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Assembly of 913 microbial genomes from metagenomic sequencing of the cow rumen
Open accessAbstract
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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“Subsequently, Svartstrom et al. (2017) assembled 99 microbial genomes from the moose rumen, Stewart et al. (2018) assembled 913 microbial genomes from the rumen of cattle, and Parks et al. (2017) assembled over 8,000 novel microbial genomes from 1,500 public datasets, some of which originated from the rumen.”
From Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future (2018) · cites this paper as Stewart et al., 2018
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“Hi-C binning has been used effectively on human feces (Press et al., 2017) as well as in ruminants (Stewart et al., 2018).”
From Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future (2018) · cites this paper as Stewart et al., 2018
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“The rumen microbiota is largely underrepresented in databases and most of them have not been cultured yet (Stewart et al., 2018).”
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BackgroundInfluentialThe microbiome of the buffalo digestive tract
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Metage2Metabo, microbiota-scale metabolic complementarity for the identification of key species
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“It has been estimated that there are ~1 billion domesticated ruminant animals [1] and numbers are predicted to increase”
BackgroundMajor genetic discontinuity and novel toxigenic species in Clostridioides difficile taxonomy
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“Our catalog displays similar features with mean 73% identity to the MAGs of Genbank and Stewart et al. [6] and 89% novel CAZymes (482,759 sequences with < 95% identity).”
InfluentialLong-read metagenomic exploration of extrachromosomal mobile genetic elements in the human gut
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“However, consistent with the results of previous metagenomic binning studies, our results showed that a large number of unclassified microbial genomes and genomes could not be resolved to the species level, with many MAGs recovered at only the kingdom level [3, 10, 12].”
BackgroundResultInfluentialJiang, Q., Lin, L., Xie, F., Jin, W., Zhu, W., Wang, M., Qiu, Q., Li, Z., Liu, J., & Mao, S. (2022) · Microbiome · doi:10.1186/s40168-022-01298-9 · Cited by 95
Genomic insights into the phylogeny and biomass-degrading enzymes of rumen ciliates
Li, Z., Wang, X., Zhang, Y., Yu, Z., Zhang, T., Dai, X., Pan, X., Jing, R., Yan, Y., Liu, Y., et al. (2022) · The ISME Journal · doi:10.1038/s41396-022-01306-8 · Cited by 100
“A broad array of CAZymes encoded by the rumen ciliate SAGs The gut microbes are of huge industrial interest due to their ability to release fermentable sugars from lignocellulose [72, 83, 84].”
BackgroundSoil Biogeochemical Cycle Couplings Inferred from a Function-Taxon Network
Ma, B., Stirling, E., Liu, Y., Zhao, K., Zhou, J. Z., Singh, B. K., Tang, C., Dahlgren, R. A., & Xu, J. M. (2021) · Research · doi:10.34133/2021/7102769 · Cited by 95
“Despite pioneering conceptual research [12], there is a paucity of information concerning the connection of microbial community composition to biogeochemical functions.”
BackgroundFibre digestion by rumen microbiota — a review of recent metagenomic and metatranscriptomic studies
Terry, S. A., Badhan, A., Wang, Y., Chaves, A. V., & McAllister, T. A. (2019) · Canadian Journal of Animal Science · doi:10.1139/cjas-2019-0024 · Cited by 94
“Similarly, Stewart et al. (2018) predicted 1743 putative PUL from the Prevotellaceae family.”
BackgroundMethodUnlocking gut-liver-brain axis communication metabolites: energy metabolism, immunity and barriers
Sun, X., Shukla, M., Wang, W., & Li, S. (2024) · npj Biofilms and Microbiomes · doi:10.1038/s41522-024-00610-9 · Cited by 101
“…that an average human male body harbors around 3.8 × 10 13 individual microorganisms 20 , the gut microbiota of mice contains approximately 1 × 10 13 to 1 × 10 14 microbes 21 , and the rumen microbiota of cows contains approximately 1 × 10 11 to 1 × 10 12 microbes per gram of rumen content 22 .”
InfluentialAccetto, T., & Avguštin, G. (2018) · Systematic and Applied Microbiology · doi:10.1016/j.syapm.2018.10.001 · Cited by 97
The Planktonic Core Microbiome and Core Functions in the Cattle Rumen by Next Generation Sequencing
Wirth, R., Kádár, G., Kakuk, B., Maróti, G., Bagi, Z., Szilágyi, Á., Rákhely, G., Horváth, J., & Kovács, K. L. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02285 · Cited by 90
Murphy, C. L., Youssef, N. H., Hanafy, R. A., Couger, M. B., Stajich, J., Wang, Y., Baker, K., Dagar, S. S., Griffith, G. W., Farag, I., et al. (2019) · Applied and Environmental Microbiology · doi:10.1128/aem.00988-19 · Cited by 88
“The majority of the putative donor taxa are strict/ facultative anaerobes, and many of which are also known to be major inhabitants of the herbivorous gut and often possess polysaccharide-degradation capabilities (51, 52).”
BackgroundTen common issues with reference sequence databases and how to mitigate them
Chorlton, S. D. (2024) · Frontiers in Bioinformatics · doi:10.3389/fbinf.2024.1278228 · Cited by 101
Understanding the microbial basis of body odor in pre-pubescent children and teenagers
Lam, T. H., Verzotto, D., Brahma, P., Ng, A. H. Q., Hu, P., Schnell, D. J., Tiesman, J. P., Kong, R., Ton, T. M. U., Li, J., et al. (2018) · Microbiome · doi:10.1186/s40168-018-0588-z · Cited by 90
Lima, J., Auffret, M. D., Stewart, R. D., Dewhurst, R. J., Duthie, C.-A., Snelling, T. J., Walker, A. W., Freeman, T. C., Watson, M., & Roehe, R. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00701 · Cited by 92
Probing the Mobilome: Discoveries in the Dynamic Microbiome
Carr, V. R., Shkoporov, A. N., Hill, C., Mullany, P. P., & Moyes, D. L. (2020) · Trends in Microbiology · doi:10.1016/j.tim.2020.05.003 · Cited by 86
Shen, J., Zheng, L., Chen, X., Han, X., Cao, Y., & Yao, J. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01003 · Cited by 84
Gharechahi, J., Sarikhan, S., Han, J., Ding, X., & Salekdeh, G. H. (2022) · npj Biofilms and Microbiomes · doi:10.1038/s41522-022-00309-9 · Cited by 85
Hi-C metagenome sequencing reveals soil phage–host interactions
Wu, R., Davison, M. R., Nelson, W. C., Smith, M. L., Lipton, M. S. W., Jansson, J. K., McClure, R., McDermott, J., & Hofmockel, K. (2023) · Nature Communications · doi:10.1038/s41467-023-42967-z · Cited by 82
“Metagenome deconvolution was performed with ProxiMeta 58,59 , which implements a graph-based clustering algorithm using the shotgun metagenome assembly and Hi-C mapping as input to generate metagenome-assembled genomes (MAGs).”
Qiu, Z. G., Yuan, L., Lian, C., Lin, B., Chen, J., Mu, R., Qiao, X., Zhang, L., Xu, Z., Fan, L., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-46539-7 · Cited by 86
“Although BASALT can function with only a single metagenomic dataset, the overall bin quality including MAG quality can be improved using multiple datasets and assemblies as inputs 36,83 .”
BackgroundMethodCurrent and Promising Approaches to Identify Horizontal Gene Transfer Events in Metagenomes
Douglas, G. M., & Langille, M. G. I. (2019) · Genome Biology and Evolution · doi:10.1093/gbe/evz184 · Cited by 80
Metatranscriptomics of the Hu sheep rumen microbiome reveals novel cellulases
He, B., Jin, S., Cao, J., Mi, L., & Wang, J. (2019) · Biotechnology for Biofuels · doi:10.1186/s13068-019-1498-4 · Cited by 83
Bertucci, M., Całusińska, M., Goux, X., Rouland-Lefèvre, C., Untereiner, B., Ferrer, P., Gerin, P. A., & Delfosse, P. (2019) · Applied and Environmental Microbiology · doi:10.1128/aem.00895-19 · Cited by 80
“AA class seemed more conserved (higher sequence similarity), as previously demonstrated for the cow rumen metagenome (36).”
BackgroundDiscovery of an Abundance of Biosynthetic Gene Clusters in Shark Bay Microbial Mats
Chen, R., Wong, H. L., Kindler, G. S., MacLeod, F. I., Benaud, N., Ferrari, B. C., & Burns, B. P. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01950 · Cited by 80
Bioinformatics in bioscience and bioengineering: Recent advances, applications, and perspectives
Uesaka, K., Oka, H., Kato, R., Kanie, K., Kojima, T., Tsugawa, H., Toda, Y., & Horinouchi, T. (2022) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2022.08.004 · Cited by 83
Metagenomic analysis of the cow, sheep, reindeer and red deer rumen
Glendinning, L., Genç, B., Wallace, R. J., & Watson, M. (2021) · Scientific Reports · doi:10.1038/s41598-021-81668-9 · Cited by 81
“Our group has previously published thousands of metagenome assembled genomes from 54 cattle rumen samples (19, 20) and hundreds of genomes from chicken caecal samples (21), many of 55 which were identified as novel species.”
BackgroundJia, M., Zhu, S., Xue, M., Chen, H., Xu, J., Song, M., Tang, Y., Liu, X., Tao, Y., Zhang, T., et al. (2024) · Nature Microbiology · doi:10.1038/s41564-024-01723-9 · Cited by 80
Bovo, S., Utzeri, V. J., Ribani, A., Cabbri, R., & Fontanesi, L. (2020) · Scientific Reports · doi:10.1038/s41598-020-66127-1 · Cited by 75
Sapountzis, P., Segura, A., Desvaux, M., & Forano, É. (2020) · Microorganisms · doi:10.3390/microorganisms8060877 · Cited by 77
“The native GIT microbiota is adapted to the breakdown of complex polysaccharides [94,102], unlike E.”
BackgroundWilkinson, T., Korir, D., Ogugo, M., Stewart, R. D., Watson, M., Paxton, E. A., Goopy, J. P., & Robert, C. (2020) · Genome biology · doi:10.1186/s13059-020-02144-7 · Cited by 76
“[11] (additional details in text) Wilkinson et al.”
BackgroundMethodInfluentialEarly-Life Immune System Maturation in Chickens Using a Synthetic Community of Cultured Gut Bacteria
Zenner, C., Hitch, T. C. A., Riedel, T., Wortmann, E., Tiede, S., Buhl, E. M., Abt, B., Neuhaus, K., Velge, P., Overmann, J., et al. (2021) · mSystems · doi:10.1128/msystems.01300-20 · Cited by 72
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Fu, J., Chen, L., Yang, S., Li, Y., Jin, L., He, X., He, L., Ao, X., Liu, S., Liu, A., et al. (2021) · Food Research International · doi:10.1016/j.foodres.2021.110294 · Cited by 74
Metadata
- 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
- Venue
- Nature Communications
- Published
- 2018-02-28
- Volume
- 9
- Issue
- 1
- Pages
- 870-870
- ISSN
- 2041-1723 (ISSN-L)
- 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
- 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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