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Title: Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming

Abstract

Microbial decomposition of soil carbon in high-latitude tundra underlain with permafrost is one of the most important, but poorly understood, potential positive feedbacks of greenhouse gas emissions from terrestrial ecosystems into the atmosphere in a warmer world. Using integrated metagenomic technologies, we showed that the microbial functional community structure in the active layer of tundra soil was significantly altered after only 1.5 years of warming, a rapid response demonstrating the high sensitivity of this ecosystem to warming. The abundances of microbial functional genes involved in both aerobic and anaerobic carbon decomposition were also markedly increased by this short-term warming. Consistent with this, ecosystem respiration (Reco) increased up to 38%. In addition, warming enhanced genes involved in nutrient cycling, which very likely contributed to an observed increase (30%) in gross primary productivity (GPP). However, the GPP increase did not offset the extra Reco, resulting in significantly more net carbon loss in warmed plots compared with control plots. Altogether, our results demonstrate the vulnerability of active-layer soil carbon in this permafrost-based tundra ecosystem to climate warming and the importance of microbial communities in mediating such vulnerability.

Authors:
 [1];  [2];  [2];  [2]; ORCiD logo [3];  [4];  [2];  [2]; ORCiD logo [2];  [5];  [6];  [7];  [8];  [8];  [9];  [9];  [9];  [10];  [11]
  1. Tsinghua Univ., Beijing (China). State Key Joint Lab. of Environment Simulation and Pollution Control; Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics
  2. Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics
  3. Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics; Chinese Academy of Sciences (CAS), Beijing (China). Research Center for Eco-Environmental Sciences
  4. Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics; Zhejiang Univ., Hangzhou (China). College of Life Sciences
  5. Univ. of Florida, Gainesville, FL (United States)
  6. Woods Hole Research Center, Falmouth, MA (United States)
  7. Univ. of Florida, Gainesville, FL (United States); Northern Arizona Univ., Flagstaff, AZ (United States). Center for Ecosystem Sciences and Society
  8. Georgia Inst. of Technology, Atlanta, GA (United States)
  9. Michigan State Univ., East Lansing, MI (United States). Center for Microbial Ecology
  10. Univ. of Oklahoma, Norman, OK (United States)
  11. Tsinghua Univ., Beijing (China). State Key Joint Lab. of Environment Simulation and Pollution Control; Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1574316
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Climate Change
Additional Journal Information:
Journal Volume: 6; Journal Issue: 6; Journal ID: ISSN 1758-678X
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES

Citation Formats

Xue, Kai, M. Yuan, Mengting, J. Shi, Zhou, Qin, Yujia, Deng, Ye, Cheng, Lei, Wu, Liyou, He, Zhili, Van Nostrand, Joy D., Bracho, Rosvel, Natali, Susan, Schuur, Edward. A. G., Luo, Chengwei, Konstantinidis, Konstantinos T., Wang, Qiong, Cole, James  R., Tiedje, James  M., Luo, Yiqi, and Zhou, Jizhong. Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming. United States: N. p., 2016. Web. doi:10.1038/nclimate2940.
Xue, Kai, M. Yuan, Mengting, J. Shi, Zhou, Qin, Yujia, Deng, Ye, Cheng, Lei, Wu, Liyou, He, Zhili, Van Nostrand, Joy D., Bracho, Rosvel, Natali, Susan, Schuur, Edward. A. G., Luo, Chengwei, Konstantinidis, Konstantinos T., Wang, Qiong, Cole, James  R., Tiedje, James  M., Luo, Yiqi, & Zhou, Jizhong. Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming. United States. https://doi.org/10.1038/nclimate2940
Xue, Kai, M. Yuan, Mengting, J. Shi, Zhou, Qin, Yujia, Deng, Ye, Cheng, Lei, Wu, Liyou, He, Zhili, Van Nostrand, Joy D., Bracho, Rosvel, Natali, Susan, Schuur, Edward. A. G., Luo, Chengwei, Konstantinidis, Konstantinos T., Wang, Qiong, Cole, James  R., Tiedje, James  M., Luo, Yiqi, and Zhou, Jizhong. Mon . "Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming". United States. https://doi.org/10.1038/nclimate2940. https://www.osti.gov/servlets/purl/1574316.
@article{osti_1574316,
title = {Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming},
author = {Xue, Kai and M. Yuan, Mengting and J. Shi, Zhou and Qin, Yujia and Deng, Ye and Cheng, Lei and Wu, Liyou and He, Zhili and Van Nostrand, Joy D. and Bracho, Rosvel and Natali, Susan and Schuur, Edward. A. G. and Luo, Chengwei and Konstantinidis, Konstantinos T. and Wang, Qiong and Cole, James  R. and Tiedje, James  M. and Luo, Yiqi and Zhou, Jizhong},
abstractNote = {Microbial decomposition of soil carbon in high-latitude tundra underlain with permafrost is one of the most important, but poorly understood, potential positive feedbacks of greenhouse gas emissions from terrestrial ecosystems into the atmosphere in a warmer world. Using integrated metagenomic technologies, we showed that the microbial functional community structure in the active layer of tundra soil was significantly altered after only 1.5 years of warming, a rapid response demonstrating the high sensitivity of this ecosystem to warming. The abundances of microbial functional genes involved in both aerobic and anaerobic carbon decomposition were also markedly increased by this short-term warming. Consistent with this, ecosystem respiration (Reco) increased up to 38%. In addition, warming enhanced genes involved in nutrient cycling, which very likely contributed to an observed increase (30%) in gross primary productivity (GPP). However, the GPP increase did not offset the extra Reco, resulting in significantly more net carbon loss in warmed plots compared with control plots. Altogether, our results demonstrate the vulnerability of active-layer soil carbon in this permafrost-based tundra ecosystem to climate warming and the importance of microbial communities in mediating such vulnerability.},
doi = {10.1038/nclimate2940},
journal = {Nature Climate Change},
number = 6,
volume = 6,
place = {United States},
year = {Mon Feb 22 00:00:00 EST 2016},
month = {Mon Feb 22 00:00:00 EST 2016}
}

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  • Biogeosciences Discussions
  • DOI: 10.5194/bg-2016-234

Massive remobilization of permafrost carbon during post-glacial warming
text, January 2016

  • Tesi, T.; Muschitiello, Francesco; Smittenberg, R. H.
  • Columbia University
  • DOI: 10.7916/d8gq6z65

Broad‐leaved forest types affect soil fungal community structure and soil organic carbon contents
journal, June 2019

  • Sheng, Yuyu; Cong, Jing; Lu, Hui
  • MicrobiologyOpen, Vol. 8, Issue 10
  • DOI: 10.1002/mbo3.874

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


Warming-induced permafrost thaw exacerbates tundra soil carbon decomposition mediated by microbial community
journal, January 2020


Identification of the Core Set of Carbon-Associated Genes in a Bioenergy Grassland Soil
journal, November 2016


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

Microbial Community and Functional Gene Changes in Arctic Tundra Soils in a Microcosm Warming Experiment
journal, September 2017


Taxonomic and Functional Responses of Soil Microbial Communities to Annual Removal of Aboveground Plant Biomass
journal, May 2018