been estimated at 2 to 12% [4]
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