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Title: The role of oxygen in stimulating methane production in wetlands

Abstract

Methane (CH4), a potent greenhouse gas, is the second most important greenhouse gas contributor to climate change after carbon dioxide (CO2). The biological emissions of CH4 from wetlands are a major uncertainty in CH4 budgets. Microbial methanogenesis by Archaea is an anaerobic process accounting for most biological CH4 production in nature, yet recent observations indicate that large emissions can originate from oxygenated or frequently oxygenated wetland soil layers. To determine how oxygen (O2) can stimulate CH4 emissions, we used incubations of Sphagnum peat to demonstrate that the temporary exposure of peat to O2 can increase CH4 yields up to 2000-fold during subsequent anoxic conditions relative to peat without O2 exposure. Geochemical (including ion cyclotron resonance mass spectrometry, X-ray absorbance spectroscopy) and microbiome (16S rDNA amplicons, metagenomics) analyses of peat showed that higher CH4 yields of redox-oscillated peat were due to functional shifts in the peat microbiome arising during redox oscillation that enhanced peat carbon (C) degradation. Novosphingobium species with O2-dependent aromatic oxygenase genes increased greatly in relative abundance during the oxygenation period in redox-oscillated peat compared to anoxic controls. Acidobacteria species were particularly important for anaerobic processing of peat C, including in the production of methanogenic substrates H2 and CO2.more » Higher CO2 production during the anoxic phase of redox-oscillated peat stimulated hydrogenotrophic CH4 production by Methanobacterium species. The persistence of reduced iron (Fe(II)) during prolonged oxygenation in redox-oscillated peat may further enhance C degradation through abiotic mechanisms (e.g., Fenton reactions). The results indicate that specific functional shifts in the peat microbiome underlie O2 enhancement of CH4 production in acidic, Sphagnum-rich wetland soils. They also imply that understanding microbial dynamics spanning temporal and spatial redox transitions in peatlands is critical for constraining CH4 budgets; predicting feedbacks between climate change, hydrologic variability, and wetland CH4 emissions; and guiding wetland C management strategies.« less

Authors:
 [1]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [2];  [3];  [4]; ORCiD logo [1]
  1. Princeton Univ., NJ (United States)
  2. Rutgers Univ., New Brunswick, NJ (United States)
  3. Lesley University, Cambridge, MA (United States)
  4. Old Dominion Univ., Norfolk, VA (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF)
OSTI Identifier:
1826790
Grant/Contract Number:  
AC02-06CH11357; SC0012704; FG02-94ER14466; DGE 1842213; CHE-1610021; EAR-1128799
Resource Type:
Accepted Manuscript
Journal Name:
Global Change Biology
Additional Journal Information:
Journal Volume: 27; Journal Issue: 22; Journal ID: ISSN 1354-1013
Publisher:
Wiley
Country of Publication:
United States
Language:
ENGLISH
Subject:
54 ENVIRONMENTAL SCIENCES; carbon mitigation; carbon-climate feedback; climate change; peatland microbiome; soil microbial carbon cycling; soil redox dynamics; wetland management; wetland methane

Citation Formats

Wilmoth, Jared L., Schaefer, Jeffra K., Schlesinger, Danielle R., Roth, Spencer W., Hatcher, Patrick G., Shoemaker, Julie K., and Zhang, Xinning. The role of oxygen in stimulating methane production in wetlands. United States: N. p., 2021. Web. doi:10.1111/gcb.15831.
Wilmoth, Jared L., Schaefer, Jeffra K., Schlesinger, Danielle R., Roth, Spencer W., Hatcher, Patrick G., Shoemaker, Julie K., & Zhang, Xinning. The role of oxygen in stimulating methane production in wetlands. United States. https://doi.org/10.1111/gcb.15831
Wilmoth, Jared L., Schaefer, Jeffra K., Schlesinger, Danielle R., Roth, Spencer W., Hatcher, Patrick G., Shoemaker, Julie K., and Zhang, Xinning. Wed . "The role of oxygen in stimulating methane production in wetlands". United States. https://doi.org/10.1111/gcb.15831. https://www.osti.gov/servlets/purl/1826790.
@article{osti_1826790,
title = {The role of oxygen in stimulating methane production in wetlands},
author = {Wilmoth, Jared L. and Schaefer, Jeffra K. and Schlesinger, Danielle R. and Roth, Spencer W. and Hatcher, Patrick G. and Shoemaker, Julie K. and Zhang, Xinning},
abstractNote = {Methane (CH4), a potent greenhouse gas, is the second most important greenhouse gas contributor to climate change after carbon dioxide (CO2). The biological emissions of CH4 from wetlands are a major uncertainty in CH4 budgets. Microbial methanogenesis by Archaea is an anaerobic process accounting for most biological CH4 production in nature, yet recent observations indicate that large emissions can originate from oxygenated or frequently oxygenated wetland soil layers. To determine how oxygen (O2) can stimulate CH4 emissions, we used incubations of Sphagnum peat to demonstrate that the temporary exposure of peat to O2 can increase CH4 yields up to 2000-fold during subsequent anoxic conditions relative to peat without O2 exposure. Geochemical (including ion cyclotron resonance mass spectrometry, X-ray absorbance spectroscopy) and microbiome (16S rDNA amplicons, metagenomics) analyses of peat showed that higher CH4 yields of redox-oscillated peat were due to functional shifts in the peat microbiome arising during redox oscillation that enhanced peat carbon (C) degradation. Novosphingobium species with O2-dependent aromatic oxygenase genes increased greatly in relative abundance during the oxygenation period in redox-oscillated peat compared to anoxic controls. Acidobacteria species were particularly important for anaerobic processing of peat C, including in the production of methanogenic substrates H2 and CO2. Higher CO2 production during the anoxic phase of redox-oscillated peat stimulated hydrogenotrophic CH4 production by Methanobacterium species. The persistence of reduced iron (Fe(II)) during prolonged oxygenation in redox-oscillated peat may further enhance C degradation through abiotic mechanisms (e.g., Fenton reactions). The results indicate that specific functional shifts in the peat microbiome underlie O2 enhancement of CH4 production in acidic, Sphagnum-rich wetland soils. They also imply that understanding microbial dynamics spanning temporal and spatial redox transitions in peatlands is critical for constraining CH4 budgets; predicting feedbacks between climate change, hydrologic variability, and wetland CH4 emissions; and guiding wetland C management strategies.},
doi = {10.1111/gcb.15831},
journal = {Global Change Biology},
number = 22,
volume = 27,
place = {United States},
year = {Wed Aug 18 00:00:00 EDT 2021},
month = {Wed Aug 18 00:00:00 EDT 2021}
}

Works referenced in this record:

ATHENA , ARTEMIS , HEPHAESTUS : data analysis for X-ray absorption spectroscopy using IFEFFIT
journal, June 2005


Aerobic and anaerobic decomposition of organic matter in marine sediment: Which is fastest?
journal, December 1995

  • Kristensen, Erik; Ahmed, Saiyed I.; Devol, Allan H.
  • Limnology and Oceanography, Vol. 40, Issue 8
  • DOI: 10.4319/lo.1995.40.8.1430

Comparative Genomic Analysis Reveals Habitat-Specific Genes and Regulatory Hubs within the Genus Novosphingobium
journal, May 2017


Characterization of subsurface methane production and release over 3years at a New Hampshire wetland
journal, August 2012


The role of iron and reactive oxygen species in the production of CO2 in arctic soil waters
journal, March 2018

  • Trusiak, Adrianna; Treibergs, Lija A.; Kling, George W.
  • Geochimica et Cosmochimica Acta, Vol. 224
  • DOI: 10.1016/j.gca.2017.12.022

Drought drives rapid shifts in tropical rainforest soil biogeochemistry and greenhouse gas emissions
journal, April 2018

  • O’Connell, Christine S.; Ruan, Leilei; Silver, Whendee L.
  • Nature Communications, Vol. 9, Issue 1
  • DOI: 10.1038/s41467-018-03352-3

ATHENA and ARTEMIS Interactive Graphical Data Analysisusing IFEFFIT
journal, January 2005


Functional and Evolutionary Relationships Among Diverse Oxygenases
journal, October 1992


Uncoupling of acetate degradation from methane formation in Alaskan wetlands: Connections to vegetation distribution: PATHWAYS OF METHANOGENESIS IN WETLANDS
journal, May 2008

  • Hines, Mark E.; Duddleston, Khrystyne N.; Rooney-Varga, Juliette N.
  • Global Biogeochemical Cycles, Vol. 22, Issue 2
  • DOI: 10.1029/2006GB002903

Emerging role of wetland methane emissions in driving 21st century climate change
journal, August 2017

  • Zhang, Zhen; Zimmermann, Niklaus E.; Stenke, Andrea
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 36
  • DOI: 10.1073/pnas.1618765114

Heterogeneous Fenton Chemistry Revisited: Mechanistic Insights from Ferrihydrite-Mediated Oxidation of Formate and Oxalate
journal, May 2021

  • Chen, Yufan; Miller, Christopher J.; Waite, T. David
  • Environmental Science & Technology
  • DOI: 10.1021/acs.est.1c00284

Hydrogen regulation of growth, growth yields, and methane gene transcription in Methanobacterium thermoautotrophicum deltaH.
journal, January 1997


Potential origin and formation for molecular components of humic acids in soils
journal, April 2016


Molecular characterization of organic matter mobilized from Bangladeshi aquifer sediment: tracking carbon compositional change during microbial utilization
journal, January 2018

  • Pracht, Lara E.; Tfaily, Malak M.; Ardissono, Robert J.
  • Biogeosciences, Vol. 15, Issue 6
  • DOI: 10.5194/bg-15-1733-2018

MEGAN Community Edition - Interactive Exploration and Analysis of Large-Scale Microbiome Sequencing Data
journal, June 2016


Thermacetogenium phaeum gen. nov., sp. nov., a strictly anaerobic, thermophilic, syntrophic acetate-oxidizing bacterium
journal, July 2000

  • Hattori, S.; Kamagata, Y.; Hanada, S.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 50, Issue 4
  • DOI: 10.1099/00207713-50-4-1601

Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014


Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions
journal, November 2017


Methane Feedbacks to the Global Climate System in a Warmer World
journal, March 2018

  • Dean, Joshua F.; Middelburg, Jack J.; Röckmann, Thomas
  • Reviews of Geophysics, Vol. 56, Issue 1
  • DOI: 10.1002/2017RG000559

Phylogenetic Analysis and In Situ Identification of Bacteria Community Composition in an Acidic Sphagnum Peat Bog
journal, March 2006


Dark Formation of Hydroxyl Radical in Arctic Soil and Surface Waters
journal, October 2013

  • Page, Sarah E.; Kling, George W.; Sander, Michael
  • Environmental Science & Technology, Vol. 47, Issue 22
  • DOI: 10.1021/es4033265

Transport of oxygen in soil pore-water systems: implications for modeling emissions of carbon dioxide and methane from peatlands
journal, July 2014


Changes in peat chemistry associated with permafrost thaw increase greenhouse gas production
journal, April 2014

  • Hodgkins, S. B.; Tfaily, M. M.; McCalley, C. K.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 16
  • DOI: 10.1073/pnas.1314641111

A new perspective on the use of plant secondary metabolites to inhibit methanogenesis in the rumen
journal, August 2010


Oxygen effects on methane production and oxidation in humid tropical forest soils
journal, August 2005


Anoxic microsites in upland soils dominantly controlled by clay content
journal, March 2018


FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010


Establishing a Measure of Reproducibility of Ultrahigh-Resolution Mass Spectra for Complex Mixtures of Natural Organic Matter
journal, September 2012

  • Sleighter, Rachel L.; Chen, Hongmei; Wozniak, Andrew S.
  • Analytical Chemistry, Vol. 84, Issue 21
  • DOI: 10.1021/ac3018026

Interpreting contemporary trends in atmospheric methane
journal, February 2019

  • Turner, Alexander J.; Frankenberg, Christian; Kort, Eric A.
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 8
  • DOI: 10.1073/pnas.1814297116

Pathways for Methanogenesis and Diversity of Methanogenic Archaea in Three Boreal Peatland Ecosystems
journal, April 2005


Do oxic–anoxic transitions constrain organic matter mineralization in eutrophic freshwater wetlands?
journal, March 2016


Persistence of soil organic matter as an ecosystem property
journal, October 2011

  • Schmidt, Michael W. I.; Torn, Margaret S.; Abiven, Samuel
  • Nature, Vol. 478, Issue 7367
  • DOI: 10.1038/nature10386

Deblur Rapidly Resolves Single-Nucleotide Community Sequence Patterns
journal, March 2017


Fast and sensitive protein alignment using DIAMOND
journal, November 2014

  • Buchfink, Benjamin; Xie, Chao; Huson, Daniel H.
  • Nature Methods, Vol. 12, Issue 1
  • DOI: 10.1038/nmeth.3176

The role of reactive oxygen species in the degradation of lignin derived dissolved organic matter
journal, July 2017

  • Waggoner, Derek C.; Wozniak, Andrew S.; Cory, Rose M.
  • Geochimica et Cosmochimica Acta, Vol. 208
  • DOI: 10.1016/j.gca.2017.03.036

Hydrogenotrophic Methanogenesis by Moderately Acid-Tolerant Methanogens of a Methane-Emitting Acidic Peat
journal, January 2003


FQC Dashboard: integrates FastQC results into a web-based, interactive, and extensible FASTQ quality control tool
journal, June 2017


Anaerobic microbial biogeochemistry in a northern bog: Acetate as a dominant metabolic end product: ANAEROBIC MICROBIAL BIOGEOCHEMISTRY IN A NORTHERN BOG
journal, October 2002

  • Duddleston, Khrystyne N.; Kinney, Monica A.; Kiene, Ronald P.
  • Global Biogeochemical Cycles, Vol. 16, Issue 4
  • DOI: 10.1029/2001GB001402

Emissions of methane from northern peatlands: a review of management impacts and implications for future management options
journal, September 2016

  • Abdalla, Mohamed; Hastings, Astley; Truu, Jaak
  • Ecology and Evolution, Vol. 6, Issue 19
  • DOI: 10.1002/ece3.2469

Development of energetic and enzymatic limitations on microbial carbon cycling in soils
journal, March 2021


A synthesis of methane emissions from 71 northern, temperate, and subtropical wetlands
journal, April 2014

  • Turetsky, Merritt R.; Kotowska, Agnieszka; Bubier, Jill
  • Global Change Biology, Vol. 20, Issue 7
  • DOI: 10.1111/gcb.12580

The contentious nature of soil organic matter
journal, November 2015


Molecular heterogeneity in pyrogenic dissolved organic matter from a thermal series of oak and grass chars
journal, October 2020


Investigating nanoscale mineral compositions: Iron L 3 -edge spectroscopic evaluation of iron oxide and oxy-hydroxide coordination
journal, March 2017

  • von der Heyden, Bjorn P.; Roychoudhury, Alakendra N.; Tyliszczak, Tolek
  • American Mineralogist, Vol. 102, Issue 3
  • DOI: 10.2138/am-2017-5805

Genome sequence of the homoacetogenic bacterium Holophaga foetida type strain (TMBS4T)
journal, May 2012

  • Anderson, Iain; Held, Brittany; Lapidus, Alla
  • Standards in Genomic Sciences, Vol. 6, Issue 2
  • DOI: 10.4056/sigs.2746047

Isolation and Characterization of Novosphingobium sp. Strain MT1, a Dominant Polychlorophenol-Degrading Strain in a Groundwater Bioremediation System
journal, January 2002

  • Tiirola, Marja A.; Männistö, Minna K.; Puhakka, Jaakko A.
  • Applied and Environmental Microbiology, Vol. 68, Issue 1
  • DOI: 10.1128/AEM.68.1.173-180.2002

Biochemical determinants of litter quality in 15 species of Sphagnum
journal, February 2018


Tannins can slow-down but also speed-up soil enzymatic activity in boreal forest
journal, April 2017


Sphagnum mosses harbour highly specific bacterial diversity during their whole lifecycle
journal, November 2011

  • Bragina, Anastasia; Berg, Christian; Cardinale, Massimiliano
  • The ISME Journal, Vol. 6, Issue 4
  • DOI: 10.1038/ismej.2011.151

The methanogenic toxicity and anaerobic degradability of a hydrolyzable tannin
journal, March 1987


Vertical Stratification of Peat Pore Water Dissolved Organic Matter Composition in a Peat Bog in Northern Minnesota: Pore Water DOM composition in a peat bog
journal, February 2018

  • Tfaily, Malak M.; Wilson, Rachel M.; Cooper, William T.
  • Journal of Geophysical Research: Biogeosciences, Vol. 123, Issue 2
  • DOI: 10.1002/2017JG004007

An enzymic 'latch' on a global carbon store
journal, January 2001

  • Freeman, Chris; Ostle, Nick; Kang, Hojeong
  • Nature, Vol. 409, Issue 6817
  • DOI: 10.1038/35051650

QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

Large rainfall changes consistently projected over substantial areas of tropical land
journal, September 2015

  • Chadwick, Robin; Good, Peter; Martin, Gill
  • Nature Climate Change, Vol. 6, Issue 2
  • DOI: 10.1038/nclimate2805

A regulatory role for phenol oxidase during decomposition in peatlands
journal, October 2004


Methanogenic archaea: ecologically relevant differences in energy conservation
journal, June 2008

  • Thauer, Rudolf K.; Kaster, Anne-Kristin; Seedorf, Henning
  • Nature Reviews Microbiology, Vol. 6, Issue 8
  • DOI: 10.1038/nrmicro1931

PEAR: a fast and accurate Illumina Paired-End reAd mergeR
journal, October 2013


Methane dynamics in an alpine fen: a field-based study on methanogenic and methanotrophic microbial communities
journal, December 2014

  • Franchini, Alessandro G.; Henneberger, Ruth; Aeppli, Meret
  • FEMS Microbiology Ecology, Vol. 91, Issue 3
  • DOI: 10.1093/femsec/fiu032

Effect of Dissolved Natural Organic Matter on the Kinetics of Ferrous Iron Oxygenation in Seawater
journal, November 2003

  • Rose, Andrew L.
  • Environmental Science & Technology, Vol. 37, Issue 21
  • DOI: 10.1021/es034152g

Elemental composition and optical properties reveal changes in dissolved organic matter along a permafrost thaw chronosequence in a subarctic peatland
journal, August 2016

  • Hodgkins, Suzanne B.; Tfaily, Malak M.; Podgorski, David C.
  • Geochimica et Cosmochimica Acta, Vol. 187
  • DOI: 10.1016/j.gca.2016.05.015

Shift from Acetoclastic to H2-Dependent Methanogenesis in a West Siberian Peat Bog at Low pH Values and Isolation of an Acidophilic Methanobacterium Strain
journal, February 2007

  • Kotsyurbenko, O. R.; Friedrich, M. W.; Simankova, M. V.
  • Applied and Environmental Microbiology, Vol. 73, Issue 7
  • DOI: 10.1128/AEM.02413-06

Decrypting bacterial polyphenol metabolism in an anoxic wetland soil
journal, April 2021

  • McGivern, Bridget B.; Tfaily, Malak M.; Borton, Mikayla A.
  • Nature Communications, Vol. 12, Issue 1
  • DOI: 10.1038/s41467-021-22765-1

Phenol oxidase, peroxidase and organic matter dynamics of soil
journal, March 2010


Are oxygen limitations under recognized regulators of organic carbon turnover in upland soils?
journal, January 2016


Combination of six enzymes of a marine Novosphingobium converts the stereoisomers of β-O-4 lignin model dimers into the respective monomers
journal, October 2015

  • Ohta, Yukari; Nishi, Shinro; Hasegawa, Ryoichi
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep15105

Evaluation of the Orbitrap Mass Spectrometer for the Molecular Fingerprinting Analysis of Natural Dissolved Organic Matter
journal, July 2016


Expert assessment of future vulnerability of the global peatland carbon sink
journal, December 2020


Comparative study of organic matter chemical characterization using negative and positive mode electrospray ionization ultrahigh-resolution mass spectrometry
journal, February 2016

  • Ohno, Tsutomu; Sleighter, Rachel L.; Hatcher, Patrick G.
  • Analytical and Bioanalytical Chemistry, Vol. 408, Issue 10
  • DOI: 10.1007/s00216-016-9346-x

Short period of oxygenation releases latch on peat decomposition
journal, May 2014


Links between archaeal community structure, vegetation type and methanogenic pathway in Alaskan peatlands: Archaeal communities and methanogenesis in northern peatlands
journal, May 2007


Degradation of natural organic matter: A thermodynamic analysis
journal, April 2011

  • LaRowe, Douglas E.; Van Cappellen, Philippe
  • Geochimica et Cosmochimica Acta, Vol. 75, Issue 8
  • DOI: 10.1016/j.gca.2011.01.020

Drought-induced carbon loss in peatlands
journal, November 2011

  • Fenner, Nathalie; Freeman, Chris
  • Nature Geoscience, Vol. 4, Issue 12
  • DOI: 10.1038/ngeo1323

Evaluating the Classical Versus an Emerging Conceptual Model of Peatland Methane Dynamics: Peatland Methane Dynamics
journal, September 2017

  • Yang, Wendy H.; McNicol, Gavin; Teh, Yit Arn
  • Global Biogeochemical Cycles, Vol. 31, Issue 9
  • DOI: 10.1002/2017GB005622