Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

Abstract

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.

This is a preview of subscription content, access via your institution

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Fig. 1: Generation of genome catalog of rumen ciliates.
Fig. 2: Genome-based taxonomy and phylogeny of rumen ciliates.
Fig. 3: Genome characteristics of rumen ciliates.
Fig. 4: CAZyme profiles of rumen ciliates.
Fig. 5: Classification rates of ciliate reads in rumen metagenomes.

Data availability

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.

References

  1. Seshadri R, Leahy SC, Attwood GT, Teh KH, Lambie SC, Cookson AL, et al. Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection. Nat Biotechnol. 2018;36:359–67.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Stewart RD, Auffret MD, Warr A, Walker AW, Roehe R, Watson M. Compendium of 4,941 rumen metagenome-assembled genomes for rumen microbiome biology and enzyme discovery. Nat Biotechnol. 2019;37:953–61.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Almeida A, Nayfach S, Boland M, Strozzi F, Beracochea M, Shi ZJ, et al. A unified catalog of 204,938 reference genomes from the human gut microbiome. Nat Biotechnol. 2020;39:105–14.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Shabat SKB, Sasson G, Doron-Faigenboim A, Durman T, Yaacoby S, Berg Miller ME, et al. Specific microbiome-dependent mechanisms underlie the energy harvest efficiency of ruminants. ISME J. 2016;10:2958–72.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Lynn DH. The Ciliated Protozoa: Characterization, Classification, and Guide to the Literature. 3rd ed. Heidelberg: Springer; 2008.

  6. Vďačný P. Evolutionary associations of endosymbiotic ciliates shed light on the timing of the marsupial-placental split. Mol Biol Evol. 2018;35:1757–69.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Williams AG. Coleman GS. The Rumen Protozoa. 1st ed. New York: Springer-Verlag; 1992.

  8. Solomon R, Wein T, Levy B, Eshed S, Dror R, Reiss V, et al. Protozoa populations are ecosystem engineers that shape prokaryotic community structure and function of the rumen microbial ecosystem. ISME J. 2022;16:1187–97.

    Article  PubMed  Google Scholar 

  9. Park T, Wijeratne S, Meulia T, Firkins JL, Yu Z. The macronuclear genome of anaerobic ciliate Entodinium caudatum reveals its biological features adapted to the distinct rumen environment. Genomics. 2021;113:1416–27.

    Article  PubMed  CAS  Google Scholar 

  10. Söllinger A, Tveit AT, Poulsen M, Noel SJ, Bengtsson M, Bernhardt J, et al. Holistic assessment of rumen microbiome dynamics through quantitative metatranscriptomics reveals multifunctional redundancy during key steps of anaerobic feed degradation. mSystems. 2018;3:e00038–18.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Terry SA, Badhan A, Wang Y, Chaves AV, McAllister TA. Fibre digestion by rumen microbiota-a review of recent metagenomic and metatranscriptomic studies. Can J Anim Sci. 2019;99:678–92.

    Article  Google Scholar 

  12. Qi M, Wang P, O’Toole N, Barboza PS, Ungerfeld E, Leigh MB, et al. Snapshot of the eukaryotic gene expression in muskoxen rumen-a metatranscriptomic approach. PLoS ONE. 2011;6:e20521.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Newbold CJ, de la Fuente G, Belanche A, Ramos-Morales E, McEwan NR. The role of ciliate protozoa in the rumen. Front Microbiol. 2015;6:1313.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Gruby D, Delafond H. Recherchessur des animalcules se devéloppant en grand nombredansl‘ estomacetdan les intestins pendant la digestion des animaux herbivores et carnivores. C R Acad Sci Paris. 1843;17:1304–8.

    Google Scholar 

  15. Russell JB. Factors that alter rumen microbial ecology. Science 2001;292:1119–22.

    Article  PubMed  CAS  Google Scholar 

  16. Firkins JL. Extending Burk Dehority’s perspectives on the role of ciliate protozoa in the rumen. Front Microbiol. 2020;11:17.

    Article  Google Scholar 

  17. Hobson PN, Stewart CS. The Rumen Microbial Ecosystem. 2nd ed. London: Blackie Academic & Professional; 1997.

  18. Dehority BA. Rumen ciliate protozoa of the blue duiker (Cephalophus monticola), with observations on morphological variation lines within the species Entodinium dubardi. J Eukaryot Microbiol. 1994;41:103–11.

    Article  PubMed  CAS  Google Scholar 

  19. Tymensen L, Barkley C, McAllister TA. Relative diversity and community structure analysis of rumen protozoa according to T-RFLP and microscopic methods. J Microbiol Methods. 2012;88:1–6.

    Article  PubMed  Google Scholar 

  20. Ishaq SL, Wright A-DG. Design and validation of four new primers for next-generation sequencing to target the 18s rRNA genes of gastrointestinal ciliate protozoa. Appl Environ Microbiol. 2014;80:5515–21.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Kittelmann S, Seedorf H, Walters WA, Clemente JC, Knight R, Gordon JI, et al. Simultaneous amplicon sequencing to explore co-occurrence patterns of bacterial, archaeal and eukaryotic microorganisms in rumen microbial communities. PLoS ONE. 2013;8:e47879.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Zhao Y, Yi Z, Gentekaki E, Zhan A, Al-Farraj SA, Song W. Utility of combining morphological characters, nuclear and mitochondrial genes: An attempt to resolve the conflicts of species identification for ciliated protists. Mol Phylogenet Evol. 2016;94:718–29.

    Article  PubMed  Google Scholar 

  23. Moon-van der Staay SY, van der Staay GWM, Michalowski T, Jouany J-P, Pristas P, Javorský P, et al. The symbiotic intestinal ciliates and the evolution of their hosts. Eur J Protistol. 2014;50:166–73.

    Article  PubMed  Google Scholar 

  24. Park T, Meulia T, Firkins JL, Yu Z. Inhibition of the rumen ciliate Entodinium caudatum by antibiotics. Front Microbiol. 2017;8:1189.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Li Z, Deng Q, Liu Y, Yan T, Li F, Cao Y, et al. Dynamics of methanogenesis, ruminal fermentation and fiber digestibility in ruminants following elimination of protozoa: a meta-analysis. J Anim Sci Biotechnol. 2018;9:89.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Feng J, Jiang C, Sun Z, Hua C, Wen J, Miao W, et al. Single-cell transcriptome sequencing of rumen ciliates provides insight into their molecular adaptations to the anaerobic and carbohydrate-rich rumen microenvironment. Mol Phylogenet Evol. 2020;143:106687.

    Article  PubMed  Google Scholar 

  27. Blackburn EH, Gall JG. A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J Mol Biol. 1978;120:33–53.

    Article  PubMed  CAS  Google Scholar 

  28. Greider CW, Blackburn EH. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature. 1989;337:331–7.

    Article  PubMed  CAS  Google Scholar 

  29. Swart EC, Bracht JR, Magrini V, Minx P, Chen X, Zhou Y, et al. The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. PLoS Biol. 2013;11:e1001473.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Hamilton EP, Kapusta A, Huvos PE, Bidwell SL, Zafar N, Tang H, et al. Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome. eLife. 2016;5:e19090.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Or-Rashid MM, Odongo NE, McBride BW. Fatty acid composition of ruminal bacteria and protozoa, with emphasis on conjugated linoleic acid, vaccenic acid, and odd-chain and branched-chain fatty acids1. J Anim Sci. 2007;85:1228–34.

    Article  PubMed  CAS  Google Scholar 

  32. Macaulay IC, Haerty W, Kumar P, Li YI, Hu TX, Teng MJ, et al. G&T-seq: parallel sequencing of single-cell genomes and transcriptomes. Nat Methods. 2015;12:519–22.

    Article  PubMed  CAS  Google Scholar 

  33. Macaulay IC, Teng MJ, Haerty W, Kumar P, Ponting CP, Voet T. Separation and parallel sequencing of the genomes and transcriptomes of single cells using G&T-seq. Nat Protoc. 2016;11:2081–103.

    Article  PubMed  CAS  Google Scholar 

  34. Dean FB, Hosono S, Fang L, Wu X, Faruqi AF, Bray-Ward P, et al. Comprehensive human genome amplification using multiple displacement amplification. Proc Natl Acad Sci USA. 2002;99:5261–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Dehority BA Ciliate protozoa. In: Makkar HPS, McSweeney CS. Methods in Gut Microbial Ecology for Ruminants. Berlin/Heidelberg: Springer-Verlag; 2005. p. 67–78.

  36. Dehority BA. Laboratory Manual for Classification and Morphology of Rumen Ciliate Protozoa. 1st ed. Boca Raton: CRC Press; 1993.

    Google Scholar 

  37. Li D, Luo R, Liu CM, Leung CM, Ting HF, Sadakane K, et al. MEGAHIT v1.0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods 2016;102:3–11.

    Article  PubMed  CAS  Google Scholar 

  38. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol J Comput. Mol Cell Biol. 2012;19:455–77.

    CAS  Google Scholar 

  39. Chakraborty M, Baldwin-Brown JG, Long AD, Emerson JJ. Contiguous and accurate de novo assembly of metazoan genomes with modest long read coverage. Nucleic Acids Res. 2016;44:e147.

    PubMed  PubMed Central  Google Scholar 

  40. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, et al. MEME Suite: tools for motif discovery and searching. Nucleic Acids Res. 2009;37:W202–8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Maurer-Alcala XX, Yan Y, Pilling OA, Knight R, Katz LA. Twisted tales: insights into genome diversity of ciliates using single-cell ‘omics. Genome Biol Evol. 2018;10:1927–39.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Manni M, Berkeley MR, Seppey M, Simão FA, Zdobnov EM. BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol Biol Evol. 2021;38:4647–54.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Kriventseva EV, Kuznetsov D, Tegenfeldt F, Manni M, Dias R, Simão FA, et al. OrthoDB v10: sampling the diversity of animal, plant, fungal, protist, bacterial and viral genomes for evolutionary and functional annotations of orthologs. Nucleic Acids Res. 2019;47:D807–11.

    Article  PubMed  CAS  Google Scholar 

  44. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12:357–60.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8:1494–512.

    Article  PubMed  CAS  Google Scholar 

  46. Stanke M, Morgenstern B. AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res. 2005;33:W465–7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Tourancheau AB, Tsao N, Klobutcher LA, Pearlman RE, Adoutte A. Genetic code deviations in the ciliates: evidence for multiple and independent events. EMBO J. 1995;14:3262–7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997;25:955–64.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK. Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods. 2015;8:12–24.

    Article  Google Scholar 

  50. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun. 2018;9:5114.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Parks DH, Chuvochina M, Chaumeil P-A, Rinke C, Mussig AJ, Hugenholtz P. A complete domain-to-species taxonomy for Bacteria and Archaea. Nat Biotechnol. 2020;38:1079–86.

    Article  PubMed  CAS  Google Scholar 

  52. Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 2019;20:238.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014;30:1312–3.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil P-A, et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol. 2018;36:996–1004.

    Article  PubMed  CAS  Google Scholar 

  55. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24:1586–91.

    Article  PubMed  CAS  Google Scholar 

  56. Mendes FK, Vanderpool D, Fulton B, Hahn MW. CAFE 5 models variation in evolutionary rates among gene families. Bioinformatics 2020;36:5516–8.

    Article  CAS  Google Scholar 

  57. Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK, Cook H, et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 2019;47:D309–14.

    Article  PubMed  CAS  Google Scholar 

  58. Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA, Sonnhammer ELL, et al. Pfam: the protein families database in 2021. Nucleic Acids Res 2020;49:D412–9.

    Article  PubMed Central  Google Scholar 

  59. Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, et al. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2018;46:W95–101.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Haitjema CH, Gilmore SP, Henske JK, Solomon KV, Groot R, de, Kuo A, et al. A parts list for fungal cellulosomes revealed by comparative genomics. Nat Microbiol. 2017;2:17087.

    Article  PubMed  CAS  Google Scholar 

  61. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37:1530–4.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Nakamura Y, Gojobori T, Ikemura T. Codon usage tabulated from international DNA sequence databases: status for the year 2000. Nucleic Acids Res. 2000;28:292.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. You S, Chen C-C, Tu T, Wang X, Ma R, Cai H, et al. Insight into the functional roles of Glu175 in the hyperthermostable xylanase XYL10C-ΔN through structural analysis and site-saturation mutagenesis. Biotechnol Biofuels. 2018;11:159.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Bailey MJ, Biely P, Poutanen K. Interlaboratory testing of methods for assay of xylanase activity. J Biotechnol. 1992;23:257–70.

    Article  CAS  Google Scholar 

  65. Yang H, Zhang Y, Li X, Bai Y, Xia W, Ma R, et al. Impact of disulfide bonds on the folding and refolding capability of a novel thermostable GH45 cellulase. Appl Microbiol Biotechnol. 2018;102:9183–92.

    Article  PubMed  CAS  Google Scholar 

  66. He H, Wu S, Mei M, Ning J, Li C, Ma L, et al. A combinational strategy for effective heterologous production of functional human lysozyme in Pichia pastoris. Front Bioeng Biotechnol. 2020;8:118.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Pan X, Cai Y, Li Z, Chen X, Heller R, Wang N, et al. Modes of genetic adaptations underlying functional innovations in the rumen. Sci China Life Sci. 2021;64:1–21.

    Article  PubMed  CAS  Google Scholar 

  68. Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol. 2019;20:257.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Zheng W, Wang C, Lynch M, Gao S. The compact macronuclear genome of the ciliate halteria grandinella: a transcriptome-like genome with 23,000 nanochromosomes. mBio 2021;12:e01964–20.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Ahrendt SR, Quandt CA, Ciobanu D, Clum A, Salamov A, Andreopoulos B, et al. Leveraging single-cell genomics to expand the fungal tree of life. Nat Microbiol. 2018;3:1417.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Labarre A, López-Escardó D, Latorre F, Leonard G, Bucchini F, Obiol A, et al. Comparative genomics reveals new functional insights in uncultured MAST species. ISME J. 2021;15:1767–81.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Hess M, Sczyrba A, Egan R, Kim T-W, Chokhawala H, Schroth G, et al. Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 2011;331:463–7.

    Article  PubMed  CAS  Google Scholar 

  73. Puniya AK, Singh R, Kamra DN. Rumen microbiology: from evolution to revolution. 1st ed. Heidelberg: Springer; 2015.

  74. Hillis DM, Moritz C, Mable BK. Molecular Systematics. 2nd ed. Sunderland: Sinauer Associates; 1996.

  75. Chen L, Qiu Q, Jiang Y, Wang K, Lin Z, Li Z, et al. Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits. Science. 2019;364:eaav6202.

    Article  PubMed  CAS  Google Scholar 

  76. Gao F, Roy SW, Katz LA. Analyses of alternatively processed genes in ciliates provide insights into the origins of scrambled genomes and may provide a mechanism for speciation. mBio. 2015;6:e01998–14.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. De Luca D, Piredda R, Sarno D, Kooistra WHCF. Resolving cryptic species complexes in marine protists: phylogenetic haplotype networks meet global DNA metabarcoding datasets. ISME J. 2021;15:1931–42.

    Article  PubMed  PubMed Central  Google Scholar 

  78. Zufall RA, McGrath CL, Muse SV, Katz LA. Genome architecture drives protein evolution in ciliates. Mol Biol Evol. 2006;23:1681–7.

    Article  PubMed  CAS  Google Scholar 

  79. Yan Y, Maurer-Alcalá XX, Knight R, Kosakovsky Pond SL, Katz LA. Single-cell transcriptomics reveal a correlation between genome architecture and gene family evolution in ciliates. mBio. 2019;10:e02524–19.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. La Terza A, Papa G, Miceli C, Luporini P. Divergence between two Antarctic species of the ciliate Euplotes, E.focardii and E.nobilii, in the expression of heat-shock protein 70 genes. Mol Ecol. 2001;10:1061–7.

    Article  PubMed  Google Scholar 

  81. Sharma N, Bryant J, Wloga D, Donaldson R, Davis RC, Jerka-Dziadosz M, et al. Katanin regulates dynamics of microtubules and biogenesis of motile cilia. J Cell Biol. 2007;178:1065–79.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Park T, Mao H, Yu Z. Inhibition of rumen protozoa by specific inhibitors of lysozyme and peptidases in vitro. Front Microbiol. 2019;10:2822.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Solomon KV, Haitjema CH, Henske JK, Gilmore SP, Borges-Rivera D, Lipzen A, et al. Early-branching gut fungi possess a large, comprehensive array of biomass-degrading enzymes. Science. 2016;351:1192–5.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Stewart RD, Auffret MD, Warr A, Wiser AH, Press MO, Langford KW, et al. Assembly of 913 microbial genomes from metagenomic sequencing of the cow rumen. Nat Commun. 2018;9:870.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Findley SD, Mormile MR, Sommer-Hurley A, Zhang X-C, Tipton P, Arnett K, et al. Activity-based metagenomic screening and biochemical characterization of bovine ruminal protozoan glycoside hydrolases. Appl Environ Microbiol. 2011;77:8106–13.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Takenaka A, Tajima K, Mitsumori M, Kajikawa H. Fiber digestion by rumen ciliate protozoa. Microbes Environ. 2004;19:203–10.

    Article  Google Scholar 

  87. Rubino F, Carberry C, M Waters S, Kenny D, McCabe MS, Creevey CJ. Divergent functional isoforms drive niche specialisation for nutrient acquisition and use in rumen microbiome. ISME J. 2017;11:932–44.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Brochet S, Quinn A, Mars RA, Neuschwander N, Sauer U, Engel P. Niche partitioning facilitates coexistence of closely related honey bee gut bacteria. eLife. 2021;10:e68583.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Andersson JO. Lateral gene transfer in eukaryotes. Cell Mol Life Sci. 2005;62:1182–97.

    Article  PubMed  CAS  Google Scholar 

  90. Xie F, Jin W, Si H, Yuan Y, Tao Y, Liu J, et al. An integrated gene catalog and over 10,000 metagenome-assembled genomes from the gastrointestinal microbiome of ruminants. Microbiome. 2021;9:137.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Ellison MJ, Conant GC, Cockrum RR, Austin KJ, Truong H, Becchi M, et al. Diet alters both the structure and taxonomy of the ovine gut microbial ecosystem. DNA Res. 2014;21:115–25.

    Article  PubMed  CAS  Google Scholar 

  92. Hook SE, Steele MA, Northwood KS, Wright A-DG, McBride BW. Impact of high-concentrate feeding and low ruminal pH on methanogens and protozoa in the rumen of dairy cows. Micro Ecol. 2011;62:94–105.

    Article  CAS  Google Scholar 

  93. Li J, Zhong H, Ramayo-Caldas Y, Terrapon N, Lombard V, Potocki-Veronese G, et al. A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment. GigaScience. 2020;9:giaa057.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Shang Z, Wang X, Jiang Y, Li Z, Ning J. Identifying rumen protozoa in microscopic images of ruminant with improved YOLACT instance segmentation. Biosyst Eng. 2022;215:156–69.

    Article  CAS  Google Scholar 

  95. Shen J, Zheng L, Chen X, Han X, Cao Y, Yao J. Metagenomic analyses of microbial and carbohydrate-active enzymes in the rumen of dairy goats fed different rumen degradable starch. Front Microbiol. 2020;11:1003.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Contributions

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.

Corresponding authors

Correspondence to Huoqing Huang or Yu Jiang.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Li, Z., Wang, X., Zhang, Y. et al. Genomic insights into the phylogeny and biomass-degrading enzymes of rumen ciliates. ISME J 16, 2775–2787 (2022). https://doi.org/10.1038/s41396-022-01306-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

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

Search

Quick links