Distinct Microbiomes Underlie Divergent Responses of Methane Emissions from Diverse Wetland Soils to Oxygen Shifts

Hydrological shifts in wetlands, a globally important methane (CH₄) source, are critical constraints on CH₄ emissions and carbon-climate feedbacks. A limited understanding of how hydrologically driven oxygen (O₂) variability affects microbial CH₄ cycling in diverse wetlands makes wetland CH₄ emissions uncertain. Transient O₂ exposure significantly stimulated anoxic CH₄ production in incubations of Sphagnum peat from a temperate bog by enriching for polyphenol oxidizers and polysaccharide degraders, enhancing substrate flow toward methanogenesis under subsequent anoxic conditions. To assess whether shifts in soil microbiome structure and function operate similarly across wetland types, here we examined the sensitivity of different wetland soils to transient oxygenation. In slurry incubations of Sphagnum peat from a minerotrophic fen, and sediments from a freshwater marsh and saltmarsh, we examined temporal shifts in microbiomes coupled with geochemical characterization of slurries and incubation headspaces. Oxygenation did not affect microbiome structure and anoxic CH₄ production in mineral-rich fen-origin peat and freshwater marsh soils. Key taxa linked to O₂-stimulated CH₄ production in the bog-origin peat were notably rare in the fen-origin peat, supporting microbiome structure as a primary determinant of wetland response to O₂ shifts. In contrast to freshwater wetland experiments, saltmarsh geochemistry—particularly pH—and microbiome structure were persistently and significantly altered post-oxygenation, albeit with no significant impact on greenhouse gas emissions. These divergent responses suggest wetlands may be differentially resistant to O₂ fluctuations. With climate change driving greater O₂ variability in wetlands, our results inform mechanisms of wetland resistance and highlight microbiome structure as a potential resiliency biomarker.