A Metagenomic Analysis of the Effect of Residual Feed Intake on Ovine Rumen Metabolism

Ruminant animals have a symbiotic relationship with microorganisms in their rumens whereby these microbes degrade complex plant-derived compounds which cannot be degraded by any known animal-encoded enzyme into simpler metabolites accessible to the host’s metabolism. Using a shotgun metagenomics approach, we obtained microbial reads from the rumens of sixteen sheep that differed in their residual feed intake (RFI: eight animals with low and eight with high RFI). Our hypothesis was that the metabolic networks of the microbes from low and high RFI animals would differ in predictable ways. Metagenomic reads from each sheep were mapped onto a database-derived microbial metabolic network, which was linked to the sheep metabolic network by interface metabolites (metabolites transferred from microbes to host). Somewhat surprising, no single enzyme was identified as significantly differentially abundant between the low and high RFI animals. However, when the metabolic network as a whole was analyzed, it was clear that microbes from the low RFI animals were using a suite of enzymes closer in network space to the host’s reactions than were the high RFI (inefficient) animals. Likewise, the low RFI animals showed significantly greater diversity both in microbial taxa and in microbial enzymes than did their high RFI counterparts. We conclude that efficient animals have induced in their rumens a microbial ecosystem that is both more efficient and better matched to the host metabolism than is that of the inefficient animals.