Metagenomic analysis of the rumen microbial community following inhibition of methane formation by a halogenated methane analog

Denman, Stuart E.; Fernández, Gonzalo Martínez; Shinkai, Takumi; Mitsumori, Makoto; McSweeney, Christopher S.

doi:10.3389/fmicb.2015.01087

Cited by 105 publications

(103 citation statements)

References 71 publications

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“…Moreover, and a potentially significant finding was the discovery of genes involved in the acetogenesis pathway, a possible alternative to methanogenesis in the rumen. However, in goats, the contribution of reductive acetogenesis in redirecting H 2 away from methanogenesis was minimal, even when methanogenesis was inhibited by bromochloromethane [43]. Instead, genes involved in propionate formation via the randomizing pathway, and numbers of corresponding bacteria among Prevotella and Selenomonas spp., increased in the presence of bromochloromethane, while the genes involved in methanogenesis decreased.…”

Section: Reviewmentioning

confidence: 99%

Application of meta-omics techniques to understand greenhouse gas emissions originating from ruminal metabolism

et al. 2017

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Methane emissions from ruminal fermentation contribute significantly to total anthropological greenhouse gas (GHG) emissions. New meta-omics technologies are beginning to revolutionise our understanding of the rumen microbial community structure, metabolic potential and metabolic activity. Here we explore these developments in relation to GHG emissions. Microbial rumen community analyses based on small subunit ribosomal RNA sequence analysis are not yet predictive of methane emissions from individual animals or treatments. Few metagenomics studies have been directly related to GHG emissions. In these studies, the main genes that differed in abundance between high and low methane emitters included archaeal genes involved in methanogenesis, with others that were not apparently related to methane metabolism. Unlike the taxonomic analysis up to now, the gene sets from metagenomes may have predictive value. Furthermore, metagenomic analysis predicts metabolic function better than only a taxonomic description, because different taxa share genes with the same function. Metatranscriptomics, the study of mRNA transcript abundance, should help to understand the dynamic of microbial activity rather than the gene abundance; to date, only one study has related the expression levels of methanogenic genes to methane emissions, where gene abundance failed to do so. Metaproteomics describes the proteins present in the ecosystem, and is therefore arguably a better indication of microbial metabolism. Both two-dimensional polyacrylamide gel electrophoresis and shotgun peptide sequencing methods have been used for ruminal analysis. In our unpublished studies, both methods showed an abundance of archaeal methanogenic enzymes, but neither was able to discriminate high and low emitters. Metabolomics can take several forms that appear to have predictive value for methane emissions; ruminal metabolites, milk fatty acid profiles, faecal long-chain alcohols and urinary metabolites have all shown promising results. Rumen microbial amino acid metabolism lies at the root of excessive nitrogen emissions from ruminants, yet only indirect inferences for nitrogen emissions can be drawn from meta-omics studies published so far. Annotation of meta-omics data depends on databases that are generally weak in rumen microbial entries. The Hungate 1000 project and Global Rumen Census initiatives are therefore essential to improve the interpretation of sequence/metabolic information.

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Section: Reviewmentioning

confidence: 99%

Application of meta-omics techniques to understand greenhouse gas emissions originating from ruminal metabolism

et al. 2017

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“…The overall interpretation would be that methane emissions depend on the abundance of the H 2 -producing bacteria present; a corollary to this is the observation that chemical inhibition of methanogenesis in goats led to increases in the abundance of H 2 -consuming Prevotella and Selenomonas spp . [73]. Proteobacteria were 4-fold less abundant (2.7 vs. 11.2% of bacteria) in high emitting beef cattle [46] and a similar finding was made in dairy cows [40].…”

Section: Introductionmentioning

confidence: 62%

The ruminal microbiome associated with methane emissions from ruminant livestock

Tapio

Snelling

Strozzi

et al. 2017

J Animal Sci Biotechnol

273

214

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Methane emissions from ruminant livestock contribute significantly to the large environmental footprint of agriculture. The rumen is the principal source of methane, and certain features of the microbiome are associated with low/high methane phenotypes. Despite their primary role in methanogenesis, the abundance of archaea has only a weak correlation with methane emissions from individual animals. The composition of the archaeal community appears to have a stronger effect, with animals harbouring the Methanobrevibacter gottschalkii clade tending to be associated with greater methane emissions. Ciliate protozoa produce abundant H2, the main substrate for methanogenesis in the rumen, and their removal (defaunation) results in an average 11% lower methane emissions in vivo, but the results are not consistent. Different protozoal genera seem to result in greater methane emissions, though community types (A, AB, B and O) did not differ. Within the bacteria, three different ‘ruminotypes’ have been identified, two of which predispose animals to have lower methane emissions. The two low-methane ruminotypes are generally characterized by less abundant H2-producing bacteria. A lower abundance of Proteobacteria and differences in certain Bacteroidetes and anaerobic fungi seem to be associated with high methane emissions. Rumen anaerobic fungi produce abundant H2 and formate, and their abundance generally corresponds to the level of methane emissions. Thus, microbiome analysis is consistent with known pathways for H2 production and methanogenesis, but not yet in a predictive manner. The production and utilisation of formate by the ruminal microbiota is poorly understood and may be a source of variability between animals.

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“…supply to the host animal (13)(14)(15). Thus, the H 2 concentration stays constant, although its consumption by methanogens is partially inhibited in the rumen.…”

Section: Significancementioning

confidence: 99%

Mode of action uncovered for the specific reduction of methane emissions from ruminants by the small molecule 3-nitrooxypropanol

Duin

Wagner

Shima

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

207

188

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Ruminants, such as cows, sheep, and goats, predominantly ferment in their rumen plant material to acetate, propionate, butyrate, CO2, and methane. Whereas the short fatty acids are absorbed and metabolized by the animals, the greenhouse gas methane escapes via eructation and breathing of the animals into the atmosphere. Along with the methane, up to 12% of the gross energy content of the feedstock is lost. Therefore, our recent report has raised interest in 3-nitrooxypropanol (3-NOP), which when added to the feed of ruminants in milligram amounts persistently reduces enteric methane emissions from livestock without apparent negative side effects [Hristov AN, et al. (2015) Proc Natl Acad Sci USA 112(34):10663–10668]. We now show with the aid of in silico, in vitro, and in vivo experiments that 3-NOP specifically targets methyl-coenzyme M reductase (MCR). The nickel enzyme, which is only active when its Ni ion is in the +1 oxidation state, catalyzes the methane-forming step in the rumen fermentation. Molecular docking suggested that 3-NOP preferably binds into the active site of MCR in a pose that places its reducible nitrate group in electron transfer distance to Ni(I). With purified MCR, we found that 3-NOP indeed inactivates MCR at micromolar concentrations by oxidation of its active site Ni(I). Concomitantly, the nitrate ester is reduced to nitrite, which also inactivates MCR at micromolar concentrations by oxidation of Ni(I). Using pure cultures, 3-NOP is demonstrated to inhibit growth of methanogenic archaea at concentrations that do not affect the growth of nonmethanogenic bacteria in the rumen.

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Metagenomic analysis of the rumen microbial community following inhibition of methane formation by a halogenated methane analog

Cited by 105 publications

References 71 publications

Application of meta-omics techniques to understand greenhouse gas emissions originating from ruminal metabolism

Application of meta-omics techniques to understand greenhouse gas emissions originating from ruminal metabolism

The ruminal microbiome associated with methane emissions from ruminant livestock

Mode of action uncovered for the specific reduction of methane emissions from ruminants by the small molecule 3-nitrooxypropanol

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