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Title: Stability of peatland carbon to rising temperatures

Abstract

Peatlands contain one-third of the world’s soil carbon (C), mostly in the deep permanently saturated anoxic zone (i.e., catotelm)1 where C mineralization rates may be constrained, in part, by low temperatures; yet all soil warming experiments to date have focused on the response of peatland C degradation to surface warming2, 3. If the slow decomposition of deep peat C is due to kinetic constraints, then increasing temperatures at depth should cause parallel increases in carbon dioxide (CO2) and/or methane (CH4) production rates. Increasing CH4 emissions are of particular concern because CH4 has a sustained-flux global warming potential (SGWP) 45-times greater than CO2 over a 100- year timeframe4, creating a significant positive feedback to climate warming. Using a novel whole-ecosystem scale experiment in a regression-based design we show that ecosystem scale warming of deep peat exponentially increased CH4 emissions —but not ecosystem respiration of CO2— in the first year. Multiple lines of evidence, including laboratory incubations and in situ analyses of 14C, dissolved gases, and microbial community metabolic potential, indicate that CH4 emissions increased due to surface processes and not degradation of deep C. Our results indicate that rapid changes to the large bank of deep buried C in temperate peatlandsmore » may be minimal under future climatic warming.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [2];  [6];  [7];  [8];  [8];  [4];  [5];  [6];  [7];  [5];  [1];  [2];  [5]
  1. Florida State Univ., Tallahassee, FL (United States). Earth, Ocean and Atmospheric Sciences
  2. Univ. of Oregon, Eugene, OR (United States). Inst. of Ecology and Evolution
  3. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab.
  4. USDA Forest Service Northern Research Station, Grand Rapids, MN (United States)
  5. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  6. Chapman Univ., Orange, CA (United States). Schmid College of Science and Technology
  7. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  8. Georgia Inst. of Technology, Atlanta, GA (United States). School of Biological Sciences and School of Earth and Atmospheric Sciences
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1336572
Alternate Identifier(s):
OSTI ID: 1339878
Report Number(s):
PNNL-SA-118747
Journal ID: ISSN 2041-1723; KP1702010; ERKP788
Grant/Contract Number:  
AC05-00OR22725; AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; Environmental Molecular Sciences Laboratory; carbon cycle

Citation Formats

Wilson, R. M., Hopple, A. M., Tfaily, M. M., Sebestyen, S. D., Schadt, C. W., Pfeifer-Meister, L., Medvedeff, C., McFarlane, K. J., Kostka, J. E., Kolton, M., Kolka, R. K., Kluber, L. A., Keller, J. K., Guilderson, T. P., Griffiths, N. A., Chanton, J. P., Bridgham, S. D., and Hanson, P. J. Stability of peatland carbon to rising temperatures. United States: N. p., 2016. Web. doi:10.1038/ncomms13723.
Wilson, R. M., Hopple, A. M., Tfaily, M. M., Sebestyen, S. D., Schadt, C. W., Pfeifer-Meister, L., Medvedeff, C., McFarlane, K. J., Kostka, J. E., Kolton, M., Kolka, R. K., Kluber, L. A., Keller, J. K., Guilderson, T. P., Griffiths, N. A., Chanton, J. P., Bridgham, S. D., & Hanson, P. J. Stability of peatland carbon to rising temperatures. United States. doi:10.1038/ncomms13723.
Wilson, R. M., Hopple, A. M., Tfaily, M. M., Sebestyen, S. D., Schadt, C. W., Pfeifer-Meister, L., Medvedeff, C., McFarlane, K. J., Kostka, J. E., Kolton, M., Kolka, R. K., Kluber, L. A., Keller, J. K., Guilderson, T. P., Griffiths, N. A., Chanton, J. P., Bridgham, S. D., and Hanson, P. J. Tue . "Stability of peatland carbon to rising temperatures". United States. doi:10.1038/ncomms13723. https://www.osti.gov/servlets/purl/1336572.
@article{osti_1336572,
title = {Stability of peatland carbon to rising temperatures},
author = {Wilson, R. M. and Hopple, A. M. and Tfaily, M. M. and Sebestyen, S. D. and Schadt, C. W. and Pfeifer-Meister, L. and Medvedeff, C. and McFarlane, K. J. and Kostka, J. E. and Kolton, M. and Kolka, R. K. and Kluber, L. A. and Keller, J. K. and Guilderson, T. P. and Griffiths, N. A. and Chanton, J. P. and Bridgham, S. D. and Hanson, P. J.},
abstractNote = {Peatlands contain one-third of the world’s soil carbon (C), mostly in the deep permanently saturated anoxic zone (i.e., catotelm)1 where C mineralization rates may be constrained, in part, by low temperatures; yet all soil warming experiments to date have focused on the response of peatland C degradation to surface warming2, 3. If the slow decomposition of deep peat C is due to kinetic constraints, then increasing temperatures at depth should cause parallel increases in carbon dioxide (CO2) and/or methane (CH4) production rates. Increasing CH4 emissions are of particular concern because CH4 has a sustained-flux global warming potential (SGWP) 45-times greater than CO2 over a 100- year timeframe4, creating a significant positive feedback to climate warming. Using a novel whole-ecosystem scale experiment in a regression-based design we show that ecosystem scale warming of deep peat exponentially increased CH4 emissions —but not ecosystem respiration of CO2— in the first year. Multiple lines of evidence, including laboratory incubations and in situ analyses of 14C, dissolved gases, and microbial community metabolic potential, indicate that CH4 emissions increased due to surface processes and not degradation of deep C. Our results indicate that rapid changes to the large bank of deep buried C in temperate peatlands may be minimal under future climatic warming.},
doi = {10.1038/ncomms13723},
journal = {Nature Communications},
number = ,
volume = 7,
place = {United States},
year = {2016},
month = {12}
}

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Works referenced in this record:

SPRUCE Stability of Peatland Carbon to Rising Temperatures: Supporting Data
dataset, January 2016


A method for experimental heating of intact soil profiles for application to climate change experiments: EXPERIMENTAL HEATING OF INTACT SOIL PROFILES
journal, January 2011


Vascular plants promote ancient peatland carbon loss with climate warming
journal, March 2016

  • Walker, Tom N.; Garnett, Mark H.; Ward, Susan E.
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Measuring phenol oxidase and peroxidase activities with pyrogallol, l-DOPA, and ABTS: Effect of assay conditions and soil type
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Temperature the dominant control on the enzyme-latch across a range of temperate peatland types
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Microbial Community Stratification Linked to Utilization of Carbohydrates and Phosphorus Limitation in a Boreal Peatland at Marcell Experimental Forest, Minnesota, USA
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Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
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Intermediate-scale community-level flux of CO2 and CH4 in a Minnesota peatland: putting the SPRUCE project in a global context
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Cultivating Uncultured Bacteria from Northern Wetlands: Knowledge Gained and Remaining Gaps
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Evidence for a nonmonotonic relationship between ecosystem-scale peatland methane emissions and water table depth
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The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill b
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Biogenic methane formation in marine and freshwater environments: CO2 reduction vs. acetate fermentation—Isotope evidence
journal, May 1986


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Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
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Biodegradability of Vegetation-Derived Dissolved Organic Carbon in a Cool Temperate Ombrotrophic Bog
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The Distribution and Stable Carbon Isotopic Composition of Dissolved Organic Carbon in Estuaries
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  • Estuaries, Vol. 17, Issue 1
  • DOI: 10.2307/1352560

Soil Warming and Carbon-Cycle Feedbacks to the Climate System
journal, December 2002


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


The carbon balance of North American wetlands
journal, December 2006


A Daily Soil Temperature Dataset and Soil Temperature Climatology of the Contiguous United States
journal, August 2003


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Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction
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Methane fluxes show consistent temperature dependence across microbial to ecosystem scales
journal, March 2014

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Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
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  • DOI: 10.1038/ismej.2012.8

A comment on “Appropriate experimental ecosystem warming methods by ecosystem, objective, and practicality” by Aronson and McNulty
journal, March 2010


UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
journal, December 2005


Carbon respiration from subsurface peat accelerated by climate warming in the subarctic
journal, July 2009

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Aspects of the chemical structure of soil organic materials as revealed by solid-state13C NMR spectroscopy
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Sensitivity of peatland carbon loss to organic matter quality: PEAT QUALITY AND CARBON LOSS
journal, July 2012

  • Leifeld, Jens; Steffens, Markus; Galego-Sala, Angela
  • Geophysical Research Letters, Vol. 39, Issue 14
  • DOI: 10.1029/2012GL051856

SPRUCE Stability of Peatland Carbon to Rising Temperatures: Supporting Data
dataset, January 2016


Aspects of the chemical structure of soil organic materials as revealed by solid-state13C NMR spectroscopy
journal, January 1992

  • Baldock, J. A.; Oades, J. M.; Waters, A. G.
  • Biogeochemistry, Vol. 16, Issue 1
  • DOI: 10.1007/bf00024251

A new model of Holocene peatland net primary production, decomposition, water balance, and peat accumulation
journal, January 2010

  • Frolking, S.; Roulet, N. T.; Tuittila, E.
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    Works referencing / citing this record:

    SPRUCE Stability of Peatland Carbon to Rising Temperatures: Supporting Data
    dataset, January 2016


    Surface production fuels deep heterotrophic respiration in northern peatlands: HETEROTROPHIC RESPIRATION IN PEATLANDS
    journal, December 2013

    • Elizabeth Corbett, J.; Burdige, David J.; Tfaily, Malak M.
    • Global Biogeochemical Cycles, Vol. 27, Issue 4
    • DOI: 10.1002/2013gb004677

    Organic matter transformation in the peat column at Marcell Experimental Forest: Humification and vertical stratification: Organic matter dynamics
    journal, April 2014

    • Tfaily, Malak M.; Cooper, William T.; Kostka, Joel E.
    • Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 4
    • DOI: 10.1002/2013jg002492

    Evidence for a nonmonotonic relationship between ecosystem-scale peatland methane emissions and water table depth
    journal, May 2014

    • Brown, Mathew G.; Humphreys, Elyn R.; Moore, Tim R.
    • Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 5
    • DOI: 10.1002/2013jg002576

    Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction
    journal, January 2005

    • Yu, Youngseob; Lee, Changsoo; Kim, Jaai
    • Biotechnology and Bioengineering, Vol. 89, Issue 6
    • DOI: 10.1002/bit.20347

    Aspects of the chemical structure of soil organic materials as revealed by solid-state13C NMR spectroscopy
    journal, February 1992

    • Baldock, J. A.; Oades, J. M.; Waters, A. G.
    • Biogeochemistry, Vol. 16, Issue 1
    • DOI: 10.1007/bf02402261

    Moving Beyond Global Warming Potentials to Quantify the Climatic Role of Ecosystems
    journal, May 2015


    Biodegradability of Vegetation-Derived Dissolved Organic Carbon in a Cool Temperate Ombrotrophic Bog
    journal, May 2016


    Intermediate-scale community-level flux of CO2 and CH4 in a Minnesota peatland: putting the SPRUCE project in a global context
    journal, August 2016


    Linking habitat modification to catastrophic shifts and vegetation patterns in bogs
    journal, June 2007


    Biogenic methane formation in marine and freshwater environments: CO2 reduction vs. acetate fermentation—Isotope evidence
    journal, May 1986


    A comment on “Appropriate experimental ecosystem warming methods by ecosystem, objective, and practicality” by Aronson and McNulty
    journal, March 2010


    ABTS assay of phenol oxidase activity in soil
    journal, December 2007

    • Floch, Carine; Alarcon-Gutiérrez, Enrique; Criquet, Stéven
    • Journal of Microbiological Methods, Vol. 71, Issue 3
    • DOI: 10.1016/j.mimet.2007.09.020

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


    Measuring phenol oxidase and peroxidase activities with pyrogallol, l-DOPA, and ABTS: Effect of assay conditions and soil type
    journal, December 2013


    Temperature the dominant control on the enzyme-latch across a range of temperate peatland types
    journal, June 2016


    Short-term response of methane fluxes and methanogen activity to water table and soil warming manipulations in an Alaskan peatland
    journal, January 2008

    • Turetsky, M. R.; Treat, C. C.; Waldrop, M. P.
    • Journal of Geophysical Research, Vol. 113
    • DOI: 10.1029/2007jg000496

    Sensitivity of peatland carbon loss to organic matter quality: PEAT QUALITY AND CARBON LOSS
    journal, July 2012

    • Leifeld, Jens; Steffens, Markus; Galego-Sala, Angela
    • Geophysical Research Letters, Vol. 39, Issue 14
    • DOI: 10.1029/2012gl051856

    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

    Acclimatization of soil respiration to warming in a tall grass prairie
    journal, October 2001

    • Luo, Yiqi; Wan, Shiqiang; Hui, Dafeng
    • Nature, Vol. 413, Issue 6856
    • DOI: 10.1038/35098065

    UniFrac: an effective distance metric for microbial community comparison
    journal, September 2010

    • Lozupone, Catherine; Lladser, Manuel E.; Knights, Dan
    • The ISME Journal, Vol. 5, Issue 2
    • DOI: 10.1038/ismej.2010.133

    Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
    journal, March 2012

    • Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
    • The ISME Journal, Vol. 6, Issue 8
    • DOI: 10.1038/ismej.2012.8

    Carbon respiration from subsurface peat accelerated by climate warming in the subarctic
    journal, July 2009

    • Dorrepaal, Ellen; Toet, Sylvia; van Logtestijn, Richard S. P.
    • Nature, Vol. 460, Issue 7255
    • DOI: 10.1038/nature08216

    Methane fluxes show consistent temperature dependence across microbial to ecosystem scales
    journal, March 2014

    • Yvon-Durocher, Gabriel; Allen, Andrew P.; Bastviken, David
    • Nature, Vol. 507, Issue 7493
    • DOI: 10.1038/nature13164

    Methane dynamics regulated by microbial community response to permafrost thaw
    journal, October 2014

    • McCalley, Carmody K.; Woodcroft, Ben J.; Hodgkins, Suzanne B.
    • Nature, Vol. 514, Issue 7523
    • DOI: 10.1038/nature13798

    Potential carbon emissions dominated by carbon dioxide from thawed permafrost soils
    journal, June 2016

    • Schädel, Christina; Bader, Martin K. -F.; Schuur, Edward A. G.
    • Nature Climate Change, Vol. 6, Issue 10
    • DOI: 10.1038/nclimate3054

    Differential abundance analysis for microbial marker-gene surveys
    journal, September 2013

    • Paulson, Joseph N.; Stine, O. Colin; Bravo, Héctor Corrada
    • Nature Methods, Vol. 10, Issue 12
    • DOI: 10.1038/nmeth.2658

    Ecosystem warming extends vegetation activity but heightens vulnerability to cold temperatures
    journal, August 2018

    • Richardson, Andrew D.; Hufkens, Koen; Milliman, Thomas
    • Nature, Vol. 560, Issue 7718, p. 368-371
    • DOI: 10.1038/s41586-018-0399-1

    Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample
    journal, June 2010

    • Caporaso, J. G.; Lauber, C. L.; Walters, W. A.
    • Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
    • DOI: 10.1073/pnas.1000080107

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


    The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill b
    journal, November 2002


    Methanogenic archaea database containing physiological and biochemical characteristics
    journal, April 2015

    • Łukaszewicz, Marcin; Jabłoński, Sławomir; Rodowicz, Paweł
    • International Journal of Systematic and Evolutionary Microbiology, Vol. 65, Issue 4
    • DOI: 10.1099/ijs.0.000065

    Vascular plants promote ancient peatland carbon loss with climate warming
    journal, March 2016

    • Walker, Tom N.; Garnett, Mark H.; Ward, Susan E.
    • Global Change Biology, Vol. 22, Issue 5
    • DOI: 10.1111/gcb.13213

    A method for experimental heating of intact soil profiles for application to climate change experiments: EXPERIMENTAL HEATING OF INTACT SOIL PROFILES
    journal, January 2011


    Temperature Responses to Infrared-Loading and Water Table Manipulations in Peatland Mesocosms
    journal, October 2008


    Soil Warming and Carbon-Cycle Feedbacks to the Climate System
    journal, December 2002


    Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
    journal, June 2007

    • Wang, Q.; Garrity, G. M.; Tiedje, J. M.
    • Applied and Environmental Microbiology, Vol. 73, Issue 16
    • DOI: 10.1128/aem.00062-07

    Microbial Community Stratification Linked to Utilization of Carbohydrates and Phosphorus Limitation in a Boreal Peatland at Marcell Experimental Forest, Minnesota, USA
    journal, March 2014

    • Lin, Xueju; Tfaily, Malak M.; Steinweg, J. Megan
    • Applied and Environmental Microbiology, Vol. 80, Issue 11
    • DOI: 10.1128/aem.00205-14

    Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
    journal, October 2009

    • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
    • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
    • DOI: 10.1128/aem.01541-09

    PCR Primers That Amplify Fungal rRNA Genes from Environmental Samples
    journal, October 2000


    UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
    journal, December 2005


    Peatlands in the Earth’s 21st century climate system
    journal, December 2011

    • Frolking, Steve; Talbot, Julie; Jones, Miriam C.
    • Environmental Reviews, Vol. 19, Issue NA
    • DOI: 10.1139/a11-014

    A Daily Soil Temperature Dataset and Soil Temperature Climatology of the Contiguous United States
    journal, August 2003


    The Earth Microbiome project: successes and aspirations
    journal, August 2014


    The carbon balance of North American wetlands
    journal, December 2006


    Rapid Carbon Response of Peatlands to Climate Change
    journal, November 2008

    • Bridgham, Scott D.; Pastor, John; Dewey, Bradley
    • Ecology, Vol. 89, Issue 11
    • DOI: 10.1890/08-0279.1

    The Distribution and Stable Carbon Isotopic Composition of Dissolved Organic Carbon in Estuaries
    journal, March 1994

    • Peterson, Bruce; Fry, Brian; Hullar, Meredith
    • Estuaries, Vol. 17, Issue 1
    • DOI: 10.2307/1352560

    Environmental and Substrate Controls over Carbon and Nitrogen Mineralization in Northern Wetlands
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