Polyphenol rewiring of the microbiome reduces methane emissions

Methane mitigation is regarded as a critical strategy to combat the scale of global warming. Currently, about 40% of methane emissions originate from microbial sources, which is causing strategies to suppress methanogens, either through direct toxic effects or by diverting their substrates and energy, to gain traction. Problematically, current microbial methane mitigation knowledge derives from rumen studies and lacks detailed microbiome-centered insights, limiting translation across ecosystems. Here we utilize genome-resolved metatranscriptomes and metabolomes to assess the impact of a proposed methane inhibitor, catechin, on greenhouse gas emissions for high-methane-emitting peatlands. In microcosms, catechin drastically reduced methane emissions by 72-84% compared to controls. Longitudinal sampling allowed for reconstruction of a novel catechin degradation pathway involving Actinomycetota and Clostridium, which break down catechin into smaller phenolic compounds within the first 21 days, followed by degradation of phenolic compounds by Pseudomonas_E from days 21 to 35. These genomes also co-expressed hydrogen-uptake genes, suggesting that hydrogenases may act as a hydrogen sink during catechin degradation, depriving methanogens of substrates. This was supported by decreased gene expression in hydrogenotrophic and hydrogen-dependent methylotrophic methanogens under catechin treatment. We also saw reduced gene expression from genomes inferred to be functioning syntrophically with hydrogen-utilizing methanogens. We propose that catechin metabolic redirection effectively starves hydrogen-utilizing methanogens, offering a potent avenue for curbing methane emissions across diverse environments including ruminants, landfills, and constructed or managed wetlands.