Microbial iron(III) reduction of iron-organic carbon phases across a permafrost thaw gradient and its impact on methane emissions

Wetlands account for roughly 20-30% of global methane (CH4) emissions, in part due to (permanently) anoxic conditions that promote methanogenesis. Low-lying permafrost peatlands are expected to be an increasing source of CH4 due to permafrost thaw in the future, due to waterlogging, anoxia and organic carbon (OC) mobilization. These processes can force an increase of the extent of wetlands and higher total CH4 emissions. Net release of CH4 depends on the availability of more energetically favorable electron acceptors in soil, such as ferric iron (Fe(III)). Fe(III) may be present as Fe(III) oxyhydroxides or Fe(III)-OC phases in peatlands. Since Fe(III)-reducing microbes and methanogens compete for the same substrates (e.g., small organic molecules such as acetate), CH4 production is often suppressed as long as there is bioavailable Fe(III) present. However, the dissolution of Fe(III)-OC phases during Fe(III) reduction would release the previously bound OC and make it more bioavailable to fermenting microorganisms. This would produce more substrates for methanogens and could therefore increase CH4 production. It is currently unknown to what extent microbial reduction of Fe(III)-OC phases and the coupled OC release effects CH4 emissions across permafrost thaw.In this study, we therefore aim to elucidate the extent of reduction of Fe(III)-OC phases upon permafrost thaw and the corresponding effect on CH4 emissions across three distinct thaw stages: (i) recently collapsed palsa hills, (ii) partly thawed bog and (iii) fully thawed fen habitats. We simulated permafrost thaw by a series of incubation experiments with soils from each thaw stage from a permafrost peatland (Stordalen Mire, Abisko, Sweden). Soils were incubated under anoxic, flooded conditions for 30 days, after which synthesized 57Fe-labelled Fe(III)-OC coprecipitates were added as representative Fe-OC phases. Over the course of the incubations (42 days), we followed Fe speciation and 57Fe fractions in the dissolved and solid phases using geochemical and synchrotron-based spectroscopy techniques in addition to quantification of greenhouse gas production. Results show that added coprecipitates were completely reduced (within 1 day) in palsa and bog soils, leading to increases in dissolved Fe2+, OC concentrations and CO2 emissions. CH4 production was not detected in palsa soils over the course of the incubation and CH4 suppression in bog soils due to Fe(III) reduction was only short-term. In contrast, added coprecipitates in fen soils were only reduced by 10% after 42 days, likely due to low dissolved OC concentrations. However, this led to a significantly higher inhibition of methanogenesis than in the palsa and bog soils. We also studied the microbial community by 16S rRNA amplicon (gene) sequencing and quantified mcrA gene copy numbers to assess the potential activity of methanogens. Overall, these results help to understand the influence of Fe-OC coprecipitates on methane emissions in thawing permafrost peatlands.