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Title: Genome-centric view of carbon processing in thawing permafrost

Abstract

As global temperatures rise, large amounts of carbon sequestered in permafrost are becoming available for microbial degradation. Accurate prediction of carbon gas emissions from thawing permafrost is limited by our understanding of these microbial communities. Here we use metagenomic sequencing of 214 samples from a permafrost thaw gradient to recover 1,529 metagenome-assembled genomes, including many from phyla with poor genomic representation. These genomes reflect the diversity of this complex ecosystem, with genus-level representatives for more than sixty per cent of the community. Meta-omic analysis revealed key populations involved in the degradation of organic matter, including bacteria whose genomes encode a previously undescribed fungal pathway for xylose degradation. Microbial and geochemical data highlight lineages that correlate with the production of greenhouse gases and indicate novel syntrophic relationships. Lastly, our findings link changing biogeochemistry to specific microbial lineages involved in carbon processing, and provide key information for predicting the effects of climate change on permafrost systems.

Authors:
ORCiD logo [1]; ORCiD logo [1];  [1];  [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [1];  [1]; ORCiD logo [4]; ORCiD logo [5];  [5]; ORCiD logo [6]; ORCiD logo [6];  [7];  [7];  [5];  [8]; ORCiD logo [9]; ORCiD logo [3]; ORCiD logo [1]
+ Show Author Affiliations
  1. Univ. of Queensland, Brisbane, QLD (Australia)
  2. The Ohio State Univ., Columbus, OH (United States); Univ. of California, Davis, CA (United States)
  3. The Ohio State Univ., Columbus, OH (United States)
  4. Rochester Institute of Technology, Rochester, NY (United States)
  5. Florida State Univ., Tallahassee, FL (United States)
  6. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  7. Univ. of New Hampshire, Durham, NH (United States)
  8. Stockholm Univ., Stockholm (Sweden)
  9. Univ. of Arizona, Tucson, AZ (United States)
Publication Date:
Research Org.:
Univ. of Arizona, Tucson, AZ (United States); The Ohio State Univ., Columbus, OH (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Contributing Org.:
Univ. of Queensland, Brisbane, QLD (Australia). Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences
OSTI Identifier:
1481643
Grant/Contract Number:  
SC0010580; SC0016440
Resource Type:
Accepted Manuscript
Journal Name:
Nature (London)
Additional Journal Information:
Journal Name: Nature (London); Journal Volume: 560; Journal Issue: 7716; Related Information: Raw metagenome and metatranscriptomes from the study: https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA386568; Journal ID: ISSN 0028-0836
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 58 GEOSCIENCES; 59 BASIC BIOLOGICAL SCIENCES; Permafrost; Metagenomics; Metatranscriptomics; Metaproteomics; Biogeochemistry; Bacteria; Archaea

Citation Formats

Woodcroft, Ben J., Singleton, Caitlin M., Boyd, Joel A., Evans, Paul N., Emerson, Joanne B., Zayed, Ahmed A. F., Hoelzle, Robert D., Lamberton, Timothy O., McCalley, Carmody K., Hodgkins, Suzanne B., Wilson, Rachel M., Purvine, Samuel O., Nicora, Carrie D., Li, Changsheng, Frolking, Steve, Chanton, Jeffrey P., Crill, Patrick M., Saleska, Scott R., Rich, Virginia I., and Tyson, Gene W. Genome-centric view of carbon processing in thawing permafrost. United States: N. p., 2018. Web. doi:10.1038/s41586-018-0338-1.
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Woodcroft, Ben J., Singleton, Caitlin M., Boyd, Joel A., Evans, Paul N., Emerson, Joanne B., Zayed, Ahmed A. F., Hoelzle, Robert D., Lamberton, Timothy O., McCalley, Carmody K., Hodgkins, Suzanne B., Wilson, Rachel M., Purvine, Samuel O., Nicora, Carrie D., Li, Changsheng, Frolking, Steve, Chanton, Jeffrey P., Crill, Patrick M., Saleska, Scott R., Rich, Virginia I., & Tyson, Gene W. Genome-centric view of carbon processing in thawing permafrost. United States. https://doi.org/10.1038/s41586-018-0338-1
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Woodcroft, Ben J., Singleton, Caitlin M., Boyd, Joel A., Evans, Paul N., Emerson, Joanne B., Zayed, Ahmed A. F., Hoelzle, Robert D., Lamberton, Timothy O., McCalley, Carmody K., Hodgkins, Suzanne B., Wilson, Rachel M., Purvine, Samuel O., Nicora, Carrie D., Li, Changsheng, Frolking, Steve, Chanton, Jeffrey P., Crill, Patrick M., Saleska, Scott R., Rich, Virginia I., and Tyson, Gene W. Mon . "Genome-centric view of carbon processing in thawing permafrost". United States. https://doi.org/10.1038/s41586-018-0338-1. https://www.osti.gov/servlets/purl/1481643.
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@article{osti_1481643,
title = {Genome-centric view of carbon processing in thawing permafrost},
author = {Woodcroft, Ben J. and Singleton, Caitlin M. and Boyd, Joel A. and Evans, Paul N. and Emerson, Joanne B. and Zayed, Ahmed A. F. and Hoelzle, Robert D. and Lamberton, Timothy O. and McCalley, Carmody K. and Hodgkins, Suzanne B. and Wilson, Rachel M. and Purvine, Samuel O. and Nicora, Carrie D. and Li, Changsheng and Frolking, Steve and Chanton, Jeffrey P. and Crill, Patrick M. and Saleska, Scott R. and Rich, Virginia I. and Tyson, Gene W.},
abstractNote = {As global temperatures rise, large amounts of carbon sequestered in permafrost are becoming available for microbial degradation. Accurate prediction of carbon gas emissions from thawing permafrost is limited by our understanding of these microbial communities. Here we use metagenomic sequencing of 214 samples from a permafrost thaw gradient to recover 1,529 metagenome-assembled genomes, including many from phyla with poor genomic representation. These genomes reflect the diversity of this complex ecosystem, with genus-level representatives for more than sixty per cent of the community. Meta-omic analysis revealed key populations involved in the degradation of organic matter, including bacteria whose genomes encode a previously undescribed fungal pathway for xylose degradation. Microbial and geochemical data highlight lineages that correlate with the production of greenhouse gases and indicate novel syntrophic relationships. Lastly, our findings link changing biogeochemistry to specific microbial lineages involved in carbon processing, and provide key information for predicting the effects of climate change on permafrost systems.},
doi = {10.1038/s41586-018-0338-1},
journal = {Nature (London)},
number = 7716,
volume = 560,
place = {United States},
year = {Mon Jul 16 00:00:00 EDT 2018},
month = {Mon Jul 16 00:00:00 EDT 2018}
}
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https://doi.org/10.1038/s41586-018-0338-1
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    • Chang, Kuang-Yu; Riley, William J.; Crill, Patrick M.
    • The Cryosphere, Vol. 13, Issue 2
    • DOI: 10.5194/tc-13-647-2019

    Towards optimized viral metagenomes for double-stranded and single-stranded DNA viruses from challenging soils
    journal, January 2019

    Ontogenic succession of thermokarst thaw ponds is linked to dissolved organic matter quality and microbial degradation potential
    journal, January 2020

    • Peura, Sari; Wauthy, Maxime; Simone, Domenico
    • Limnology and Oceanography, Vol. 65, Issue S1
    • DOI: 10.1002/lno.11349

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

    The known and the unknown in soil microbial ecology
    journal, January 2019

    Scientists’ warning to humanity: microorganisms and climate change
    text, January 2019

    Niche differentiation is spatially and temporally regulated in the rhizosphere
    journal, January 2020

    Think global, act local: The small-scale environment mainly influences microbial community development and function in lake sediment
    text, January 2020

    • Orland, C.; Yakimovich, Km; Mykytczuk, Ncs
    • Apollo - University of Cambridge Repository
    • DOI: 10.17863/cam.44763

    Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments
    journal, February 2019

    Distinct Drivers of Core and Accessory Components of Soil Microbial Community Functional Diversity under Environmental Changes
    journal, October 2019

    The Signal and the Noise: Characteristics of Antisense RNA in Complex Microbial Communities
    journal, February 2020

    • Michaelsen, Thomas Yssing; Brandt, Jakob; Singleton, Caitlin Margaret
    • mSystems, Vol. 5, Issue 1
    • DOI: 10.1128/msystems.00587-19

    Consistent Metagenome-Derived Metrics Verify and Delineate Bacterial Species Boundaries
    journal, January 2020

    Genomic and in-situ Transcriptomic Characterization of the Candidate Phylum NPL-UPL2 From Highly Alkaline Highly Reducing Serpentinized Groundwater
    journal, December 2018

    • Suzuki, Shino; Nealson, Kenneth H.; Ishii, Shun’ichi
    • Frontiers in Microbiology, Vol. 9
    • DOI: 10.3389/fmicb.2018.03141

    Identification of Molecular Markers That Are Specific to the Class Thermoleophilia
    journal, May 2019

    Distinct Taxonomic and Functional Profiles of the Microbiome Associated With Different Soil Horizons of a Moist Tussock Tundra in Alaska
    journal, June 2019

    Contrasting Winter Versus Summer Microbial Communities and Metabolic Functions in a Permafrost Thaw Lake
    journal, July 2019

    Evolutionary Implications of Anoxygenic Phototrophy in the Bacterial Phylum Candidatus Eremiobacterota (WPS-2)
    journal, July 2019

    • Ward, Lewis M.; Cardona, Tanai; Holland-Moritz, Hannah
    • Frontiers in Microbiology, Vol. 10
    • DOI: 10.3389/fmicb.2019.01658

    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

    Microbial Community Structure and Methane Cycling Potential along a Thermokarst Pond-Peatland Continuum
    journal, October 2019

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