Microbial iron(III) reduction during palsa collapse promotes greenhouse gas emissions before complete permafrost thaw

Abstract

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.

Seasonal Fluctuations in Iron Cycling in Thawing Permafrost Peatlands

“…In the active layer of the palsa underlain by intact permafrost, continuous oxic conditions promoted Fe(II) oxidation to Fe(III) phases through early to late summer, presumably from the influx and oxidation of dissolved Fe(II) from the surrounding soil which has a porewater Fe(II) concentration of up to approximately 2 mM. 77 A (62.1 ± 40.2)–(155.3 ± 27.3)% gain in solid Fe(III) (0.5 and 6 M HCl extractable) was observed in bags deployed in early to late summer ((3.55 ± 0.87)–(5.58 ± 0.44) mg Fe(III) per g sand in comparison to 2.19 ± 0.26 mg per g sand in the reference material). In the active layer of the partially thawed bog, weakly to moderately reduced redox conditions in early summer favored Fe(III) (oxyhydr)oxide reduction which is indicated by Fe(III) mineral dissolution leading to a 47.2 ± 20.3% loss of Fe (i.e., loss of 1.03 ± 0.34 mg 0.5 M HCl extractable Fe(III) per g sand, Figure 2 ).…”

“… 24 Abiotic oxidation of dissolved Fe 2+ by O 2 produces hydroxyl radicals that are known to degrade organic matter to low molecular weight organic molecules and CO 2 . 75 , 76 Thus, the absence of porewater DOC, due to its potential high bioavailability, 77 as well as the radical formation following abiotic oxidation of dissolved Fe 2+ by O 2 could explain the absence of OC associated with the FH-coated sands in the active layer of the palsa soils.…”

“…In the active layer of the palsa underlain by intact permafrost, continuous oxic conditions promoted Fe­(II) oxidation to Fe­(III) phases through early to late summer, presumably from the influx and oxidation of dissolved Fe­(II) from the surrounding soil which has a porewater Fe­(II) concentration of up to approximately 2 mM . A (62.1 ± 40.2)–(155.3 ± 27.3)% gain in solid Fe­(III) (0.5 and 6 M HCl extractable) was observed in bags deployed in early to late summer ((3.55 ± 0.87)–(5.58 ± 0.44) mg Fe­(III) per g sand in comparison to 2.19 ± 0.26 mg per g sand in the reference material).…”

Spatial distribution and biogeochemistry of redox active species in arctic sedimentary porewaters and seeps

“…60 Based on our voltammetric data, this possibly indicates that methanogens near the sediment water interface are able to persist on H 2 and CO 2 generated from organic matter mineralization coupled to Fe( iii ) reduction (or abiotic reduction of Mn( iii , iv )). 61 Indeed, measured methogenic communities increased in abundance concurrently with Fe-reducing communities in the upper mms of STL15 sediment (Fig. 3a and b).…”