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

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Abstract

Greenhouse gas (GHG) emissions from thawed permafrost are difficult to predict because they result from complex interactions between abiotic drivers and multiple, often competing, microbial metabolic processes. Our objective was to characterize mechanisms controlling methane (CH4) and carbon dioxide (CO2) production from permafrost. We simulated permafrost thaw for the length of one growing season (90 days) in oxic and anoxic treatments at 1 and 15 °C to stimulate aerobic and anaerobic respiration. We measured headspace CH4 and CO2 concentrations, as well as soil chemical and biological parameters (e.g. dissolved organic carbon (DOC) chemistry, microbial enzyme activity, N2O production, bacterial community structure), and applied an information theoretic approach and the Akaike information criterion to find the best explanation for mechanisms controlling GHG flux. In addition to temperature and redox status, CH4 production was explained by the relative abundance of methanogens, activity of non-methanogenic anaerobes, and substrate chemistry. Carbon dioxide production was explained by microbial community structure and chemistry of the DOC pool. We suggest that models of permafrost CO2 production are refined by a holistic view of the system, where the prokaryote community structure and detailed chemistry are considered. In contrast, although CH4 production is the result of many syntrophic interactions, these actions can be aggregated into a linear approach, where there is a single path of organic matter degradation and multiple conditions must be satisfied in order for methanogenesis to occur. This concept advances our mechanistic understanding of the processes governing anaerobic GHG flux, which is critical to understanding the impact the release of permafrost C will have on the global C cycle.

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Abbreviations

GHG:

Greenhouse gas

CH4 :

Methane

CO2 :

Carbon dioxide

DOC:

Dissolved organic carbon

IT:

Information theoretic

AICc:

Akaike information criterion

C:

Carbon

ESM:

Earth systems models

FTIR:

Fourier transformed mid-infrared spectroscopy

PCoA:

Principle coordinates analysis

ANOSIM:

Analysis of similarity

PCA:

Principle components analysis

MBC:

Microbial biomass carbon

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Acknowledgements

Jessica Ernakovich was funded by generous support from the National Science Foundation (Graduate Research Fellowship Program and Doctoral Dissertation Improvement Grant) and the Department of Energy Global Change Education Program Fellowship. Matthew Wallenstein was supported by Award Number 0902030 from the National Science Foundation Office of Polar Programs and an NSF CAREER Award (#1255228). This material is also based upon work supported by the U.S. Department of Energy, Office of Science, Office of Terrestrial Ecosystem Science, Award Number DE-SC0010568. Many thanks to Rachel Paige and Claire Freeman for assistance with laboratory measures, and to Guy Beresford for the preparation of molecular libraries. Early discussions with J. Megan Steinweg, Sarah Evans and Joe vonFisher had a significant impact on the direction of this work. We would also like to thank the three anonymous reviewers and the editor for the time taken during review, as their comments significantly improved the manuscript.

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The use of trade, firm, or corporation names is for the information and convenience of the reader. Such use does not constitute an official endorsement or approval by the United States Department of Agriculture or the Agricultural Research Service of any product or service to the exclusion of others that may be suitable. The U.S. Department of Agriculture (USDA) prohibits discrimination in all its programs and activities on the basis of race, color, national origin, age, disability, and where applicable, sex, marital status, familial status, parental status, religion, sexual orientation, genetic information, political beliefs, reprisal, or because all or part of an individual’s income is derived from any public assistance program.

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Authors and Affiliations

  1. CSIRO Agriculture & Food, PMB 2 Waite Rd., Urrbrae, SA, 5064, Australia

    Jessica G. Ernakovich

  2. Natural Resource Ecology Laboratory, Colorado State University, 1499 Campus Delivery, Fort Collins, CO, 80523, USA

    Jessica G. Ernakovich, Laurel M. Lynch, Francisco J. Calderon & Matthew D. Wallenstein

  3. Graduate Degree Program in Ecology, 1036 Campus Delivery Colorado State University, Fort Collins, CO, 80523, USA

    Laurel M. Lynch

  4. Smithsonian Environmental Research Center, 647 Contees Wharf Rd, Edgewater, MD, 21037, USA

    Paul E. Brewer

  5. USDA-ARS, Central Great Plains Research Station, 40335 Co Rd GG, Akron, CO, 80720, USA

    Francisco J. Calderon

  6. Department of Ecosystem Science and Sustainability, Colorado State University, 1499 Campus Delivery, Fort Collins, CO, 80523, USA

    Matthew D. Wallenstein

Authors
  1. Jessica G. Ernakovich
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  2. Laurel M. Lynch
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  3. Paul E. Brewer
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  4. Francisco J. Calderon
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  5. Matthew D. Wallenstein
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Corresponding author

Correspondence to Jessica G. Ernakovich.

Additional information

Responsible Editor: E. Matzner.

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Ernakovich, J.G., Lynch, L.M., Brewer, P.E. et al. Redox and temperature-sensitive changes in microbial communities and soil chemistry dictate greenhouse gas loss from thawed permafrost. Biogeochemistry 134, 183–200 (2017). https://doi.org/10.1007/s10533-017-0354-5

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  • DOI: https://doi.org/10.1007/s10533-017-0354-5

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