Metabolic Redox Coupling Controls Methane Production in Permafrost-Affected Peatlands Through Organic Matter Quality-Dependent Energy Allocation.

Permafrost thaw represents one of Earth's largest climate feedback risks, potentially releasing vast carbon (C) stores as greenhouse gases (GHG). However, our ability to predict emissions remains limited by poor understanding of how changing organic matter (OM) composition affects microbial carbon processing. We test a metabolism-centered redox framework, which views microbial processes as coupled oxidative-reductive reactions, to mechanistically explain how organic matter metabolite quality controls greenhouse gas production in permafrost-affected peatland ecosystems. Rather than relying solely on geochemical redox measurements, our approach examines how microbes balance electron flow through metabolic pathways. Using active layer peat (9-19 cm) from contrasting environments (bog and fen), we employed multi-omics approaches, including metabolomics, metagenomics, and metatranscriptomics, to link OM chemistry to microbial function. Our results reveal distinct dissolved organic matter metabolite composition, with fen systems enriched in compounds with higher substrate quality (low molecular weight (MW) sugars with high H:C ratios and low aromaticity) and bog systems dominated by compounds with lower substrate quality (high MW phenols with lower H:C ratios and higher aromaticity). In fen samples, these sugar-like compounds correlated with higher oxidative metabolism and methanogenesis, supported by increased glycolysis gene expression. Initially, electrons from increased oxidative metabolism were balanced through nitrate and sulfate reduction, but as these electron acceptors were depleted, methanogenesis increased to maintain redox balance. Fen samples showed rapid degradation of both high- and low-substrate-quality compounds, suggesting sufficient energy for efficient C cycling. Conversely, bog samples exhibited more polyphenolic compounds, lower glycolysis activity, and higher stress-related gene expression, suggesting energy was diverted towards cell maintenance under acidic conditions rather than C processing. This approach suggests that predicting greenhouse gas emissions requires an understanding of how organic matter quality shapes microbial energy allocation strategies, providing a mechanistic framework for improving emission predictions from permafrost-affected peatlands and similar ecosystems.