Red seaweed supplementation suppresses methanogenesis in the rumen, revealing potentially advantageous traits among hydrogenotrophic bacteria

Macroalgae belonging to the genus Asparagopsis have been shown to reduce the production of methane (CH4) during rumen fermentation, while increasing feed efficiency when added to the feed of cattle. However, little is known about how the microbial community in the rumen responds to Asparagopsis supplementation, and how changes in the rumen microbiome may contribute to shifts in rumen function and ultimately the hosts phenotype. In this study, we generated and analyzed metagenomic and metatranscriptomic data from the microbiome associated with rumen fluid collected from two cohorts of lactating dairy cows, one fed a diet supplemented with Asparagopsis armata (treatment) and another fed the same diet without A. armata supplementation (control). The reduction of CH4 emission from animals that received A. armata was coupled to a qualitative decrease in relative archaeal abundance and a significant reduction in the transcription of methanogenesis pathways. Additionally, a significant decrease in the transcription of genes for complex carbon catabolism and a re-organization of the expression profile of carbon catabolic genes at the species level was observed in treated animals. Increased H2 production, a consequence of methanogenesis suppression, was coupled to a significant increase in the transcription of hydrogenases that mediate hydrogenotrophic metabolism in the treatment group. Analysis of metatranscriptome data identified a single uncultured hydrogenotrophic bacterial species (a Duodenibacillus sp.) as the dominant driver of this transcriptional change. Comparative genomic analysis between the Duodenibacillus sp. and other hydrogenotrophic rumen organisms revealed metabolic traits in the Duodenibacillus that may provide a competitive advantage in H2 scavenging. These findings provide an initial understanding of how rumen microbiota respond to a promising CH4 reducing feed additive, and may serve as a model to understand alternative stable rumen microbiome states that produce less methane and increase animal productivity.