The role of oxygen in stimulating methane production in wetlands

Methane (CH₄ ), a potent greenhouse gas, is the second most important greenhouse gas contributor to climate change after carbon dioxide (CO₂ ). The biological emissions of CH₄ from wetlands are a major uncertainty in CH₄ budgets. Microbial methanogenesis by Archaea is an anaerobic process accounting for most biological CH₄ production in nature, yet recent observations indicate that large emissions can originate from oxygenated or frequently oxygenated wetland soil layers. To determine how oxygen (O₂ ) can stimulate CH₄ emissions, we used incubations of Sphagnum peat to demonstrate that the temporary exposure of peat to O₂ can increase CH₄ yields up to 2000-fold during subsequent anoxic conditions relative to peat without O₂ exposure. Geochemical (including ion cyclotron resonance mass spectrometry, X-ray absorbance spectroscopy) and microbiome (16S rDNA amplicons, metagenomics) analyses of peat showed that higher CH₄ yields of redox-oscillated peat were due to functional shifts in the peat microbiome arising during redox oscillation that enhanced peat carbon (C) degradation. Novosphingobium species with O₂ -dependent aromatic oxygenase genes increased greatly in relative abundance during the oxygenation period in redox-oscillated peat compared to anoxic controls. Acidobacteria species were particularly important for anaerobic processing of peat C, including in the production of methanogenic substrates H₂ and CO₂ . Higher CO₂ production during the anoxic phase of redox-oscillated peat stimulated hydrogenotrophic CH₄ production by Methanobacterium species. The persistence of reduced iron (Fe(II)) during prolonged oxygenation in redox-oscillated peat may further enhance C degradation through abiotic mechanisms (e.g., Fenton reactions). The results indicate that specific functional shifts in the peat microbiome underlie O₂ enhancement of CH₄ production in acidic, Sphagnum-rich wetland soils. They also imply that understanding microbial dynamics spanning temporal and spatial redox transitions in peatlands is critical for constraining CH₄ budgets; predicting feedbacks between climate change, hydrologic variability, and wetland CH₄ emissions; and guiding wetland C management strategies.