Reduction of iron-organic carbon associations shifts net greenhouse gas release after initial permafrost thaw

In thawing permafrost soils, associations between organic carbon (OC) and ferric iron (Fe(III)) (oxyhydr)oxide minerals may stabilize OC in recently thawed soil layers, thus limiting the microbially mediated release of greenhouse gases (GHGs) such as carbon dioxide (CO2) and methane (CH4). Conversely, the development of anoxic conditions during thaw could lead to the microbial reductive dissolution of these Fe(III)-OC associations, resulting in a mobilization of the associated OC with unknown consequences for GHG release. In this study, we investigated the role of Fe(III)-OC associations (in the form of Fe(III)-OC coprecipitates) in soil GHG release during the collapse of previously oxic permafrost soils (“palsa”) and the inundation of seasonally anoxic soils (“bog”) at Stordalen Mire (Abisko, Sweden). We performed anoxic microcosm experiments using these two soils with the addition of 57Fe-labeled Fe(III)-OC coprecipitates. The coprecipitates were reduced entirely after 42 days, with rapid reductive dissolution of 22 ± 7% and 20 ± 7% of coprecipitates within 1 day in palsa and bog soils, respectively. Emissions of GHG varied depending on soil type: in case of the palsa soil, cumulative CO2 emissions increased by 43 ± 16% after addition of the Fe(III)-OC coprecipitates compared to a non-amended control, due to microbial Fe(III) reduction coupled to OC oxidation and likely additional OC input due to the release of Fe-bound OC. Concurrently, we observed an increase in activity of fermenting and complex OC-degrading microorganisms. Within the bog soil, it was notable that CH4 emissions were temporarily suppressed, likely due to inhibition of methanogenesis by microbial Fe(III) reduction of the added coprecipitates, indicated by a decrease in mcrA gene copies. In conclusion, our findings demonstrate that Fe(III)-OC associations do not provide protection for OC after establishment of anoxic conditions during permafrost thaw, with resulting GHG emissions controlled by previous redox status of the soils and the microbial community.