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Cited by 374Ruminant Nutrition and Digestive PhysiologyGenetic and phenotypic traits in livestockAnaerobic Digestion and Biogas Production

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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

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Roehe, Rainer, Dewhurst, Richard J., Duthie, Carol-Anne, Rooke, John A., McKain, Nest, Ross, Dave W., Hyslop, Jimmy J., Waterhouse, Anthony, Freeman, Tom C., Watson, Mick, Wallace, R. John·2016·PLoS Genetics
DOI 10.1371/journal.pgen.1005846PMC PMC4758630
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Abstract

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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Crossref · 10.1371/journal.pgen.1005846

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Fig 1 Distribution of methane emissions and archaea:bacteria ratios within breed type and diet. The box plot shows the large variation and range of methane emissions (per day or per kg DMI = dry matter intake) and archaea:bacteria ratios within crossbred breed type (AA = Aberdeen Angus sired, LIM = Limousin sired) and diet (CON = concentrate based diet, FOR = forage based diet). The total number of animals in the 2 × 2 factorial design experiment was 68.
Fig 1 Distribution of methane emissions and archaea:bacteria ratios within breed type and diet. The box plot shows the large variation and range of methane emissions (per day or per kg DMI = dry matter intake) and archaea:bacteria ratios within crossbred breed type (AA = Aberdeen Angus sired, LIM = Limousin sired) and diet (CON = concentrate based diet, FOR = forage based diet). The total number of animals in the 2 × 2 factorial design experiment was 68.CC BY · PubMed Central
Fig 2 Host genetic effects on methane emissions and relative microbial abundance. Host genetic effects were estimated by least squares means (± standard errors, different letters above bars indicate significant different estimates) of sire progeny groups (AA = Aberdeen Angus sired, LIM = Limousin sired) adjusted for diet, respiration chamber and randomized block effects. Relative microbial abundance was calculated as archaea:bacteria ratio.
Fig 2 Host genetic effects on methane emissions and relative microbial abundance. Host genetic effects were estimated by least squares means (± standard errors, different letters above bars indicate significant different estimates) of sire progeny groups (AA = Aberdeen Angus sired, LIM = Limousin sired) adjusted for diet, respiration chamber and randomized block effects. Relative microbial abundance was calculated as archaea:bacteria ratio.CC BY · PubMed Central
Fig 3 Functional clusters of microbial genes identified using network analysis. (A) Correlation analysis of microbial gene abundance was used to construct networks, where nodes represent microbial genes and edges the correlation in their abundance. Networks were clustered using the MCL algorithm and the profiles of clusters 1 to 6 are shown. Each chart represents the average abundance of genes in a cluster across the animals studied. Animals are ordered alternately being low (red bar beneath plot) and high methane emitter (yellow), whereby the first and last 4 bars represent animals offered concentrate (green) and forage (light blue) diets, respectively. See S2 Table for KEGG genes associated within each cluster. (B) Microbial gene networks of cluster 4 and 6 contained most of the microbial genes associated with methane metabolism; explicitly shown in yellow are the KEGG genes identified by the PLS analysis to be most closely associated with methane emissions (see Fig 4 and S3 Table).
Fig 3 Functional clusters of microbial genes identified using network analysis. (A) Correlation analysis of microbial gene abundance was used to construct networks, where nodes represent microbial genes and edges the correlation in their abundance. Networks were clustered using the MCL algorithm and the profiles of clusters 1 to 6 are shown. Each chart represents the average abundance of genes in a cluster across the animals studied. Animals are ordered alternately being low (red bar beneath plot) and high methane emitter (yellow), whereby the first and last 4 bars represent animals offered concentrate (green) and forage (light blue) diets, respectively. See S2 Table for KEGG genes associated within each cluster. (B) Microbial gene networks of cluster 4 and 6 contained most of the microbial genes associated with methane metabolism; explicitly shown in yellow are the KEGG genes identified by the PLS analysis to be most closely associated with methane emissions (see Fig 4 and S3 Table).CC BY · PubMed Central
Fig 4 Heatmap of the relative abundance of microbial genes associated with methane emissions as identified in the partial least squares analysis. The relative abundance of microbial genes (blue = low to yellow = high) changed depending on methane emissions (g/kg DMI) for the animals selected for low and high methane emissions within breed type and diet. The labels on the horizontal axis indicate the crossbred breed type (AA = Aberdeen Angus sired, LIM = Limousin sired), diet (CON = concentrate based diet, FOR = forage based diet) and the amount of methane emissions (g/kg DMI).
Fig 4 Heatmap of the relative abundance of microbial genes associated with methane emissions as identified in the partial least squares analysis. The relative abundance of microbial genes (blue = low to yellow = high) changed depending on methane emissions (g/kg DMI) for the animals selected for low and high methane emissions within breed type and diet. The labels on the horizontal axis indicate the crossbred breed type (AA = Aberdeen Angus sired, LIM = Limousin sired), diet (CON = concentrate based diet, FOR = forage based diet) and the amount of methane emissions (g/kg DMI).CC BY · PubMed Central
Fig 5 Heatmap of the relative abundance of microbial genes associated with feed conversion efficiency as identified in the partial least squares analysis. The relative abundance of microbial genes (blue = low to yellow = high) changed depending on feed conversion ratio (kg feed intake/kg growth) for the animals selected for low and high methane emissions within breed type and diet. The labels on the horizontal axis represent the breed type (AA = Aberdeen Angus sired, LIM = Limousin sired), diet (CON = concentrate based diet, FOR = forage based diet) and the feed conversion ratio (kg daily feed intake / kg daily growth).
Fig 5 Heatmap of the relative abundance of microbial genes associated with feed conversion efficiency as identified in the partial least squares analysis. The relative abundance of microbial genes (blue = low to yellow = high) changed depending on feed conversion ratio (kg feed intake/kg growth) for the animals selected for low and high methane emissions within breed type and diet. The labels on the horizontal axis represent the breed type (AA = Aberdeen Angus sired, LIM = Limousin sired), diet (CON = concentrate based diet, FOR = forage based diet) and the feed conversion ratio (kg daily feed intake / kg daily growth).CC BY · PubMed Central

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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
DOI
10.1371/journal.pgen.1005846
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
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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