4.8 Article

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

Journal

ISME JOURNAL
Volume 16, Issue 12, Pages 2775-2787

Publisher

SPRINGERNATURE
DOI: 10.1038/s41396-022-01306-8

Keywords

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Funding

  1. National Natural Science Foundation of China [31902126, U21A20247, 31822052]
  2. China Postdoctoral Science Foundation [2019M663841]

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Understanding the biodiversity and genetics of gut microbiomes is important for host physiology and industrial enzymes. In this study, high-quality ciliate genomes were acquired using single-cell sequencing, providing insights into the taxonomy, phylogeny, and carbohydrate degradation capabilities of rumen ciliates. The ciliate dataset also facilitated metagenomic analysis of rumen microbiota.
Understanding the biodiversity and genetics of gut microbiomes has important implications for host physiology and industrial enzymes, whereas most studies have been focused on bacteria and archaea, and to a lesser extent on fungi and viruses. One group, still underexplored and elusive, is ciliated protozoa, despite its importance in shaping microbiota populations. Integrating single-cell sequencing and an assembly-and-identification pipeline, we acquired 52 high-quality ciliate genomes of 22 rumen morphospecies from 11 abundant morphogenera. With these genomes, we resolved the taxonomic and phylogenetic framework that revised the 22 morphospecies into 19 species spanning 13 genera and reassigned the genus Dasytricha from Isotrichidae to a new family Dasytrichidae. Comparative genomic analyses revealed that extensive horizontal gene transfers and gene family expansion provided rumen ciliate species with a broad array of carbohydrate-active enzymes (CAZymes) to degrade all major kinds of plant and microbial carbohydrates. In particular, the genomes of Diplodiniinae and Ophryoscolecinae species encode as many CAZymes as gut fungi, and similar to 80% of their degradative CAZymes act on plant cell-wall. The activities of horizontally transferred cellulase and xylanase of ciliates were experimentally verified and were 2-9 folds higher than those of the inferred corresponding bacterial donors. Additionally, the new ciliate dataset greatly facilitated rumen metagenomic analyses by allowing similar to 12% of the metagenomic sequencing reads to be classified as ciliate sequences.

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