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Evidence for a hydrogen-sink mechanism of (+)catechin-mediated emission reduction of the ruminant greenhouse gas methane

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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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References

  • Becker, P. M., & van Wikselaar, P. G. (2011). Effects of plant antioxidants and natural vicinal diketones on methane production, studied in vitro with rumen fluid and a polylactate as maintenance substrate. Animal Feed Science and Technology, 170, 201–208.

    Article  CAS  Google Scholar 

  • Bibi, N., Sattar, A., & Chaudry, M. A. (1991). Phenolic constituents in major fractions of tropical rapeseed. Die Nahrung, 35, 1053–1059.

    Article  CAS  Google Scholar 

  • Calsamiglia, S., Busquet, M., Cardozo, P. W., Castillejos, L., & Ferret, A. (2007). Essential oils as modifiers of rumen microbial fermentation. Journal of Dairy Science, 90, 2580–2595.

    Article  CAS  PubMed  Google Scholar 

  • Chen, M., & Wolin, M. J. (1977). Influence of CH4 production by Methanobacterium ruminantium on the fermentation of glucose and lactate by Selenomonas ruminantium. Applied Environmental Microbiology, 34, 756–759.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chesson, A., Stewart, C. S., & Wallace, R. J. (1982). Influence of plant phenolic acids on growth and cellulolytic activity of rumen bacteria. Applied Environmental Microbiology, 44, 597–603.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deppenmeier, U., & Müller, V. (2008). Bioenergetics. Energy conservation and conversion. In G. Schäfer & H. Penefsky (Eds.), Series: Results and problems in cell differentiation (Vol. 45, p. 123). Heidelberg: Springer.

    Google Scholar 

  • Dixon, R. A., Xie, D.-Y., & Sharma, S. B. (2005). Proanthocyanidins—A final frontier in flavonoid research? New Phytologist, 165, 9–28.

    Article  CAS  PubMed  Google Scholar 

  • Feng, W. Y. (2006). Metabolism of green tea catechins: An overview. Current Drug Metabolism, 7, 755–809.

    Article  CAS  PubMed  Google Scholar 

  • Hjorth, M., Mondolot, L., Buatois, B., Andary, C., Rapior, S., Kudsk, P., et al. (2006). An easy and rapid method using microscopy to determine herbicide effects in Poaceae weed species. Pest Management Science, 62, 515–521.

    Article  CAS  PubMed  Google Scholar 

  • Krumholz, L. R., & Bryant, M. P. (1986). Eubacterium oxidoreducans sp. nov. requiring H2 or formate to degrade gallate, pyrogallol, phloroglucinol and quercetin. Archives of Microbiology, 144, 8–14.

    Article  CAS  Google Scholar 

  • Kumar, R., & Singh, M. (1984). Tannins: their adverse role in ruminant nutrition. Journal of Agricultural and Food Chemistry, 32, 447–453.

    Article  CAS  Google Scholar 

  • Lassey, K. R. (2008). Livestock methane emission and its perspective in the global methane cycle. Australian Journal of Experimental Agriculture, 48, 114–118.

    Article  CAS  Google Scholar 

  • McAllister, T. A., & Newbold, C. J. (2008). Redirecting rumen fermentation to reduce methanogenesis. Australian Journal of Experimental Agriculture, 48, 7–13.

    Article  CAS  Google Scholar 

  • Meselhy, R. M., Nakamura, N., & Hattori, M. (1997). Biotransformation of (−)-epicatechin 3-O-gallate by human intestinal bacteria. Chemical & Pharmaceutical Bulletin, 45, 888–893.

    Article  CAS  Google Scholar 

  • Min, B. R., Attwood, G. T., McNabb, W. C., Molan, A. L., & Barry, T. N. (2005). The effect of condensed tannins from Lotus corniculatus on the proteolytic activities and growth of rumen bacteria. Animal Feed Science and Technology, 121, 45–58.

    Article  CAS  Google Scholar 

  • Monagas, M., Urpi-Sarda, M., Sánchez-Patán, F., Llorach, R., Garrido, I., Gómez-Cordovés, C., et al. (2010). Insights into the metabolism and microbial biotransformation of dietary flavan-3-ols and the bioactivity of their metabolites. Food & Function, 1, 233–253.

    Article  CAS  Google Scholar 

  • Patra, A. K., & Saxena, J. (2010). A new perspective on the use of plant secondary metabolites to inhibit methanogenesis in the rumen. Phytochemistry, 71, 1198–1222.

    Article  CAS  PubMed  Google Scholar 

  • Reynaud, A., Fraisse, D., Cornu, A., Farruggia, A., Pujos-Guillot, E., Besle, J.-M., et al. (2010). Variation in content and composition of phenolic compounds in permanent pastures according to botanical variation. Journal of Agricultural and Food Chemistry, 58, 5485–5494.

    Article  CAS  PubMed  Google Scholar 

  • Sandefur, C. A., & Koenigsberg, S. S. (1999). The use of hydrogen release compound for the accelerated bioremediation of anaerobically degradable contaminants: The advent of time-release electron donors. Remediation Journal, 10, 31–53.

    Article  Google Scholar 

  • Scheline, R. R. (1970). The metabolism of (+)-catechin to hydroxyphenylvaleric acids by the intestinal microflora. Biochimica Biophysica Acta, 222, 228–230.

    Article  CAS  Google Scholar 

  • Shindell, D. T., Faluvegi, G., Koch, D. M., Schmidt, G. A., Unger, N., & Bauer, S. E. (2009). Improved attribution of climate forcing to emissions. Science, 326, 716–718.

    Article  CAS  PubMed  Google Scholar 

  • Tikunov, Y., Lommen, A., De Vos, C. H. R., Verhoeven, H. A., Bino, R. J., Hall, R. D., et al. (2005). A novel approach for non-targeted data analysis for metabolomics. Large-scale profiling of tomato fruit volatiles. Plant Physiology, 139, 1125–1137.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Unachukwu, U. J., Ahmed, S., Kavalier, A., Lyles, J. T., & Kennelly, E. J. (2010). White and green teas (Camellia sinensis var. sinensis): Variation in phenolic, methylxanthine, and antioxidant profiles. Journal of Food Science, 75, C541–C548.

    Article  CAS  PubMed  Google Scholar 

  • Ungerfeld, E. M., Kohn, R. A., Wallace, R. J., & Newbold, C. J. (2007). A meta-analysis of fumarate effects on methane production in ruminal batch cultures. Journal of Animal Science, 85, 2556–2563.

    Article  CAS  PubMed  Google Scholar 

  • U.S. EPA. (2012). Global anthropogenic non-CO 2 greenhouse gas emissions, 1990–2030. EPA Report 430-R-12-006. Washington, DC: Office of Atmospheric Programs, Climate Change Division, U.S. Environmental Protection Agency.

  • Waghorn, G. C., & McNabb, W. C. (2003). Consequences of plant phenolic compounds for productivity and health of ruminants. Proceedings of the Nutrition Society, 62, 383–392.

    Article  CAS  PubMed  Google Scholar 

  • Walle, T., Hsieh, F., DeLegge, M. H., Oatis, J. E., & Walle, U. K. (2004). High absorption but low bioavailability of oral resveratrol in humans. Drug Metabolism and Disposition, 32, 1377–1382.

    Article  CAS  PubMed  Google Scholar 

  • Williamson, G., & Clifford, M. N. (2010). Colonic metabolites of berry polyphenols: the missing link to biological activity? British Journal of Nutrition, 104, S48–S66.

    Article  CAS  PubMed  Google Scholar 

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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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Correspondence to Petra Maria Becker.

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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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