Rumen metagenome and metatranscriptome analyses of low methane yield sheep reveals a Sharpea-enriched microbiome characterised by lactic acid formation and utilisation
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BACKGROUND: Enteric fermentation by farmed ruminant animals is a major source of methane and constitutes the second largest anthropogenic contributor to global warming. Reducing methane emissions from ruminants is needed to ensure sustainable animal production in the future. Methane yield varies naturally in sheep and is a heritable trait that can be used to select animals that yield less methane per unit of feed eaten. We previously demonstrated elevated expression of hydrogenotrophic methanogenesis pathway genes of methanogenic archaea in the rumens of high methane yield (HMY) sheep compared to their low methane yield (LMY) counterparts. Methane production in the rumen is strongly connected to microbial hydrogen production through fermentation processes. In this study, we investigate the contribution that rumen bacteria make to methane yield phenotypes in sheep. RESULTS: Using deep sequence metagenome and metatranscriptome datasets in combination with 16S rRNA gene amplicon sequencing from HMY and LMY sheep, we show enrichment of lactate-producing Sharpea spp. in LMY sheep bacterial communities. Increased gene and transcript abundances for sugar import and utilisation and production of lactate, propionate and butyrate were also observed in LMY animals. Sharpea azabuensis and Megasphaera spp. act as important drivers of lactate production and utilisation according to phylogenetic analysis and read mappings. CONCLUSIONS: Our findings show that the rumen microbiome in LMY animals supports a rapid heterofermentative growth, leading to lactate production. We postulate that lactate is subsequently metabolised mainly to butyrate in LMY animals, producing 2 mol of hydrogen and 0.5 mol of methane per mol hexose, which represents 24 % less than the 0.66 mol of methane formed from the 2.66 mol of hydrogen produced if hexose fermentation was directly to acetate and butyrate. These findings are consistent with the theory that a smaller rumen size with a higher turnover rate, where rapid heterofermentative growth would be an advantage, results in lower hydrogen production and lower methane formation. Together with previous methanogen gene expression data, this builds a strong concept of how animal traits and microbial communities shape the methane phenotype in sheep.
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In the rumens of high methane-emitting sheep, members of Ruminococcaceae and Lachnospiraceae were found at higher relative abundance, while the rumens of low methane-emitting sheep were enriched with Erysipelotrichaceae, especially Sharpea spp.
“In the rumens of high methane-emitting sheep, members of Ruminococcaceae and Lachnospiraceae were found at higher relative abundance, while the rumens of low methane-emitting sheep were enriched with Erysipelotrichaceae, especially Sharpea spp. (Kamke et al., 2016).”
From Comparative Analysis of the Microbiota Between Sheep Rumen and Rabbit Cecum Provides New Insight Into Their Differential Methane Production (2018) · cites this paper as Kamke et al., 2016
Density of Sharpea has been shown to be significantly lower in low methane emitting animals.
“When investigating the rumen bacterial associations with methane production, density of Sharpea has been shown to be significantly lower in low methane emitting animals (Kamke et al., 2016).”
From Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future (2018) · cites this paper as Kamke et al., 2016
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- Authors
- Kamke, J., Kittelmann, S., Soni, P., Li, Y., Tavendale, M., Ganesh, S., Janssen, P. H., Shi, W., Froula, J., Rubin, E. M., & Attwood, G. T.
- Affiliations
- AgResearch (NZ)
- Lawrence Berkeley National Laboratory (US)
- Corresponding author
- Attwood, Graeme T.
- ORCID
- Venue
- Microbiome
- Published
- 2016-10-19
- Volume
- 4
- Issue
- 1
- Pages
- 56-56
- ISSN
- 2049-2618 (ISSN-L)
- PMC
- PMC5069950
- OpenAlex
- W2534284271
- Cited by
- 339
- References
- 52
- Citations by year
- 2026: 27 · 2025: 27 · 2024: 46 · 2023: 38 · 2022: 52 · 2021: 38 · 2020: 41 · 2019: 25 · 2018: 29 · 2017: 15
- FWCI
- 48.45
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Microbiome (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- New Zealand Fund for Global Partnerships in Livestock Emissions Research (15809)
- Office of Science of the U.S. Department of Energy (DE-AC02-05CH11231)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Ruminant Nutrition and Digestive Physiology
- Physical Sciences › Engineering › Building and Construction › Anaerobic Digestion and Biogas Production
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- rumen microbiome, Megasphaera, lactic acid production, hydrogen production, enteric methane, rumen bacteria, butyrate, propionate, sugar metabolism
- MeSH terms
- Animals, Bacteria, Base Sequence, Butyrates, Fatty Acids, Fermentation, Hexoses, Lactobacillaceae, Methane, Propionates, RNA, Ribosomal, 16S, Rumen, Sheep, Sequence Analysis, DNA, Lactic Acid, Metagenome, Global Warming, High-Throughput Nucleotide Sequencing, Microbiota
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