Differential partitioning of key carbon substrates at the rumen wall by recently diverged Campylobacteraceae populations

While the activities of different microbes in the rumen have been shown to modulate the host’s ability to utilize plant biomass, microbes colonizing the host-rumen interface have received little attention. Here, we show that highly abundant Campylobacteraceae on the rumen epithelia have recently diverged into two populations, one of which has become a sink for acetate, the main carbon source for the host. Genomic comparisons suggest that the populations were structured by genome-wide selective sweeps after which they acquired several specific adaptations. These include differential expression and domain duplication in acetate utilization genes, which led to the ability to grow on acetate but also to inhibition by propionate in one population. This metabolic trade-off also manifests itself in differential dynamics of the two populations in vivo. By exploring population-level adaptations that otherwise remain cryptic in culture independent analyses, our results highlight recent evolutionary dynamics with unexpected consequences for ruminant nutrition.