Uncovering rumen microbiome components shaping feed efficiency in dairy cows

Abstract

Ruminants provide human society with high quality food from non-human-edible resources, but their emissions negatively impact the environment via greenhouse gas production. The rumen and its resident microorganisms dictate both processes. The overall goal of this project was to determine whether a causal relationship exists between the rumen microbiome and the host animal's physiology, and if so, to isolate and examine the specific determinants that enable this causality. To this end, we divided the project into three specific parts: (1) determining the feed efficiency of 200 milking cows, (2) determining whether the feed- efficiency phenotype can be transferred by transplantation and (3) isolating and examining microbial consortia that can affect the feed-efficiency phenotype by their transplantation into germ-free ruminants. We finally included 1000 dairy cow metadata in our study that revealed a global core microbiome present in the rumen whose composition and abundance predicted many of the cows’ production phenotypes, including methane emission. Certain members of the core microbiome are heritable and have strong associations to cardinal rumen metabolites and fermentation products that govern the efficiency of milk production. These heritable core microbes therefore present primary targets for rumen manipulation towards sustainable and environmentally friendly agriculture. We then went beyond examining the metagenomic content, and asked whether microbes behave differently with relation to the host efficiency state. We sampled twelve animals with two extreme efficiency phenotypes, high efficiency and low efficiency where the first represents animals that maximize energy utilization from their feed whilst the later represents animals with very low utilization of the energy from their feed. Our analysis revealed differences in two host efficiency states in terms of the microbial expression profiles both with regards to protein identities and quantities. Another aim of the proposal was the cultivation of undescribed rumen microorganisms is one of the most important tasks in rumen microbiology. Our findings from phylogenetic analysis of cultured OTUs on the lower branches of the phylogenetic tree suggest that multifactorial traits govern cultivability. Interestingly, most of the cultured OTUs belonged to the rare rumen biosphere. These cultured OTUs could not be detected in the rumen microbiome, even when we surveyed it across 38 rumen microbiome samples. These findings add another unique dimension to the complexity of the rumen microbiome and suggest that a large number of different organisms can be cultured in a single cultivation effort. In the context of the grant, the establishment of ruminant germ-free facility was possible and preliminary experiments were successful, which open up the way for direct applications of the new concepts discovered here, prior to the larger scale implementation at the agricultural level.