Suppression of Methanogenesis by Microbial Reduction of Iron-Organic Carbon Associations in Fully Thawed Permafrost Soil

Abstract

Global methane (CH₄) emissions from thawing permafrost peatlands are expected to increase substantially in the future. Net emission of CH₄ depends on the presence of more favorable terminal electron acceptors for microbial respiration, such as ferric iron (Fe(III)). In soils with high OC content, Fe(III) is often coprecipitated with organic carbon (OC). The presence of Fe(III)-OC coprecipitates could either suppress CH₄ emissions due to inhibition of methanogenesis and stimulation of anaerobic methane oxidation coupled to Fe(III) reduction, or enhance emissions by providing additional OC. Here, we investigated the role of Fe(III)-OC coprecipitates in net CH₄ release in a fully thawed, waterlogged permafrost peatland (Stordalen Mire, Abisko, Sweden). We synthesized Fe(III)-OC coprecipitates using natural organic matter from the field site and added them to waterlogged soil in a microcosm experiment and in situ, and followed Fe speciation and changes in greenhouse gas emissions over time. Fe(III)-OC coprecipitates were partially reduced (22%) within 42 days in the microcosm experiment, while almost full reduction (92 ± 4%) occurred in situ within 53 days. This led to a decrease in CH₄ emissions by 94% and 40% in the microcosm and field experiments, respectively, compared to no-coprecipitate controls. A decrease in both RNA-based mcrA copy numbers and relative abundance of detected methanogens indicated that methanogenesis was mainly inhibited by the addition of the coprecipitates due to microbial Fe(III) reduction. In conclusion, Fe(III)-OC coprecipitates temporarily suppress net CH₄ emissions in fully thawed permafrost soils, and might play a similar role in mitigating CH₄ release in other (periodically) flooded soils.