Monique Sezanne Patzner, Merritt Logan, Amy McKenna, Robert B Young, Zhe Zhou, Hanna Joss, Carsten W Mueller, Carmen Hoeschen, Thomas Scholten, Daniel Straub, Sara Kleindienst, Thomas Borch, Andreas Kappler, Casey Bryce

Reactive iron (Fe) minerals can preserve organic carbon (OC) in soils overlying intact permafrost. With permafrost thaw, reductive dissolution of iron minerals releases Fe and OC into the porewater, potentially increasing the bioavailability of OC for microbial decomposition. However, the stability of this so-called rusty carbon sink, the microbial community driving mineral dissolution, the identity of the iron-associated carbon and the resulting impact on greenhouse gas emissions are unknown. We examined palsa hillslopes, gradients from intact permafrost-supported palsa to semi-wet partially-thawed bog in a permafrost peatland in Abisko (Sweden). Using high-resolution mass spectrometry, we found that Fe-bound OC in intact palsa is comprised of loosely bound more aliphatic and strongly-bound more aromatic species. Iron mineral dissolution by both fermentative and dissimilatory Fe(III) reduction releases Fe-bound OC along the palsa hillslopes, before complete permafrost thaw. The increasing bioavailability of dissolved OC (DOC) leads to its further decomposition, demonstrated by an increasing nominal oxidation state of carbon (NOSC) and a peak in bioavailable acetate (61.7±42.6 mg C/L) at the collapsing palsa front. The aqueous Fe2+ released is partially re-oxidized by Fe(II)-oxidizing bacteria but cannot prevent the overall loss of the rusty carbon sink with palsa collapse. The increasing relative abundance and activity of Fe(III)-reducers is accompanied by an increasing abundance of methanogens and a peak in methane (CH4) emissions at the collapsing front. Our data suggest that the loss of the rusty carbon sink directly contributes to carbon dioxide (CO2) production by Fe(III) reduction coupled to OC oxidation and indirectly to CH4 emission by promoting methanogenesis even before complete permafrost thaw.