The role of oxygen in stimulating methane production in wetlands.

Abstract

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.