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Abstract
Background
Many environments contain redox transition zones, where transient oxygenation events can modulate anaerobic reactions that influence the cycling of iron (Fe) and carbon (C) on a global scale. In predominantly anoxic soils, this biogeochemical cycling depends on Fe mineral composition and the activity of mixed Fe(III)-reducer populations that may be altered by periodic pulses of molecular oxygen (O2).
Methods
We repeatedly exposed anoxic (4% H2:96% N2) suspensions of soil from the Luquillo Critical Zone Observatory to 1.05 × 102, 1.05 × 103, and 1.05 × 104 mmol O2 kg−1 soil h−1 during pulsed oxygenation treatments. Metatranscriptomic analysis and 57Fe Mössbauer spectroscopy were used to investigate changes in Fe(III)-reducer gene expression and Fe(III) crystallinity, respectively.
Results
Slow oxygenation resulted in soil Fe-(oxyhydr)oxides of higher crystallinity (38.1 ± 1.1% of total Fe) compared to fast oxygenation (30.6 ± 1.5%, P < 0.001). Transcripts binning to the genomes of Fe(III)-reducers Anaeromyxobacter, Geobacter, and Pelosinus indicated significant differences in extracellular electron transport (e.g., multiheme cytochrome c, multicopper oxidase, and type-IV pilin gene expression), adhesion/contact (e.g., S-layer, adhesin, and flagellin gene expression), and selective microbial competition (e.g., bacteriocin gene expression) between the slow and fast oxygenation treatments during microbial Fe(III) reduction. These data also suggest that diverse Fe(III)-reducer functions, including cytochrome-dependent extracellular electron transport, are associated with type-III fibronectin domains. Additionally, the metatranscriptomic data indicate that Methanobacterium was significantly more active in the reduction of CO2 to CH4 and in the expression of class(III) signal peptide/type-IV pilin genes following repeated fast oxygenation compared to slow oxygenation.
Conclusions
This study demonstrates that specific Fe(III)-reduction mechanisms in mixed Fe(III)-reducer populations are uniquely sensitive to the rate of O2 influx, likely mediated by shifts in soil Fe(III)-(oxyhydr)oxide crystallinity. Overall, we provide evidence that transient oxygenation events play an important role in directing anaerobic pathways within soil microbiomes, which is expected to alter Fe and C cycling in redox-dynamic environments.
Subject Keywords
Coverage
Spatial
Temporal
Start Date: | |
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Content
ReadMe.md
LCZO -- Soil Microbes, Soil Biogeochemistry -- Iron redox, Soil Microbiome -- Bisley -- (2012-2017)
OVERVIEW
Description/Abstract
Background
Many environments contain redox transition zones, where transient oxygenation events can modulate anaerobic reactions that influence the cycling of iron (Fe) and carbon (C) on a global scale. In predominantly anoxic soils, this biogeochemical cycling depends on Fe mineral composition and the activity of mixed Fe(III)-reducer populations that may be altered by periodic pulses of molecular oxygen (O2).
Methods
We repeatedly exposed anoxic (4% H2:96% N2) suspensions of soil from the Luquillo Critical Zone Observatory to 1.05 × 102, 1.05 × 103, and 1.05 × 104 mmol O2 kg−1 soil h−1 during pulsed oxygenation treatments. Metatranscriptomic analysis and 57Fe Mössbauer spectroscopy were used to investigate changes in Fe(III)-reducer gene expression and Fe(III) crystallinity, respectively.
Results
Slow oxygenation resulted in soil Fe-(oxyhydr)oxides of higher crystallinity (38.1 ± 1.1% of total Fe) compared to fast oxygenation (30.6 ± 1.5%, P < 0.001). Transcripts binning to the genomes of Fe(III)-reducers Anaeromyxobacter, Geobacter, and Pelosinus indicated significant differences in extracellular electron transport (e.g., multiheme cytochrome c, multicopper oxidase, and type-IV pilin gene expression), adhesion/contact (e.g., S-layer, adhesin, and flagellin gene expression), and selective microbial competition (e.g., bacteriocin gene expression) between the slow and fast oxygenation treatments during microbial Fe(III) reduction. These data also suggest that diverse Fe(III)-reducer functions, including cytochrome-dependent extracellular electron transport, are associated with type-III fibronectin domains. Additionally, the metatranscriptomic data indicate that Methanobacterium was significantly more active in the reduction of CO2 to CH4 and in the expression of class(III) signal peptide/type-IV pilin genes following repeated fast oxygenation compared to slow oxygenation.
Conclusions
This study demonstrates that specific Fe(III)-reduction mechanisms in mixed Fe(III)-reducer populations are uniquely sensitive to the rate of O2 influx, likely mediated by shifts in soil Fe(III)-(oxyhydr)oxide crystallinity. Overall, we provide evidence that transient oxygenation events play an important role in directing anaerobic pathways within soil microbiomes, which is expected to alter Fe and C cycling in redox-dynamic environments.
Creator/Author
Wilmoth, Jared Lee |Moran, Mary Ann|Thompson, Aaron
CZOs
Luquillo
Contact
Miguel Leon, Miguel.Leon@unh.edu
Subtitle
Transient O2 pulses direct Fe crystallinity and Fe(III)-reducer gene expression within a soil microbiome
SUBJECTS
Disciplines
Biogeochemistry|Biology / Ecology
Topics
Soil Microbes|Soil Biogeochemistry
Subtopic
Iron redox, Soil Microbiome
Keywords
Soil microbiome|redox cycling|microbial FE(III) reduction|carbon cyling|metatranscriptomics|mössbauer spectroscopy
Variables
ferric ion|ferrous ion|Biomass|soil bacterial DNA|
Variables ODM2
Biomass|Biomass, soil bacterial deoxyribonucleic acid (DNA)
TEMPORAL
Date Start
2012-06-01
Date End
2017-04-07
SPATIAL
Field Areas
Bisley
Location
Bisley
North latitude
18.3202
South latitude
18.3053
West longitude
-65.7494
East longitude
-65.7346
REFERENCE
Citation
Jared Lee Wilmoth, Mary Ann Moran, Aaron Thompson (2018): Transient O2 pulses direct Fe crystallinity and Fe(III)-reducer gene expression within a soil microbiome. Microbiome. DOI: 10.1186/s40168-018-0574-5
Publications of this data
Jared Lee Wilmoth, Mary Ann Moran, Aaron Thompson (2018). Transient O2 pulses direct Fe crystallinity and Fe(III)-reducer gene expression within a soil microbiome. Microbiome http://dx.doi.org/10.1186/s40168-018-0574-5
CZO ID
7167
Additional Metadata
Name | Value |
---|---|
czos | Luquillo |
czo_id | 7167 |
citation | Jared Lee Wilmoth, Mary Ann Moran, Aaron Thompson (2018): Transient O2 pulses direct Fe crystallinity and Fe(III)-reducer gene expression within a soil microbiome. Microbiome. DOI: 10.1186/s40168-018-0574-5 |
keywords | Soil microbiome, redox cycling, microbial FE(III) reduction, carbon cyling, metatranscriptomics, mössbauer spectroscopy |
subtitle | Transient O2 pulses direct Fe crystallinity and Fe(III)-reducer gene expression within a soil microbiome |
variables | ferric ion, ferrous ion, Biomass, soil bacterial DNA, |
disciplines | Biogeochemistry, Biology / Ecology |
Related Resources
This resource is referenced by | Jared Lee Wilmoth, Mary Ann Moran, Aaron Thompson (2018). Transient O2 pulses direct Fe crystallinity and Fe(III)-reducer gene expression within a soil microbiome. Microbiome http://dx.doi.org/10.1186/s40168-018-0574-5 |
How to Cite
This resource is shared under the Creative Commons Attribution CC BY.
http://creativecommons.org/licenses/by/4.0/
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