Genomic insights into the phylogeny and biomass-degrading enzymes of rumen ciliates | The ISME Journal

2022-08-19 22:53:40 By : Ms. Victoria Ye

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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 ~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 ~12% of the metagenomic sequencing reads to be classified as ciliate sequences.

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All sequencing data and the ciliate genomes assembled in this study have been deposited in the NCBI database with the accession ID PRJNA777442. The GenBank accession ID of the five overexpressed CAZymes are ON513421-ON513423, SEL14292.1, and WP_022932480.1.

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This study was financially supported by the National Natural Science Foundation of China (31902126, U21A20247, and 31822052) and the China Postdoctoral Science Foundation (2019M663841). We thank the High-Performance Computing Platform of Northwest A&F University and the National Supercomputing Center in Xi’an and Hefei for providing the computing resources for the bioinformatic analyses.

These authors contributed equally: Zongjun Li, Xiangnan Wang, Yu Zhang, Zhongtang Yu, Tingting Zhang.

Center for Ruminant Genetics and Evolution, College of Animal Science and Technology, Northwest A&F University, Yangling, 712100, China

Zongjun Li, Xiangnan Wang, Yu Zhang, Tingting Zhang, Xuelei Dai, Xiangyu Pan, Ruoxi Jing, Yueyang Yan, Yangfan Liu, Shan Gao, Youqin Huang, Junhu Yao, Tao Shi & Yu Jiang

Department of Animal Sciences, The Ohio State University, Columbus, OH, 43210, USA

College of Animal Engineering, Yangling Vocational & Technical College, Yangling, 712100, China

State Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, 730020, China

Fei Li & Youqin Huang

State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, 100193, China

Jian Tian, Bin Yao & Huoqing Huang

Key Laboratory of Animal Biotechnology of the Ministry of Agriculture, College of Veterinary Medicine, Northwest A&F University, Yangling, 712100, China

College of Information Engineering, Northwest A&F University, Yangling, 712100, China

Center for Functional Genomics, Institute of Future Agriculture, Northwest A&F University, Yangling, 712100, China

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ZL and YJ conceived and supervised the project. ZL, XW, TZ, YL, TS and XX collected the samples. XW, ZL, YL, FL, YH, HH, JN, and JT carried out the experiments. ZL, YZ, XW, TZ, XD, XP, RJ, YY, and SG performed bioinformatic analyses. ZL and ZY wrote the manuscript. ZY, YJ, HH, JY and BY revised the manuscript. All authors have read and approved the final manuscript.

Correspondence to Huoqing Huang or Yu Jiang.

The authors declare no competing interests.

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Li, Z., Wang, X., Zhang, Y. et al. Genomic insights into the phylogeny and biomass-degrading enzymes of rumen ciliates. ISME J (2022). https://doi.org/10.1038/s41396-022-01306-8

DOI: https://doi.org/10.1038/s41396-022-01306-8

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