Abstract
Methane formation in the rumen is a major cause of greenhouse gas emission. Plant secondary compounds in ruminant diets, such as essential oils, saponins and tannins, are known to affect methane production. However, their methane-lowering properties have generally been associated with undesired side effects such as impaired feed digestibility. Here we show that microbial methane formation in diluted and buffered rumen fluid was significantly lowered in the presence of (+)-catechin, a natural polyphenol. This flavan-3-ol, a tannin precursor, decreased the production of methane in a dose-dependent manner, where 1.0 mol catechin prevented the emission of 1.2 mol methane. During methane mitigation, (+)-catechin was step-wise degraded via C- and A-ring cleavage and reductive dehydroxylation reactions, as indicated by LC-QToF-MS based metabolomic profiling and NMR-based metabolite identification. This accounted for the acceptance of six hydrogen atoms per catechin molecule. Consequently, catechin functions as an extensive hydrogen sink, thereby competing with methane production by rumen methanogens (\( {\text{CO}}_{2} + 4{\text{H}}_{2} \Rightarrow {\text{CH}}_{4} + 2{\text{H}}_{2} {\text{O}} \)). Catechin therefore acts as an antireductant under the anaerobic test conditions, in contrast to its well-known antioxidant role during oxidative stress. The reductive degradation of catechin had no impact on the formation of ruminal fermentation products such as short-chain fatty acids in this model system. These results highlight the potential of plant secondary compounds to replace methane precursors as hydrogen sinks, and justify future scientific screening programs for similar, potentially more effective organic compounds.
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Acknowledgments
This study was funded by the NL Agency Energy and Climate of the Dutch Ministry of Economic Affairs, Agriculture and Innovation (EL&I) in the framework of the program “Reduction of non-CO2 greenhouse gases”. PM Becker and PG van Wikselaar are also indebted to the EU FP6 project SAFEWASTES (STREP 513949) and the EU FP7 New-Indigo project PLANTY. Financial support was also supplied by the EU FP7-KBBE Collaborative Project ATHENA (245121). RD Hall and CHR de Vos acknowledge support from the Centre for BioSystems Genomics and the Netherlands Metabolomics Centre, both under the auspices of the Netherlands Genomics Initiative. Harry Jonker is acknowledged for valuable assistance in sample preparation.
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The authors declare no conflicts of interest and that all institutional and national guidelines for the care and use of laboratory animals were followed.
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Becker, P.M., van Wikselaar, P.G., Franssen, M.C.R. et al. Evidence for a hydrogen-sink mechanism of (+)catechin-mediated emission reduction of the ruminant greenhouse gas methane. Metabolomics 10, 179–189 (2014). https://doi.org/10.1007/s11306-013-0554-5
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DOI: https://doi.org/10.1007/s11306-013-0554-5