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Title: Methanotrophy across a natural permafrost thaw environment

Abstract

The fate of carbon sequestered in permafrost is a key concern for future global warming as this large carbon stock is rapidly becoming a net methane source due to widespread thaw. Methane release from permafrost is moderated by methanotrophs, which oxidise 20-60% of this methane before emission to the atmosphere. Despite the importance of methanotrophs to carbon cycling, these microorganisms are under-characterised and have not been studied across a natural permafrost thaw gradient. Here, we examine methanotroph communities from the active layer of a permafrost thaw gradient in Stordalen Mire (Abisko, Sweden) spanning three years, analysing 188 metagenomes and 24 metatranscriptomes paired with in situ biogeochemical data. Methanotroph community composition and activity varied significantly as thaw progressed from intact permafrost palsa, to partially-thawed bog and fully-thawed fen. Thirteen methanotroph population genomes were recovered, including two novel genomes belonging to the uncultivated upland soil cluster alpha (USCα) group and a novel potentially methanotrophic Hyphomicrobiaceae. Combined analysis of porewater δ 13C-CH 4 isotopes and methanotroph abundances showed methane oxidation was greatest below the oxic-anoxic interface in the bog. Here, these results detail the direct effect of thaw on autochthonous methanotroph communities, and their consequent changes in population structure, activity, and methane moderationmore » potential.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1];  [1];  [1]; ORCiD logo [3]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [5]; ORCiD logo [6]; ORCiD logo [7]; ORCiD logo [1]
  1. Univ. of Queensland, Brisbane, QLD (Australia)
  2. Rochester Institute of Technology, Rochester, NY (United States)
  3. Florida State Univ., Tallahassee, FL (United States)
  4. Univ. of New Hampshire, Durham, NH (United States)
  5. Stockholm Univ., Stockholm (Sweden)
  6. Univ. of Arizona, Tucson, AZ (United States)
  7. The Ohio State Univ., Columbus, OH (United States)
Publication Date:
Research Org.:
Univ. of Queensland, Brisbane, QLD (Australia). Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1481728
Grant/Contract Number:  
SC0016440
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 12; Journal Issue: 10; Related Information: Raw DNA and RNA sequencing data:https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA386568; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; 58 GEOSCIENCES; Methanotrophs; Permafrost; Bacteria; Metagenomics

Citation Formats

Singleton, Caitlin M., McCalley, Carmody K., Woodcroft, Ben J., Boyd, Joel A., Evans, Paul N., Hodgkins, Suzanne B., Chanton, Jeffrey P., Frolking, Steve, Crill, Patrick M., Saleska, Scott R., Rich, Virginia I., and Tyson, Gene W. Methanotrophy across a natural permafrost thaw environment. United States: N. p., 2018. Web. doi:10.1038/s41396-018-0065-5.
Singleton, Caitlin M., McCalley, Carmody K., Woodcroft, Ben J., Boyd, Joel A., Evans, Paul N., Hodgkins, Suzanne B., Chanton, Jeffrey P., Frolking, Steve, Crill, Patrick M., Saleska, Scott R., Rich, Virginia I., & Tyson, Gene W. Methanotrophy across a natural permafrost thaw environment. United States. doi:10.1038/s41396-018-0065-5.
Singleton, Caitlin M., McCalley, Carmody K., Woodcroft, Ben J., Boyd, Joel A., Evans, Paul N., Hodgkins, Suzanne B., Chanton, Jeffrey P., Frolking, Steve, Crill, Patrick M., Saleska, Scott R., Rich, Virginia I., and Tyson, Gene W. Thu . "Methanotrophy across a natural permafrost thaw environment". United States. doi:10.1038/s41396-018-0065-5. https://www.osti.gov/servlets/purl/1481728.
@article{osti_1481728,
title = {Methanotrophy across a natural permafrost thaw environment},
author = {Singleton, Caitlin M. and McCalley, Carmody K. and Woodcroft, Ben J. and Boyd, Joel A. and Evans, Paul N. and Hodgkins, Suzanne B. and Chanton, Jeffrey P. and Frolking, Steve and Crill, Patrick M. and Saleska, Scott R. and Rich, Virginia I. and Tyson, Gene W.},
abstractNote = {The fate of carbon sequestered in permafrost is a key concern for future global warming as this large carbon stock is rapidly becoming a net methane source due to widespread thaw. Methane release from permafrost is moderated by methanotrophs, which oxidise 20-60% of this methane before emission to the atmosphere. Despite the importance of methanotrophs to carbon cycling, these microorganisms are under-characterised and have not been studied across a natural permafrost thaw gradient. Here, we examine methanotroph communities from the active layer of a permafrost thaw gradient in Stordalen Mire (Abisko, Sweden) spanning three years, analysing 188 metagenomes and 24 metatranscriptomes paired with in situ biogeochemical data. Methanotroph community composition and activity varied significantly as thaw progressed from intact permafrost palsa, to partially-thawed bog and fully-thawed fen. Thirteen methanotroph population genomes were recovered, including two novel genomes belonging to the uncultivated upland soil cluster alpha (USCα) group and a novel potentially methanotrophic Hyphomicrobiaceae. Combined analysis of porewater δ13C-CH4 isotopes and methanotroph abundances showed methane oxidation was greatest below the oxic-anoxic interface in the bog. Here, these results detail the direct effect of thaw on autochthonous methanotroph communities, and their consequent changes in population structure, activity, and methane moderation potential.},
doi = {10.1038/s41396-018-0065-5},
journal = {The ISME Journal},
number = 10,
volume = 12,
place = {United States},
year = {2018},
month = {6}
}

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Cited by: 11 works
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    journal, July 2008


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    • Keltjens, Jan T.; Pol, Arjan; Reimann, Joachim
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    • Neumann, Rebecca B.; Blazewicz, Steven J.; Conaway, Christopher H.
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    Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms
    journal, September 2012

    • Tveit, Alexander; Schwacke, Rainer; Svenning, Mette M.
    • The ISME Journal, Vol. 7, Issue 2
    • DOI: 10.1038/ismej.2012.99

    The (d)evolution of methanotrophy in the Beijerinckiaceae—a comparative genomics analysis
    journal, August 2013


    An active atmospheric methane sink in high Arctic mineral cryosols
    journal, April 2015

    • Lau, M. C. Y.; Stackhouse, B. T.; Layton, A. C.
    • The ISME Journal, Vol. 9, Issue 8
    • DOI: 10.1038/ismej.2015.13

    Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival
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    • Greening, Chris; Biswas, Ambarish; Carere, Carlo R.
    • The ISME Journal, Vol. 10, Issue 3
    • DOI: 10.1038/ismej.2015.153

    Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center
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    • Anantharaman, Karthik; Breier, John A.; Dick, Gregory J.
    • The ISME Journal, Vol. 10, Issue 1
    • DOI: 10.1038/ismej.2015.81

    Methylacidiphilum fumariolicum SolV, a thermoacidophilic ‘Knallgas’ methanotroph with both an oxygen-sensitive and -insensitive hydrogenase
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    • Mohammadi, Sepehr; Pol, Arjan; van Alen, Theo A.
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    • DOI: 10.1038/ismej.2016.171

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    • Nature, Vol. 450, Issue 7171
    • DOI: 10.1038/nature06222

    Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia
    journal, November 2007

    • Dunfield, Peter F.; Yuryev, Anton; Senin, Pavel
    • Nature, Vol. 450, Issue 7171
    • DOI: 10.1038/nature06411

    Nitrite-driven anaerobic methane oxidation by oxygenic bacteria
    journal, March 2010

    • Ettwig, Katharina F.; Butler, Margaret K.; Le Paslier, Denis
    • Nature, Vol. 464, Issue 7288
    • DOI: 10.1038/nature08883

    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

    Climate change and the permafrost carbon feedback
    journal, April 2015

    • Schuur, E. A. G.; McGuire, A. D.; Schädel, C.
    • Nature, Vol. 520, Issue 7546
    • DOI: 10.1038/nature14338

    Discovery of a novel methanogen prevalent in thawing permafrost
    journal, February 2014

    • Mondav, Rhiannon; Woodcroft, Ben J.; Kim, Eun-Hae
    • Nature Communications, Vol. 5, Issue 1
    • DOI: 10.1038/ncomms4212

    Identification and characterization of multiple rubisco activases in chemoautotrophic bacteria
    journal, November 2015

    • Tsai, Yi-Chin Candace; Lapina, Maria Claribel; Bhushan, Shashi
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