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Abstract Microorganisms drive many aspects of organic carbon cycling in thawing permafrost soils, but the compositional trajectory of the post-thaw microbiome and its metabolic activity remain uncertain, which limits our ability to predict permafrost–climate feedbacks in a warming world. Using quantitative metabarcoding and metagenomic sequencing, we determined relative and absolute changes in microbiome composition and functional gene abundance during thaw incubations of wet sedge tundra collected from northern Alaska, USA. Organic soils from the tundra active-layer (0–50 cm), transition-zone (50–70 cm), and permafrost (70+ cm) depths were incubated under reducing conditions at 4 °C for 30 days to mimic an extended thaw duration. Following extended thaw, we found that iron (Fe)-cycling Gammaproteobacteria, specifically the heterotrophic Fe(III)-reducing Rhodoferax sp. and chemoautotrophic Fe(II)-oxidizing Gallionella sp., increased by 3–5 orders of magnitude in absolute abundance within the transition-zone and permafrost microbiomes, accounting for 65% of community abundance. We also found that the abundance of genes for Fe(III) reduction (e.g., MtrE) and Fe(II) oxidation (e.g., Cyc1) increased concurrently with genes for benzoate degradation and pyruvate metabolism, in which pyruvate is used to generate acetate that can be oxidized, along with benzoate, to CO2 when coupled with Fe(III) reduction. Gene abundance for CH4 metabolism decreased following extended thaw, suggesting dissimilatory Fe(III) reduction suppresses acetoclastic methanogenesis under reducing conditions. Our genomic evidence indicates that microbial carbon degradation is dominated by iron redox metabolism via an increase in gene abundance associated with Fe(III) reduction and Fe(II) oxidation during initial permafrost thaw, likely increasing microbial respiration while suppressing methanogenesis in wet sedge tundra.
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Spatial distribution and biogeochemistry of redox active species in arctic sedimentary porewaters and seeps
Redox active species in Arctic lacustrine sediments play an important, regulatory role in the carbon cycle, yet there is little information on their spatial distribution, abundance, and oxidation states. Here, we use voltammetric microelectrodes to quantify the in situ concentrations of redox-active species at high vertical resolution (mm to cm) in the benthic porewaters of an oligotrophic Arctic lake (Toolik Lake, AK, USA). Mn( ii ), Fe( ii ), O 2 , and Fe( iii )-organic complexes were detected as the major redox-active species in these porewaters, indicating both Fe( ii ) oxidation and reductive dissolution of Fe( iii ) and Mn( iv ) minerals. We observed significant spatial heterogeneity in their abundance and distribution as a function of both location within the lake and depth. Microbiological analyses and solid phase Fe( iii ) measurements were performed in one of the Toolik Lake cores to determine the relationship between biogeochemical redox gradients and microbial communities. Our data reveal iron cycling involving both oxidizing (FeOB) and reducing (FeRB) bacteria. Additionally, we profiled a large microbial iron mat in a tundra seep adjacent to an Arctic stream (Oksrukuyik Creek) where we observed Fe( ii ) and soluble Fe( iii ) in a highly reducing environment. The variable distribution of redox-active substances at all the sites yields insights into the nature and distribution of the important terminal electron acceptors in both lacustrine and tundra environments capable of exerting significant influences on the carbon cycle.
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- Award ID(s):
- 1754358
- PAR ID:
- 10357981
- Date Published:
- Journal Name:
- Environmental Science: Processes & Impacts
- Volume:
- 24
- Issue:
- 3
- ISSN:
- 2050-7887
- Page Range / eLocation ID:
- 426 to 438
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1039/d1em00505g
