Genomic insights into the phylogeny and biomass-degrading enzymes of rumen ciliates

Ciliated protozoa constitute a major group of the rumen microbiome and play several roles important to ruminants. However, many of their important biological traits, including phylogeny and metabolism, remain to the learned. We sequenced and analyzed 52 high-quality single-ciliate amplified genomes of 22 rumen morphospecies, which were resolved into 19 species spanning 13 genera and three families based on the genomic information. Nine synonymic morphospecies and two cryptic species were identified, and the genus Dasytricha was reassigned from Isotrichidae to a new family Dasytrichidae, which diverged with Isotrichidae ~75 million years ago and had obvious differences in genomic structure. Collectively, these genomes encode 33,693 non-redundant carbohydrate-active enzymes (CAZymes), 99% of which do not have a good match in public databases. Each genome encodes a large repertoire of CAZymes that can synergistically degrade nearly all kinds of plant and microbial carbohydrates. In particular, species of Diplodiniinae and Ophryoscolecinae had extensive CAZymes gene family expansion and recruitment via horizontal gene transfers. The genomic resources and new phylogenetic framework can facilitate or enable future research on many biological traits (e.g., genomic, evolutionary, metabolic, and ecological) of ciliates in general and gut ciliates in particular.