Microbial iron cycling in permafrost peatlands affected by global warming - Impact on carbon mobilization and greenhouse gas emissions

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URI: http://hdl.handle.net/10900/121085
Dokumentart: PhDThesis
Date: 2023-10-20
Language: English
Faculty: 7 Mathematisch-Naturwissenschaftliche Fakultät
Department: Geographie, Geoökologie, Geowissenschaft
Advisor: Kappler, Andreas (Prof. Dr.)
Day of Oral Examination: 2021-10-21
DDC Classifikation: 500 - Natural sciences and mathematics
550 - Earth sciences
570 - Life sciences; biology
Other Keywords: Auftauender Permafrost
organischer Kohlenstoff
soil organic carbon
Thawing permafrost
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Northern Hemisphere peatlands store vast amounts of carbon, particularly in permafrost regions where low temperatures inhibited organic matter decomposition since the last glacial ice age. With high latitudes warming faster than anywhere else on the planet, there is urgent concern about the impact of permafrost thaw on the stability of this carbon sink. It has been shown that iron(III) (oxyhydr)oxides can trap organic carbon in soils, underlain by intact permafrost, which may limit carbon mobilization and thus its degradation. Therefore, it is considered as a so-called rusty carbon sink. However, controls on the stability of iron-carbon associations in permafrost peatlands and their response to warming temperatures are poorly understood. Only little is known about the microbial iron cycle in permafrost peatlands and how it is impacted by global warming. Its consequences for carbon mobilization and ultimately greenhouse gas emissions such as carbon dioxide and methane prevail unexplored. Aiming to fill these knowledge gaps, we characterized the dynamic interactions between iron and carbon in a subarctic thawing permafrost peatland (Stordalen mire) in Abisko, Northern Sweden. Here, in the discontinuous permafrost zone, oxic palsa mounds with ice-rich cores are rapidly collapsing into acidic bogs before they ultimately transform into ice-free fen-type wetlands. We show that reactive Fe minerals such as iron(III) (oxyhydr)oxides bind significant quantities of organic carbon (up to 20% of total organic carbon) in areas of intact permafrost. However, these iron-carbon associations are not stable during permafrost thaw. Iron(III)-reducing bacteria, such as e.g. Geobacter spp., reductively dissolve iron(III) (oxyhydr)oxides coupled to carbon oxidation, and release aqueous iron (iron(II)) and the previously iron-bound, aliphatic-like organic carbon that becomes mobilized. The microbially driven iron(III) reduction thus directly contributes to greenhouse gas emissions such as carbon dioxide by iron(III) reduction coupled to carbon oxidation and indirectly by releasing bioavailable organic carbon which then can become further metabolized to carbon dioxide and/or methane by the present microbial community. Iron(III)-reducing bacteria increase in abundance soon after thaw initiates, as it results in increased water saturation and expanding reducing conditions. The loss of the rusty carbon sink in permafrost soils coincides with the highest measured dissolved organic carbon (535.75±133.74 mg C/L) and highly bioavailable acetate concentrations (61.7±42.6 mg C/L) along a permafrost thaw gradient, a significant increase in the abundance of methanogens and methanotrophs, and with increasing fluxes of the greenhouse gases carbon dioxide and methane. We found that permafrost thaw also increases the abundance of iron(II)-oxidizing microorganisms, such as Gallionella spp. and Sideroxydans spp. This suggests that post-thaw iron cycling and interlinked greenhouse gas emissions are highly dynamic, and that the measured iron redox state is a result of the net balance between reductive and oxidative processes. Indeed, seasonal re-precipitation of iron(III) (oxyhydr)oxides was observed in the active layer of partially-thawed bog areas. Ultimately, iron(II)-oxidizing microorganisms can not sustain or reform the rusty carbon sink after complete permafrost thaw in fully-thawed fen-type wetlands. This work has greatly expanded our understanding of microbe-mineral interactions in permafrost peatlands. It reveals an important and previously overlooked role of iron-cycling microorganisms in the release of iron mineral-associated organic carbon and its impact on greenhouse gas emissions of thawing permafrost peatlands – one of Earth’s most rapidly changing ecosystems.

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