Cited by 600Genomics and Phylogenetic StudiesRuminant Nutrition and Digestive PhysiologyAnaerobic Digestion and Biogas Production

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Assembly of 913 microbial genomes from metagenomic sequencing of the cow rumen

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Stewart, Robert D., Auffret, Marc D., Warr, Amanda, Wiser, Andrew H., Press, Maximilian O., Langford, Kyle W., Liachko, Ivan, Snelling, Timothy J., Dewhurst, Richard J., Walker, Alan W., Roehe, Rainer, Watson, Mick·2018·Nature Communications

DOI 10.1038/s41467-018-03317-6PMC PMC5830445

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Abstract

The cow rumen is adapted for the breakdown of plant material into energy and nutrients, a task largely performed by enzymes encoded by the rumen microbiome. Here we present 913 draft bacterial and archaeal genomes assembled from over 800 Gb of rumen metagenomic sequence data derived from 43 Scottish cattle, using both metagenomic binning and Hi-C-based proximity-guided assembly. Most of these genomes represent previously unsequenced strains and species. The draft genomes contain over 69,000 proteins predicted to be involved in carbohydrate metabolism, over 90% of which do not have a good match in public databases. Inclusion of the 913 genomes presented here improves metagenomic read classification by sevenfold against our own data, and by fivefold against other publicly available rumen datasets. Thus, our dataset substantially improves the coverage of rumen microbial genomes in the public databases and represents a valuable resource for biomass-degrading enzyme discovery and studies of the rumen microbiome.

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Fig. 1 Phylogenetic tree of 913 draft genomes from the cow rumen, and closely related public genomes including 15 binned genomes from Hess et al1. Coloured circles represent the RUGs. White circles represent public genomes and have corresponding labelsCC BY · PubMed Central

Fig. 2 Distribution of carbohydrate-active enzyme classes across the 913 RUGs. GH glycoside hydrolase, GT glycosyl transferase, PL polysaccharide lyases, CE carbohydrate esterases, AA auxiliary activities, CB carbohydrate binding. White = absent, dark red = abundantCC BY · PubMed Central

Fig. 3 Distribution of the maximum percentage identity of the RUG proteins against five public databases for six classes of carbohydrate-active enzymes. GH glycoside hydrolase, GT glycosyl transferase, PL polysaccharide lyases, CE carbohydrate esterases, AA auxiliary activities, CB carbohydrate bindingCC BY · PubMed Central

Fig. 4 Classification rate for three datasets against various Kraken databases. BFAP bacterial, archaeal, fungal and protozoan genomes from RefSeq, BGEB BFAP + 1003 GEBA genomes, BHIC BFAP + 63 hRUG genomes, BHUN BFAP + 410 genomes from the Hungate 1000 project, BRUG BFAP + 850 RUG MAGs, BRHI BFAP + all 913 genomes from this study, BRHH BFAP + 913 RUGs + 410 Hungate 1000 genomes. Addition of rumen-specific RUGs or Hungate 1000 genomes has the most dramatic effectCC BY · PubMed Central

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Faculty Opinions recommendation of New insights from uncultivated genomes of the global human gut microbiome.
Gaston, H. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.735313835.793562946
Peer Review #3 of "Yak rumen microbial diversity at different forage growth stages of an alpine meadow on the Qinghai-Tibet Plateau (v0.2)"
(2019) · PeerJ · doi:10.7287/peerj.7645v0.2/reviews/3
“This method has been used in previous studies (Ramos143 Morales et al. 2014; Xue et al. 2017; Sun et al. 2018), and they have shown that the stomach tube and 144 rumen cannulation methods do not have any influence on the results.”
Method
Peer Review #2 of "Yak rumen microbial diversity at different forage growth stages of an alpine meadow on the Qinghai-Tibet Plateau (v0.1)"
(2019) · PeerJ · doi:10.7287/peerj.7645v0.1/reviews/2
Faculty Opinions recommendation of Fecal pollution can explain antibiotic resistance gene abundances in anthropogenically impacted environments.
MacLean, C. R. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.734774541.793557712
Phylogenetic systematics of Butyrivibrio and Pseudobutyrivibrio pure culture and metagenomically assembled genomes suggest existence of 59 genera and 75 species, alongside possession of open pangenomes with an abundance of carbohydrate-active enzyme family isoformsPreprint
Pidcock, S., Skvortsov, T., Courtney, S. J., Creevey, C. J., & Huws, S. (2022) · Research Square · doi:10.21203/rs.3.rs-2289353/v1
Microbial colonisation of low-quality fodders in the bovine rumen
Abbasabadi, M. (2022) · Queensland University of Technology · doi:10.5204/thesis.eprints.236799
МЕТАНООБРАЗОВАНИЕ В РУБЦЕ И МЕТОДЫ ЕГО СНИЖЕНИЯ С ИСПОЛЬЗОВАНИЕМ АЛИМЕНТАРНЫХ ФАКТОРОВ (обзор)
Эрнста, Ф. И. Ц. Ж. —. В. А. К., & БОГОЛЮБОВА, Н. В. (2023) · Sel skokhozyaistvennaya Biologiya · doi:10.15389/agrobiology.2022.6.1025rus · Cited by 5
Characterization of comammox bacteria in wastewater secondary treatment systems
Cotto, I. (2022) · doi:10.17760/d20467262
Integrated de novo gene prediction and peptide assembly of metagenomic sequencing data
Thippabhotla, S., Liu, B., Podgorny, A., Yooseph, S., Yang, Y., Zhang, J., & Zhong, C. (2023) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqad023
“We used six real datasets from different environments (from human gut (61), soil (62), marine (63), cow rumen (64), a mock community, and sugarcane rhizosphere) to benchmark iMPP.”
Method
Temporal colonization of the gut microbiome in neonatal Bos taurus at single nucleotide resolutionPreprint
Dong, Q., Hua, D., Wang, X., Jiao, Y., Liu, L., Deng, Q., Wu, T., Zou, H., Ding, L., Hu, S., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.03.30.535011
“We compared these representative 101 genomes with existing microbial genomes obtained from cattle, including RUG [16], RUG2.”
BackgroundResultInfluential
Dietary n-3 PUFA Enhances DMI in Transition Cows by Regulating Taste Transduction Gene Expression in Liver Associated with Rumen Microbial AlterationPreprint
Sun, X., Guo, C., Wang, Q., Zhang, Y., Wang, Z., Cao, Z., Wang, W., & Li, S. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.07.24.550439
Rodents consuming the same toxic diet harbor a unique taxonomic and functional core microbiomePreprint
Stapleton, T. E., Lindsey, L. M., Sundar, H., & Dearing, M. D. (2023) · Research Square · doi:10.21203/rs.3.rs-3419959/v1
Identifying Mobile Genetic Elements in the Ruminal Microbiome of Nellore Cattle: An Initial InvestigationPreprint
Faleiros, C. A., Nunes, A. T., Gonçalves, O. S., Alexandre, P. A., Poleti, M., Oliveira, E. C. M., Perna, F., Rodrigues, P. H. M., & Fukumasu, H. (2024) · Research Square · doi:10.21203/rs.3.rs-3749940/v1
Removal of sequencing adapter contamination improves microbial genome databasesPreprint
Moeller, A. H., Dillard, B. A., Goldman, S. L., Real, M. V. F., & Sprockett, D. D. (2024) · Research Square · doi:10.21203/rs.3.rs-3888769/v1
Development of novel tools for monitoring antimicrobial resistance in complex microbial communities and their application to improving our stewardship of antimicrobials in livestock
Beyi, A. F. (2021) · doi:10.31274/td-20240329-235
Additional file 5 of Metagenomic insights into the microbe-mediated B and K2 vitamin biosynthesis in the gastrointestinal microbiome of ruminants
Jiang, Q., Lin, L., Xie, F., Jin, W., Zhu, W., Wang, M., Qiu, Q., Li, Z., Liu, J., & Mao, S. (2022) · Figshare · doi:10.6084/m9.figshare.20356425
Additional file 8 of An integrated gene catalog and over 10,000 metagenome-assembled genomes from the gastrointestinal microbiome of ruminants
Xie, F., Jin, W., Si, H., Yuan, Y., Tao, Y., Liu, J., Wang, X., Yang, C., Li, Q., Yan, X., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14775444
Additional file 3 of An integrated gene catalog and over 10,000 metagenome-assembled genomes from the gastrointestinal microbiome of ruminants
Xie, F., Jin, W., Si, H., Yuan, Y., Tao, Y., Liu, J., Wang, X., Yang, C., Li, Q., Yan, X., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14775423
Additional file 11 of Expanded catalogue of metagenome-assembled genomes reveals resistome characteristics and athletic performance-associated microbes in horse
Li, C., Li, X., Guo, R., Ni, W., Liu, K., Liu, Z., Dai, J., Xu, Y., Abduriyim, S., Wu, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22610680
Additional file 18 of Expanded catalogue of metagenome-assembled genomes reveals resistome characteristics and athletic performance-associated microbes in horse
Li, C., Li, X., Guo, R., Ni, W., Liu, K., Liu, Z., Dai, J., Xu, Y., Abduriyim, S., Wu, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22610704
Additional file 4 of An integrated gene catalog and over 10,000 metagenome-assembled genomes from the gastrointestinal microbiome of ruminants
Xie, F., Jin, W., Si, H., Yuan, Y., Tao, Y., Liu, J., Wang, X., Yang, C., Li, Q., Yan, X., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14775429
Additional file 3 of Metagenomic insights into the microbe-mediated B and K2 vitamin biosynthesis in the gastrointestinal microbiome of ruminants
Jiang, Q., Lin, L., Xie, F., Jin, W., Zhu, W., Wang, M., Qiu, Q., Li, Z., Liu, J., & Mao, S. (2022) · Figshare · doi:10.6084/m9.figshare.20356419
Additional file 10 of Expanded catalogue of metagenome-assembled genomes reveals resistome characteristics and athletic performance-associated microbes in horse
Li, C., Li, X., Guo, R., Ni, W., Liu, K., Liu, Z., Dai, J., Xu, Y., Abduriyim, S., Wu, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22610677
Additional file 1 of Expanded catalogue of metagenome-assembled genomes reveals resistome characteristics and athletic performance-associated microbes in horse
Li, C., Li, X., Guo, R., Ni, W., Liu, K., Liu, Z., Dai, J., Xu, Y., Abduriyim, S., Wu, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22610650
Additional file 7 of An integrated gene catalog and over 10,000 metagenome-assembled genomes from the gastrointestinal microbiome of ruminants
Xie, F., Jin, W., Si, H., Yuan, Y., Tao, Y., Liu, J., Wang, X., Yang, C., Li, Q., Yan, X., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14775441
Additional file 1 of Holistic view of the seascape dynamics and environment impact on macro-scale genetic connectivity of marine plankton populations
Laso‐Jadart, R., O’Malley, M., Sykulski, A. M., Ambroise, C., & Madoui, M. (2023) · Figshare · doi:10.6084/m9.figshare.24076955
Additional file 9 of Expanded catalogue of metagenome-assembled genomes reveals resistome characteristics and athletic performance-associated microbes in horse
Li, C., Li, X., Guo, R., Ni, W., Liu, K., Liu, Z., Dai, J., Xu, Y., Abduriyim, S., Wu, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22610674
Additional file 2 of Expanded catalogue of metagenome-assembled genomes reveals resistome characteristics and athletic performance-associated microbes in horse
Li, C., Li, X., Guo, R., Ni, W., Liu, K., Liu, Z., Dai, J., Xu, Y., Abduriyim, S., Wu, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22610653
Additional file 7 of Expanded catalogue of metagenome-assembled genomes reveals resistome characteristics and athletic performance-associated microbes in horse
Li, C., Li, X., Guo, R., Ni, W., Liu, K., Liu, Z., Dai, J., Xu, Y., Abduriyim, S., Wu, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22610668
Additional file 22 of Expanded catalogue of metagenome-assembled genomes reveals resistome characteristics and athletic performance-associated microbes in horse
Li, C., Li, X., Guo, R., Ni, W., Liu, K., Liu, Z., Dai, J., Xu, Y., Abduriyim, S., Wu, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22610719
Additional file 16 of Expanded catalogue of metagenome-assembled genomes reveals resistome characteristics and athletic performance-associated microbes in horse
Li, C., Li, X., Guo, R., Ni, W., Liu, K., Liu, Z., Dai, J., Xu, Y., Abduriyim, S., Wu, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22610695
Additional file 5 of An integrated gene catalog and over 10,000 metagenome-assembled genomes from the gastrointestinal microbiome of ruminants
Xie, F., Jin, W., Si, H., Yuan, Y., Tao, Y., Liu, J., Wang, X., Yang, C., Li, Q., Yan, X., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14775432
Additional file 14 of Expanded catalogue of metagenome-assembled genomes reveals resistome characteristics and athletic performance-associated microbes in horse
Li, C., Li, X., Guo, R., Ni, W., Liu, K., Liu, Z., Dai, J., Xu, Y., Abduriyim, S., Wu, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22610689
Additional file 23 of Expanded catalogue of metagenome-assembled genomes reveals resistome characteristics and athletic performance-associated microbes in horse
Li, C., Li, X., Guo, R., Ni, W., Liu, K., Liu, Z., Dai, J., Xu, Y., Abduriyim, S., Wu, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22610722

Authors: Stewart, R. D., Auffret, M. D., Warr, A., Wiser, A. H., Press, M. O., Langford, K. W., Liachko, I., Snelling, T. J., Dewhurst, R. J., Walker, A. W., Roehe, R., & Watson, M.
Affiliations: Roslin Institute (GB)
Scotland's Rural College (GB)
University of Aberdeen (GB)
Corresponding author: Watson, Mick
ORCID: Auffret, Marc D.
Warr, Amanda
Press, Maximilian O.
Langford, Kyle W.
Liachko, Ivan
Snelling, Timothy J.
Dewhurst, Richard J.
Walker, Alan W.
Roehe, Rainer
Watson, Mick
Venue: Nature Communications
Publisher: Springer Science and Business Media LLC
Published: 2018-02-28
Volume: 9
Issue: 1
Pages: 870-870
ISSN: 2041-1723 (ISSN-L)
DOI: 10.1038/s41467-018-03317-6
PMC: PMC5830445
OpenAlex: W2786358949
Cited by: 559
References: 83
Citations by year: 2026: 39 · 2025: 48 · 2024: 77 · 2023: 69 · 2022: 64 · 2021: 73 · 2020: 89 · 2019: 73 · 2018: 27
FWCI: 24.09
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Nature Communications (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Edinburgh Research Explorer (University of Edinburgh) (publishedVersion, cc-by)
RePEc: Research Papers in Economics (submittedVersion)
Aberdeen University Research Archive (Aberdeen University) (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: Rural and Environment Science and Analytical Services Division
Scottish Government
Scotland’s Rural College
Directorate for Biological Sciences
Biotechnology and Biological Sciences Research Council (BBS/E/D/30002276, BB/M01844X/1, BB/J004235/1, BB/R015023/1, BB/P013732/1, BB/J004235, BB/N016742/1, BB/ J004243/1, BB/N01720X/1, P013759, BBP013759/1, BBS/E/D/20310000)
National Institute of Allergy and Infectious Diseases (R43AI122654, R44AI122654)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Ruminant Nutrition and Digestive Physiology
Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Anaerobic Digestion and Biogas Production
Keywords: rumen microbiome, draft genome sequence, metagenome binning, Hi-C, cattle, rumen bacteria, rumen archaea, carbohydrate metabolism, biomass-degrading enzymes, metagenome-assembled genomes, read classification
MeSH terms: Animals, Bacteria, Bacterial Proteins, Cattle, Phylogeny, Rumen, Genome, Bacterial, Metagenome, Metagenomics

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Assembly of 913 microbial genomes from metagenomic sequencing of the cow rumen

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