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Cited by 367Ruminant Nutrition and Digestive PhysiologyAnaerobic Digestion and Biogas ProductionMicrobial metabolism and enzyme function

Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen

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Poulsen, Morten, Schwab, Clarissa, Borg Jensen, Bent, Engberg, Ricarda M., Spang, Anja, Canibe, Nuria, Højberg, Ole, Milinovich, Gabriel +6 more·2013·Nature Communications
DOI 10.1038/ncomms2432
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Abstract

Rumen methanogens are major sources of anthropogenic methane emissions, and these archaea are targets in strategies aimed at reducing methane emissions. Here we show that the poorly characterised Thermoplasmata archaea in bovine rumen are methylotrophic methanogens and that they are reduced upon dietary supplementation with rapeseed oil in lactating cows. In a metatranscriptomic survey, Thermoplasmata 16S rRNA and methyl-coenzyme M reductase (mcr) transcripts decreased concomitantly with mRNAs of enzymes involved in methanogenesis from methylamines that were among the most abundant archaeal transcripts, indicating that these Thermoplasmata degrade methylamines. Their methylotrophic methanogenic lifestyle was corroborated by in vitro incubations, showing enhanced growth of these organisms upon methylamine supplementation paralleled by elevated methane production. The Thermoplasmata have a high potential as target in future strategies to mitigate methane emissions from ruminant livestock. Our findings and the findings of others also indicate a wider distribution of methanogens than previously anticipated. Rumen methanogenic archaea are major sources of methane emissions and potential targets for methane mitigation strategies. Poulsen et al.now show that dietary rapeseed oil (RSO) supplementation can reduce the abundance of methanogenic Thermoplasmata archaea inhabiting the bovine rumen.

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  • During rumen fermentation, CO2 and H2 are converted into CH4 by methanogens like Methanopyrales, Methanomicrobiales, Methanobacteriales, Methanococcales, Methanocellales, and Methanosarcinales.

    “During rumen fermentation of feed, some by-products are additionally produced, such as CO2 and H2, which are further converted into CH4 by some methanogens like Methanopyrales, Methanomicrobiales, Methanobacteriales, Methanococcales, Methanocellales, and Methanosarcinales).”

    From Phytogenic Additives Can Modulate Rumen Microbiome to Mediate Fermentation Kinetics and Methanogenesis Through Exploiting Diet–Microbe Interaction (2020) · cites this paper as [8]

    Our copy says that rumen methanogens in Methanobacteriales and Methanomicrobiales use H₂/CO₂ produced during fermentation (Abstract; page unavailable). It does not identify Methanopyrales, Methanococcales, Methanocellales, or Methanosarcinales as rumen methanogens carrying out that conversion; the Rumen metatranscriptomics section instead identifies Methanobacteriales and RCC Thermoplasmata in the sampled rumen community. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • The genus Methanobrevibacter is the most ubiquitous and predominant hydrogenotrophic methanogen in the foregut and hindgut of herbivores.

    “The genus Methanobrevibacter is the most ubiquitous and predominant hydrogenotrophic methanogens found in the foregut and hindgut of herbivores (Kušar and Avguštin, 2010; St-Pierre and Wright, 2013) although several species of Methanomassiliicoccales can use methyl substrates (Poulsen et al., 2013).”

    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 Poulsen et al., 2013

    Poulsen et al. is attached to the sentence’s methyl-substrate clause, not to the preceding claim about Methanobrevibacter. The section “Methylotrophic methanogenesis from methylamines (MAs)” reports methylamine use by rumen-cluster Thermoplasmata and methanol use by the related Methanomassiliicoccus luminyensis. It does not establish that several identified species can use methyl substrates. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • Some archaea (Methanoplasmatales or Thermoplasmatales) can form CH4 through substrates such as methanol and mono-, di-, and tri-methylamine.

    “Some archaea (Methanoplasmatales or Thermoplasmatales) can also form CH4 through other substrates, such as methanol and mono-, di-, and tri-methylamine (6–8).”

    From Phytogenic Additives Can Modulate Rumen Microbiome to Mediate Fermentation Kinetics and Methanogenesis Through Exploiting Diet–Microbe Interaction (2020) · cites this paper as [8]

  • Methanogenesis in the rumen and hindgut is predominantly driven via the hydrogenotrophic pathway using H2 and CO2 (also formate) as substrates.

    “Methanogenesis in the rumen and hindgut is predominately driven via the hydrogenotrophic pathway using hydrogen (H2) and CO2 (also formate) as the substrates (Liu and Whitman, 2008) though some CH4 is also produced through the methylotrophic methanogenesis pathway using methanol and methylamines as the substrates (Poulsen et al., 2013).”

    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 Poulsen et al., 2013

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Authors
Poulsen, M., Schwab, C., Borg Jensen, B., Engberg, R. M., Spang, A., Canibe, N., Højberg, O., Milinovich, G., Fragner, L., Schleper, C., Weckwerth, W., Lund, P., Schramm, A., & Urich, T.
Affiliations
  • Aarhus University (DK)
  • University of Vienna (AT)
Corresponding author
  • Poulsen, Morten
  • Urich, Tim
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2013-02-05
Volume
4
Issue
1
Pages
1428-1428
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/ncomms2432
OpenAlex
W1996457200
Cited by
361
References
38
Citations by year
2026: 10 · 2025: 18 · 2024: 23 · 2023: 23 · 2022: 26 · 2021: 24 · 2020: 33 · 2019: 29 · 2018: 36 · 2017: 38 · 2016: 23 · 2015: 39 · 2014: 26 · 2013: 13
FWCI
71.54
Type
journal article
Language
en
Update notices
erratum (2013-06-06)
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
  • Phaidra (Universität Wien) (submittedVersion, cc-by-nc-nd)
  • RePEc: Research Papers in Economics (submittedVersion)
Funders
  • Aarhus Universitet
  • Bundesministerium für Wissenschaft und Forschung
  • Naturvidenskab og Teknologi, Aarhus Universitet
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 › Microbial metabolism and enzyme function
Keywords
Thermoplasmata, methanogenic archaea, rumen, methylotrophic methanogenesis, methyl-coenzyme M reductase, lactating dairy cows, methane mitigation, ruminant livestock, metatranscriptomics
MeSH terms
Rapeseed Oil, Animals, Cattle, Fatty Acids, Monounsaturated, Methane, Methylamines, Phylogeny, Plant Oils, RNA, Messenger, Rumen, Likelihood Functions, Dietary Supplements, Euryarchaeota, Metagenome, Nitrogen Cycle, Transcriptome

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