Rumen ciliates modulate methane emissions in ruminants

Rumen ciliates are major contributors to enteric methane emissions from ruminant animals, yet the underlying mechanisms remain poorly understood. We present a catalog of 450 rumen ciliate genomes, with 87% newly generated. Using this resource, we quantified methane emissions from 100 cows and analyzed 1877 rumen metagenomic and metatranscriptomic datasets, which revealed correlations among ciliate abundance, methanogen abundance, and methane emissions. We further demonstrated that taxon-specific effects of rumen ciliates on methane production arise from a single-membrane, hydrogen-producing organelle called the hydrogenobody (HB), which is distinct from canonical hydrogenosomes in other protists. HBs are positioned near ciliary basal bodies and harbor specific hydrogenases and oxygen reductases. We found that Vestibuliferida ciliates, which have more abundant HBs than do Entodiniomorphida, exhibit enhanced hydrogen production and oxygen-scavenging capacity, thereby strongly promoting methanogenesis.