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Bovine Host Genetic Variation Influences Rumen Microbial Methane Production with Best Selection Criterion for Low Methane Emitting and Efficiently Feed Converting Hosts Based on Metagenomic Gene Abundance
Open accessAbstract
Methane produced by methanogenic archaea in ruminants contributes significantly to anthropogenic greenhouse gas emissions. The host genetic link controlling microbial methane production is unknown and appropriate genetic selection strategies are not developed. We used sire progeny group differences to estimate the host genetic influence on rumen microbial methane production in a factorial experiment consisting of crossbred breed types and diets. Rumen metagenomic profiling was undertaken to investigate links between microbial genes and methane emissions or feed conversion efficiency. Sire progeny groups differed significantly in their methane emissions measured in respiration chambers. Ranking of the sire progeny groups based on methane emissions or relative archaeal abundance was consistent overall and within diet, suggesting that archaeal abundance in ruminal digesta is under host genetic control and can be used to genetically select animals without measuring methane directly. In the metagenomic analysis of rumen contents, we identified 3970 microbial genes of which 20 and 49 genes were significantly associated with methane emissions and feed conversion efficiency respectively. These explained 81% and 86% of the respective variation and were clustered in distinct functional gene networks. Methanogenesis genes (e.g. mcrA and fmdB) were associated with methane emissions, whilst host-microbiome cross talk genes (e.g. TSTA3 and FucI) were associated with feed conversion efficiency. These results strengthen the idea that the host animal controls its own microbiota to a significant extent and open up the implementation of effective breeding strategies using rumen microbial gene abundance as a predictor for difficult-to-measure traits on a large number of hosts. Generally, the results provide a proof of principle to use the relative abundance of microbial genes in the gastrointestinal tract of different species to predict their influence on traits e.g. human metabolism, health and behaviour, as well as to understand the genetic link between host and microbiome.
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“In a beef cattle experiment, Roehe et al. (2016) ranked beef sire progeny groups based on relative archaeal abundance and reported that group ranking remained consistent overall and within diet, suggesting that archaeal abundance in ruminal digesta is also, in part under host genetic control.”
From Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future (2018) · cites this paper as Roehe et al., 2016
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“Recent work using metagenomics and/or metatranscriptomics has confirmed significant relationships between the abundances of key rumen microbial genes and feed efficiency (Roehe et al., 2016; Shabat et al., 2016; Li and Guan, 2017) and/or methane production (Roehe et al., 2016).”
From Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future (2018) · cites this paper as Roehe et al., 2016
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“We are only in the early stages of applying these approaches to the rumen microbiome, and while network scaffolds for specific animal studies have been generated (Roehe et al., 2016), large-scale, integrative models have yet to be developed.”
From Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future (2018) · cites this paper as Roehe et al., 2016
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Metadata
- Authors
- Roehe, R., Dewhurst, R. J., Duthie, C.-A., Rooke, J. A., McKain, N., Ross, D. W., Hyslop, J. J., Waterhouse, A., Freeman, T. C., Watson, M., & Wallace, R. J.
- Affiliations
- Scotland's Rural College (GB)
- University of Aberdeen (GB)
- Roslin Institute (GB)
- Corresponding author
- Roehe, Rainer
- ORCID
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2016-02-18
- Volume
- 12
- Issue
- 2
- Pages
- e1005846
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC4758630
- OpenAlex
- W2275915069
- Cited by
- 359
- References
- 60
- Citations by year
- 2026: 29 · 2025: 27 · 2024: 33 · 2023: 33 · 2022: 30 · 2021: 39 · 2020: 51 · 2019: 33 · 2018: 42 · 2017: 32 · 2016: 10
- FWCI
- 81.88
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Aberdeen University Research Archive (Aberdeen University) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
- Funders
- Scottish Government
- Department for Environment, Food and Rural Affairs, UK Government
- Directorate for Biological Sciences
- Medical Research Council (MR/K001744/1)
- Biotechnology and Biological Sciences Research Council (BBS/E/D/05191132, BB/J004235/1, BBS/E/D/20211553, BBS/E/D/20211552, BBS/E/D/20211550, BBS/E/D/20211551, BB/N016742/1, BB/ J004243/1, BB/N01720X/1, BB/I001107/1, BBS/E/D/20310000)
- Natural Environment Research Council (NBAF010003)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Ruminant Nutrition and Digestive Physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Anaerobic Digestion and Biogas Production
- Keywords
- host genetic variation, methanogenic archaea, feed efficiency, rumen metagenomics, microbial gene abundance, diet effects, mcrA, host-microbiome interactions, genetic selection, livestock greenhouse gas emissions
- MeSH terms
- Animals, Animal Feed, Animal Nutritional Physiological Phenomena, Archaea, Cattle, Female, Male, Methane, Rumen, Genetic Variation, Metagenomics, Microbiota
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