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

Eric R. Johnston, Janet K. Hatt, Zhili He, Liyou Wu, Xue Guo, Yiqi Luo, Edward A. G. Schuur, James M. Tiedje, Jizhong Zhou, and Konstantinos T. Konstantinidis
PNAS July 23, 2019 116 (30) 15096-15105; first published July 8, 2019 https://doi.org/10.1073/pnas.1901307116

  1. Edited by Edward F. DeLong, University of Hawaii at Mānoa, Honolulu, HI, and approved June 10, 2019 (received for review January 23, 2019)

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Significance

Ongoing permafrost thaw is expected to stimulate microbial release of greenhouse gases, threatening to further exacerbate climate change (cause positive feedback). In this study, a unique field warming experiment was conducted in Interior Alaska to promote surface permafrost degradation while maintaining uniform hydraulic conditions. After 5 winters of experimental warming by ∼1 °C, microbial community shifts were observed at the receded permafrost/active layer boundary, which reflected more reduced conditions, including increased methanogenesis. In contrast, increased carbohydrate utilization (respiration) was observed at the surface layer. These shifts were relatable to observed increases in CO2 and CH4 release from this study site and the surrounding ecosystem. Collectively, our results demonstrate that microbial responses to warming are rapid and identify potential biomarkers that could be important in modeling.

Abstract

Northern-latitude tundra soils harbor substantial carbon (C) stocks that are highly susceptible to microbial degradation with rising global temperatures. Understanding the magnitude and direction (e.g., C release or sequestration) of the microbial responses to warming is necessary to accurately model climate change. In this study, Alaskan tundra soils were subjected to experimental in situ warming by ∼1.1 °C above ambient temperature, and the microbial communities were evaluated using metagenomics after 4.5 years, at 2 depths: 15 to 25 cm (active layer at outset of the experiment) and 45 to 55 cm (transition zone at the permafrost/active layer boundary at the outset of the experiment). In contrast to small or insignificant shifts after 1.5 years of warming, 4.5 years of warming resulted in significant changes to the abundances of functional traits and the corresponding taxa relative to control plots (no warming), and microbial shifts differed qualitatively between the two soil depths. At 15 to 25 cm, increased abundances of carbohydrate utilization genes were observed that correlated with (increased) measured ecosystem carbon respiration. At the 45- to 55-cm layer, increased methanogenesis potential was observed, which corresponded with a 3-fold increase in abundance of a single archaeal clade of the Methanosarcinales order, increased annual thaw duration (45.3 vs. 79.3 days), and increased CH4 emissions. Collectively, these data demonstrate that the microbial responses to warming in tundra soil are rapid and markedly different between the 2 critical soil layers evaluated, and identify potential biomarkers for the corresponding microbial processes that could be important in modeling.

Footnotes

  • ↵1To whom correspondence may be addressed. Email: kostas{at}ce.gatech.edu.

  • Author contributions: E.R.J., Z.H., L.W., Y.L., E.A.G.S., J.M.T., J.Z., and K.T.K. designed research; E.R.J., J.K.H., and X.G. performed research; E.R.J. analyzed data; and E.R.J. and K.T.K. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: Metagenome and MAG sequences have been deposited in the European Nucleotide Archive (study ID PRJEB31848). Individual accession IDs for metagenomes and metagenome-assembled genomes can be found in SI Appendix, Tables S1 and S5, respectively.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1901307116/-/DCSupplemental.

Published under the PNAS license.

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Responses of tundra soil microbial communities to half a decade of experimental warming at two critical depths
Eric R. Johnston, Janet K. Hatt, Zhili He, Liyou Wu, Xue Guo, Yiqi Luo, Edward A. G. Schuur, James M. Tiedje, Jizhong Zhou, Konstantinos T. Konstantinidis
Proceedings of the National Academy of Sciences Jul 2019, 116 (30) 15096-15105; DOI: 10.1073/pnas.1901307116
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