Differential carbon utilization enables co-existence of recently speciated Campylobacteraceae in the cow rumen epithelial microbiome

The activities of different microbes in the cow rumen have been shown to modulate the host's ability to utilize plant biomass, while the host-rumen interface has received little attention. As datasets collected worldwide have pointed to Campylobacteraceae as particularly abundant members of the rumen epithelial microbiome, we targeted this group in a subset of seven cows with meta- and isolate genome analysis. We show that the dominant Campylobacteraceae lineage has recently speciated into two populations that were structured by genome-wide selective sweeps followed by population-specific gene import and recombination. These processes led to differences in gene expression and enzyme domain composition that correspond to the ability to utilize acetate, the main carbon source for the host, at the cost of inhibition by propionate. This trade-off in competitive ability further 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 how recent evolutionary dynamics can shape key functional roles in the rumen microbiome.

Automated summary

The activities of different microbes in the cow rumen affect the host's ability to utilize plant biomass, with little attention paid to the host-rumen interface. Campylobacteraceae has been found to be abundant in the rumen epithelial microbiome, and this study focused on this group in seven cows. The results showed recent speciation within the Campylobacteraceae lineage, resulting in differences in gene expression and enzyme domain composition that impact the host's carbon source utilization and competitive ability in vivo.