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Title: Methane dynamics regulated by microbial community response to permafrost thaw

Abstract

Permafrost contains about 50% of the global soil carbon. It is thought that the thawing of permafrost can lead to a loss of soil carbon in the form of methane and carbon dioxide emissions. The magnitude of the resulting positive climate feedback of such greenhouse gas emissions is still unknown and may to a large extent depend on the poorly understood role of microbial community composition in regulating the metabolic processes that drive such ecosystem-scale greenhouse gas fluxes. Here we show that changes in vegetation and increasing methane emissions with permafrost thaw are associated with a switch from hydrogenotrophic to partly acetoclastic methanogenesis, resulting in a large shift in the δ13C signature (10–15‰) of emitted methane. We used a natural landscape gradient of permafrost thaw in northern Sweden as a model to investigate the role of microbial communities in regulating methane cycling, and to test whether a knowledge of community dynamics could improve predictions of carbon emissions under loss of permafrost. Abundance of the methanogen Candidatus ‘Methanoflorens stordalenmirensis’ is a key predictor of the shifts in methane isotopes, which in turn predicts the proportions of carbon emitted as methane and as carbon dioxide, an important factor for simulating the climatemore » feedback associated with permafrost thaw in global models. By showing that the abundance of key microbial lineages can be used to predict atmospherically relevant patterns in methane isotopes and the proportion of carbon metabolized to methane during permafrost thaw, we establish a basis for scaling changing microbial communities to ecosystem isotope dynamics. Here, our findings indicate that microbial ecology may be important in ecosystem-scale responses to global change.« less

Authors:
 [1];  [2];  [3];  [1];  [1];  [2];  [4];  [3];  [1];  [2];  [1]
+ Show Author Affiliations
  1. Univ. of Arizona, Tucson, AZ (United States)
  2. Univ. of Queensland, Brisbane, QLD (Australia)
  3. Florida State Univ., Tallahassee, FL (United States)
  4. Stockholm Univ. (Sweden)
Publication Date:
Research Org.:
Univ. of Arizona, Tucson, AZ (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1776499
Grant/Contract Number:  
SC0004632
Resource Type:
Accepted Manuscript
Journal Name:
Nature (London)
Additional Journal Information:
Journal Name: Nature (London); Journal Volume: 514; Journal Issue: 7523; Journal ID: ISSN 0028-0836
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; Biogeochemistry; Microbial ecology; Stable isotope analysis

Citation Formats

McCalley, Carmody K., Woodcroft, Ben J., Hodgkins, Suzanne B., Wehr, Richard A., Kim, Eun-Hae, Mondav, Rhiannon, Crill, Patrick M., Chanton, Jeffrey P., Rich, Virginia I., Tyson, Gene W., and Saleska, Scott R. Methane dynamics regulated by microbial community response to permafrost thaw. United States: N. p., 2014. Web. doi:10.1038/nature13798.
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McCalley, Carmody K., Woodcroft, Ben J., Hodgkins, Suzanne B., Wehr, Richard A., Kim, Eun-Hae, Mondav, Rhiannon, Crill, Patrick M., Chanton, Jeffrey P., Rich, Virginia I., Tyson, Gene W., & Saleska, Scott R. Methane dynamics regulated by microbial community response to permafrost thaw. United States. https://doi.org/10.1038/nature13798
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McCalley, Carmody K., Woodcroft, Ben J., Hodgkins, Suzanne B., Wehr, Richard A., Kim, Eun-Hae, Mondav, Rhiannon, Crill, Patrick M., Chanton, Jeffrey P., Rich, Virginia I., Tyson, Gene W., and Saleska, Scott R. Wed . "Methane dynamics regulated by microbial community response to permafrost thaw". United States. https://doi.org/10.1038/nature13798. https://www.osti.gov/servlets/purl/1776499.
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@article{osti_1776499,
title = {Methane dynamics regulated by microbial community response to permafrost thaw},
author = {McCalley, Carmody K. and Woodcroft, Ben J. and Hodgkins, Suzanne B. and Wehr, Richard A. and Kim, Eun-Hae and Mondav, Rhiannon and Crill, Patrick M. and Chanton, Jeffrey P. and Rich, Virginia I. and Tyson, Gene W. and Saleska, Scott R.},
abstractNote = {Permafrost contains about 50% of the global soil carbon. It is thought that the thawing of permafrost can lead to a loss of soil carbon in the form of methane and carbon dioxide emissions. The magnitude of the resulting positive climate feedback of such greenhouse gas emissions is still unknown and may to a large extent depend on the poorly understood role of microbial community composition in regulating the metabolic processes that drive such ecosystem-scale greenhouse gas fluxes. Here we show that changes in vegetation and increasing methane emissions with permafrost thaw are associated with a switch from hydrogenotrophic to partly acetoclastic methanogenesis, resulting in a large shift in the δ13C signature (10–15‰) of emitted methane. We used a natural landscape gradient of permafrost thaw in northern Sweden as a model to investigate the role of microbial communities in regulating methane cycling, and to test whether a knowledge of community dynamics could improve predictions of carbon emissions under loss of permafrost. Abundance of the methanogen Candidatus ‘Methanoflorens stordalenmirensis’ is a key predictor of the shifts in methane isotopes, which in turn predicts the proportions of carbon emitted as methane and as carbon dioxide, an important factor for simulating the climate feedback associated with permafrost thaw in global models. By showing that the abundance of key microbial lineages can be used to predict atmospherically relevant patterns in methane isotopes and the proportion of carbon metabolized to methane during permafrost thaw, we establish a basis for scaling changing microbial communities to ecosystem isotope dynamics. Here, our findings indicate that microbial ecology may be important in ecosystem-scale responses to global change.},
doi = {10.1038/nature13798},
journal = {Nature (London)},
number = 7523,
volume = 514,
place = {United States},
year = {Wed Oct 22 00:00:00 EDT 2014},
month = {Wed Oct 22 00:00:00 EDT 2014}
}
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    Community structure – Ecosystem function relationships in the Congo Basin methane cycle depend on the physiological scale of function
    journal, May 2020

    • Meyer, Kyle M.; Hopple, Anya M.; Klein, Ann M.
    • Molecular Ecology, Vol. 29, Issue 10
    • DOI: 10.1111/mec.15442

    The global methane budget 2000–2012
    journal, January 2016

    • Saunois, Marielle; Bousquet, Philippe; Poulter, Ben
    • Earth System Science Data, Vol. 8, Issue 2
    • DOI: 10.5194/essd-8-697-2016

    Seasonal time bombs: dominant temperate viruses affect Southern Ocean microbial dynamics
    journal, August 2015

    • Brum, Jennifer R.; Hurwitz, Bonnie L.; Schofield, Oscar
    • The ISME Journal, Vol. 10, Issue 2
    • DOI: 10.1038/ismej.2015.125

    Differential response of carbon cycling to long-term nutrient input and altered hydrological conditions in a continental Canadian peatland
    journal, January 2018

    • Berger, Sina; Praetzel, Leandra S. E.; Goebel, Marie
    • Biogeosciences, Vol. 15, Issue 3
    • DOI: 10.5194/bg-15-885-2018

    Nonequilibrium clumped isotope signals in microbial methane
    journal, March 2015

    The long-term fate of permafrost peatlands under rapid climate warming
    journal, December 2015

    • Swindles, Graeme T.; Morris, Paul J.; Mullan, Donal
    • Scientific Reports, Vol. 5, Issue 1
    • DOI: 10.1038/srep17951

    First evidence for cold-adapted anaerobic oxidation of methane in deep sediments of thermokarst lakes
    journal, March 2019

    • Winkel, M.; Sepulveda-Jauregui, A.; Martinez-Cruz, K.
    • Environmental Research Communications, Vol. 1, Issue 2
    • DOI: 10.1088/2515-7620/ab1042

    Host-linked soil viral ecology along a permafrost thaw gradient
    journal, July 2018

    Landscape topography structures the soil microbiome in arctic polygonal tundra
    journal, February 2018

    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

    Genome-centric view of carbon processing in thawing permafrost
    journal, July 2018

    Variation in Soil Methane Fluxes and Comparison between Two Forests in China
    journal, April 2018

    • Wei, Hua; Peng, Changhui; Liu, Shirong
    • Forests, Vol. 9, Issue 4
    • DOI: 10.3390/f9040204

    Distinct microbial communities in the active and permafrost layers on the Tibetan Plateau
    journal, November 2017

    • Chen, Yong-Liang; Deng, Ye; Ding, Jin-Zhi
    • Molecular Ecology, Vol. 26, Issue 23
    • DOI: 10.1111/mec.14396

    Ecosystem carbon response of an Arctic peatland to simulated permafrost thaw
    journal, February 2019

    • Voigt, Carolina; Marushchak, Maija E.; Mastepanov, Mikhail
    • Global Change Biology, Vol. 25, Issue 5
    • DOI: 10.1111/gcb.14574

    Winter precipitation and snow accumulation drive the methane sink or source strength of Arctic tussock tundra
    journal, May 2016

    • Blanc-Betes, Elena; Welker, Jeffrey M.; Sturchio, Neil C.
    • Global Change Biology, Vol. 22, Issue 8
    • DOI: 10.1111/gcb.13242

    Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes
    journal, March 2015

    • Hultman, Jenni; Waldrop, Mark P.; Mackelprang, Rachel
    • Nature, Vol. 521, Issue 7551
    • DOI: 10.1038/nature14238

    The global methane budget 2000--2012
    text, January 2016

    • Saunois, Marielle; Bousquet, Philippe; Poulter, Ben
    • Copernicus Publications
    • DOI: 10.7892/boris.91436

    Effect of permafrost thaw on plant and soil fungal community in a boreal forest: Does fungal community change mediate plant productivity response?
    journal, February 2019

    • Schütte, Ursel M. E.; Henning, Jeremiah A.; Ye, Yuzhen
    • Journal of Ecology, Vol. 107, Issue 4
    • DOI: 10.1111/1365-2745.13139

    Linking microbial communities to ecosystem functions: what we can learn from genotype–phenotype mapping in organisms
    journal, March 2020

    • Morris, Andrew; Meyer, Kyle; Bohannan, Brendan
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 375, Issue 1798
    • DOI: 10.1098/rstb.2019.0244

    Redox and temperature-sensitive changes in microbial communities and soil chemistry dictate greenhouse gas loss from thawed permafrost
    journal, July 2017

    • Ernakovich, Jessica G.; Lynch, Laurel M.; Brewer, Paul E.
    • Biogeochemistry, Vol. 134, Issue 1-2
    • DOI: 10.1007/s10533-017-0354-5

    Molecular mechanisms of water table lowering and nitrogen deposition in affecting greenhouse gas emissions from a Tibetan alpine wetland
    journal, September 2016

    • Wang, Hao; Yu, Lingfei; Zhang, Zhenhua
    • Global Change Biology, Vol. 23, Issue 2
    • DOI: 10.1111/gcb.13467

    Responses of tundra soil microbial communities to half a decade of experimental warming at two critical depths
    journal, July 2019

    • Johnston, Eric R.; Hatt, Janet K.; He, Zhili
    • Proceedings of the National Academy of Sciences, Vol. 116, Issue 30
    • DOI: 10.1073/pnas.1901307116

    Incorporation of Microbial Functional Traits in Biogeochemistry Models Provides Better Estimations of Benthic Denitrification and Anammox Rates in Coastal Oceans
    journal, October 2018

    • Zhang, Xiaoli; Zhang, Qianqian; Yang, Anjing
    • Journal of Geophysical Research: Biogeosciences, Vol. 123, Issue 10
    • DOI: 10.1029/2018jg004682

    Multi-year effect of wetting on CH4 flux at taiga–tundra boundary in northeastern Siberia deduced from stable isotope ratios of CH4
    journal, January 2019

    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

    Co-cultivation of the strictly anaerobic methanogen Methanosarcina barkeri with aerobic methanotrophs in an oxygen-limited membrane bioreactor
    journal, May 2018

    • in ’t Zandt, Michiel H.; van den Bosch, Tijs J. M.; Rijkers, Ruud
    • Applied Microbiology and Biotechnology, Vol. 102, Issue 13
    • DOI: 10.1007/s00253-018-9038-x

    Diversity and abundance of microbial eukaryotes in stream sediments from Svalbard
    journal, March 2017

    Stability of peatland carbon to rising temperatures
    journal, December 2016

    • Wilson, R. M.; Hopple, A. M.; Tfaily, M. M.
    • Nature Communications, Vol. 7, Article No. 13723
    • DOI: 10.1038/ncomms13723

    Methanotrophy across a natural permafrost thaw environment
    journal, June 2018

    • Singleton, Caitlin M.; McCalley, Carmody K.; Woodcroft, Ben J.
    • The ISME Journal, Vol. 12, Issue 10
    • DOI: 10.1038/s41396-018-0065-5

    Landscape topography structures the soil microbiome in arctic polygonal tundra
    journal, February 2018

    Tropical peatland carbon storage linked to global latitudinal trends in peat recalcitrance
    journal, September 2018

    • Hodgkins, Suzanne B.; Richardson, Curtis J.; Dommain, René
    • Nature Communications, Vol. 9, Issue 1
    • DOI: 10.1038/s41467-018-06050-2

    Host-linked soil viral ecology along a permafrost thaw gradient
    journal, July 2018

    Chemical Structure of the Lipid A component of Pseudomonas sp. strain PAMC 28618 from Thawing Permafrost in Relation to Pathogenicity
    journal, May 2017

    Key evidence of the role of desertification in protecting the underlying permafrost in the Qinghai–Tibet Plateau
    journal, October 2015

    • Xie, Shengbo; Qu, Jianjun; Lai, Yuanming
    • Scientific Reports, Vol. 5, Issue 1
    • DOI: 10.1038/srep15152

    The long-term fate of permafrost peatlands under rapid climate warming
    journal, December 2015

    • Swindles, Graeme T.; Morris, Paul J.; Mullan, Donal
    • Scientific Reports, Vol. 5, Issue 1
    • DOI: 10.1038/srep17951

    Archaeal and bacterial communities across a chronosequence of drained lake basins in arctic alaska
    journal, December 2015

    • Kao-Kniffin, J.; Woodcroft, B. J.; Carver, S. M.
    • Scientific Reports, Vol. 5, Issue 1
    • DOI: 10.1038/srep18165

    Bridging the divide: a model-data approach to Polar & Alpine Microbiology
    journal, January 2016

    Increases in temperature and nutrient availability positively affect methane‐cycling microorganisms in Arctic thermokarst lake sediments
    journal, September 2018

    • de Jong, Anniek E. E.; in ’t Zandt, Michiel H.; Meisel, Ove H.
    • Environmental Microbiology, Vol. 20, Issue 12
    • DOI: 10.1111/1462-2920.14345

    Metagenomics Reveals Pervasive Bacterial Populations and Reduced Community Diversity across the Alaska Tundra Ecosystem
    journal, April 2016

    • Johnston, Eric R.; Rodriguez-R, Luis M.; Luo, Chengwei
    • Frontiers in Microbiology, Vol. 7
    • DOI: 10.3389/fmicb.2016.00579

    Implication of Viral Infections for Greenhouse Gas Dynamics in Freshwater Wetlands: Challenges and Perspectives
    journal, August 2019

    • Bonetti, Giuditta; Trevathan-Tackett, Stacey M.; Carnell, Paul E.
    • Frontiers in Microbiology, Vol. 10
    • DOI: 10.3389/fmicb.2019.01962

    Biotic and Environmental Drivers of Plant Microbiomes Across a Permafrost Thaw Gradient
    journal, May 2020

    Toxic Algae Silence Physiological Responses to Multiple Climate Drivers in a Tropical Marine Food Chain
    journal, April 2019

    • Turner, Lucy M.; Havenhand, Jonathan N.; Alsterberg, Christian
    • Frontiers in Physiology, Vol. 10
    • DOI: 10.3389/fphys.2019.00373

    Reviews and syntheses: Four decades of modeling methane cycling in terrestrial ecosystems
    journal, January 2016

    Methane dynamics in the subarctic tundra: combining stable isotope analyses, plot- and ecosystem-scale flux measurements
    journal, January 2016

    The ratio of methanogens to methanotrophs and water-level dynamics drive methane transfer velocity in a temperate kettle-hole peat bog
    journal, January 2019

    The Global Methane Budget 2000–2017
    journal, January 2020

    • Saunois, Marielle; Stavert, Ann R.; Poulter, Ben
    • Earth System Science Data, Vol. 12, Issue 3
    • DOI: 10.5194/essd-12-1561-2020

    The global methane budget 2000–2012
    journal, January 2016

    • Saunois, Marielle; Bousquet, Philippe; Poulter, Ben
    • Earth System Science Data, Vol. 8, Issue 2
    • DOI: 10.5194/essd-8-697-2016

    Climate warming over the past half century has led to thermal degradation of permafrost on the Qinghai–Tibet Plateau
    journal, January 2018

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