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Shifting microbial communities sustain multi-year iron reduction and methanogenesis in ferruginous sediment incubations

Marcus S. Bray, Jieying Wu, Benjamin C. Reed, Cecilia B. Kretz, Keaton M. Belli, Rachel L. Simister, Cynthia Henny, Frank J. Stewart, Thomas J. DiChristina, Jay A. Brandes, David A. Fowle, Sean A. Crowe, Jennifer B. Glass
doi: https://doi.org/10.1101/087783
Marcus S. Bray
1School of Biology, Georgia Institute of Technology, Atlanta, GA, 30332, USA
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Jieying Wu
1School of Biology, Georgia Institute of Technology, Atlanta, GA, 30332, USA
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Benjamin C. Reed
1School of Biology, Georgia Institute of Technology, Atlanta, GA, 30332, USA
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Cecilia B. Kretz
2School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA
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Keaton M. Belli
2School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA
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Rachel L. Simister
3Departments of Microbiology & Immunology and Earth, Ocean, & Atmospheric Sciences, University of British Columbia, Vancouver, BC, Canada
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Cynthia Henny
4Research Center for Limnology, Indonesian Institute of Sciences, Cibinong, Indonesia
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Frank J. Stewart
1School of Biology, Georgia Institute of Technology, Atlanta, GA, 30332, USA
2School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA
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Thomas J. DiChristina
1School of Biology, Georgia Institute of Technology, Atlanta, GA, 30332, USA
2School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA
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Jay A. Brandes
5Skidaway Institute of Oceanography, Savannah, GA, 31411, USA
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David A. Fowle
6Department of Geology, University of Kansas, Lawrence, KS, 66045, USA
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Sean A. Crowe
3Departments of Microbiology & Immunology and Earth, Ocean, & Atmospheric Sciences, University of British Columbia, Vancouver, BC, Canada
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Jennifer B. Glass
1School of Biology, Georgia Institute of Technology, Atlanta, GA, 30332, USA
2School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA
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  • For correspondence: Jennifer.Glass@eas.gatech.edu
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Abstract

Reactive Fe(III) minerals can influence methane (CH4) emissions by inhibiting microbial methanogenesis or by stimulating anaerobic CH4 oxidation. The balance between Fe(III) reduction, methanogenesis, and methane oxidation in ferruginous Archean and Paleoproterozoic oceans would have controlled CH4 fluxes to the atmosphere, thereby regulating the capacity for CH4 to warm the early Earth under the Faint Young Sun. We studied CH4 and Fe cycling in anoxic incubations of ferruginous sediment from the ancient ocean analogue Lake Matano, Indonesia over three successive transfers (500 days total). Iron reduction, methanogenesis, methane oxidation, and microbial taxonomy were monitored in treatments amended with ferrihydrite or goethite. After three dilutions, Fe(III) reduction persisted only in bottles with ferrihydrite. Enhanced CH4 production was observed in the presence of goethite, highlighting the potential for reactive Fe(III)-oxides to inhibit methanogenesis. Supplementing the media with hydrogen, nickel and selenium did not stimulate methanogenesis. There was limited evidence for Fe(III)-dependent CH4 oxidation, although some incubations displayed CH4-stimulated Fe(III)-reduction. 16S rRNA profiles continuously changed over the course of enrichment, with ultimate dominance of unclassified members of the order Desulfuromonadales in all treatments. Microbial diversity decreased markedly over the course of incubation, with subtle differences between ferrihydrite and goethite amendments. These results suggest that Fe(III)-oxide mineralogy and availability of electron donors could have led to spatial separation of Fe(III)-reducing and methanogenic microbial communities in ferruginous marine sediments, potentially explaining the persistence of CH4 as a greenhouse gas throughout the first half of Earth history.

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Posted February 13, 2017.
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Shifting microbial communities sustain multi-year iron reduction and methanogenesis in ferruginous sediment incubations
Marcus S. Bray, Jieying Wu, Benjamin C. Reed, Cecilia B. Kretz, Keaton M. Belli, Rachel L. Simister, Cynthia Henny, Frank J. Stewart, Thomas J. DiChristina, Jay A. Brandes, David A. Fowle, Sean A. Crowe, Jennifer B. Glass
bioRxiv 087783; doi: https://doi.org/10.1101/087783
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Shifting microbial communities sustain multi-year iron reduction and methanogenesis in ferruginous sediment incubations
Marcus S. Bray, Jieying Wu, Benjamin C. Reed, Cecilia B. Kretz, Keaton M. Belli, Rachel L. Simister, Cynthia Henny, Frank J. Stewart, Thomas J. DiChristina, Jay A. Brandes, David A. Fowle, Sean A. Crowe, Jennifer B. Glass
bioRxiv 087783; doi: https://doi.org/10.1101/087783

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