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 (TeX). 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
LanguageEnglish
Pages179-189
JournalMetabolomics
Volume10
Issue number2
DOIs
Publication statusPublished - 2014

Fingerprint

Catechin
Methane
Ruminants
Greenhouse gases
Hydrogen
Gases
Rumen
Tannins
Methanogens
Oxidative stress
Metabolomics
Volatile Fatty Acids
Saponins
Polyphenols
Volatile Oils
Nutrition
Metabolites
Gas emissions
Organic compounds
Fermentation

Keywords

  • rumen bacteria
  • fermentation
  • methanogenesis
  • perspective
  • metabolites
  • tannins
  • growth
  • acids

Cite this

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title = "Evidence for a hydrogen-sink mechanism of (+)catechin-mediated emission reduction of the ruminant greenhouse gas methane",
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 (TeX). 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",
keywords = "rumen bacteria, fermentation, methanogenesis, perspective, metabolites, tannins, growth, acids",
author = "P.M. Becker and {van Wikselaar}, P.G. and M.C.R. Franssen and {de Vos}, C.H. and R.D. Hall and M.J. Beekwilder",
year = "2014",
doi = "10.1007/s11306-013-0554-5",
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TY - JOUR

T1 - Evidence for a hydrogen-sink mechanism of (+)catechin-mediated emission reduction of the ruminant greenhouse gas methane

AU - Becker, P.M.

AU - van Wikselaar, P.G.

AU - Franssen, M.C.R.

AU - de Vos, C.H.

AU - Hall, R.D.

AU - Beekwilder, M.J.

PY - 2014

Y1 - 2014

N2 - 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 (TeX). 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

AB - 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 (TeX). 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

KW - rumen bacteria

KW - fermentation

KW - methanogenesis

KW - perspective

KW - metabolites

KW - tannins

KW - growth

KW - acids

U2 - 10.1007/s11306-013-0554-5

DO - 10.1007/s11306-013-0554-5

M3 - Article

VL - 10

SP - 179

EP - 189

JO - Metabolomics

T2 - Metabolomics

JF - Metabolomics

SN - 1573-3882

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ER -