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Research Article | Applied and Environmental Science

Long-Term Warming in Alaska Enlarges the Diazotrophic Community in Deep Soils

Jiajie Feng, C. Ryan Penton, Zhili He, Joy D. Van Nostrand, Mengting M. Yuan, Liyou Wu, Cong Wang, Yujia Qin, Zhou J. Shi, Xue Guo, Edward A. G. Schuur, Yiqi Luo, Rosvel Bracho, Konstantinos T. Konstantinidis, James R. Cole, James M. Tiedje, Yunfeng Yang, Jizhong Zhou
Paul Keim, Editor
Jiajie Feng
aInstitute for Environmental Genomics, University of Oklahoma, Norman, Oklahoma, USA
bDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA
cSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, Oklahoma, USA
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C. Ryan Penton
dCollege of Integrative Sciences and Arts, Arizona State University, Mesa, Arizona, USA
eCenter for Fundamental and Applied Microbiomics, The Biodesign Institute, Arizona State University, Tempe, Arizona, USA
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Zhili He
aInstitute for Environmental Genomics, University of Oklahoma, Norman, Oklahoma, USA
bDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA
cSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, Oklahoma, USA
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Joy D. Van Nostrand
aInstitute for Environmental Genomics, University of Oklahoma, Norman, Oklahoma, USA
bDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA
cSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, Oklahoma, USA
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Mengting M. Yuan
aInstitute for Environmental Genomics, University of Oklahoma, Norman, Oklahoma, USA
bDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA
cSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, Oklahoma, USA
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Liyou Wu
aInstitute for Environmental Genomics, University of Oklahoma, Norman, Oklahoma, USA
bDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA
cSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, Oklahoma, USA
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Cong Wang
aInstitute for Environmental Genomics, University of Oklahoma, Norman, Oklahoma, USA
bDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA
cSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, Oklahoma, USA
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Yujia Qin
aInstitute for Environmental Genomics, University of Oklahoma, Norman, Oklahoma, USA
bDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA
cSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, Oklahoma, USA
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Zhou J. Shi
aInstitute for Environmental Genomics, University of Oklahoma, Norman, Oklahoma, USA
bDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA
cSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, Oklahoma, USA
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Xue Guo
fState Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, China
aInstitute for Environmental Genomics, University of Oklahoma, Norman, Oklahoma, USA
bDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA
cSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, Oklahoma, USA
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Edward A. G. Schuur
gCenter for Ecosystem Science and Society, Northern Arizona University, Flagstaff, Arizona, USA
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Yiqi Luo
gCenter for Ecosystem Science and Society, Northern Arizona University, Flagstaff, Arizona, USA
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Rosvel Bracho
hSchool of Forest Resources and Conservation, Department of Biology, University of Florida, Gainesville, Florida, USA
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Konstantinos T. Konstantinidis
iSchool of Civil and Environmental Engineering, Georgia Institute of Technology, Atlanta, Georgia, USA
lSchool of Biology, Center for Bioinformatics and Computational Genomics, Georgia Institute of Technology, Atlanta, Georgia, USA
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James R. Cole
jCenter for Microbial Ecology, Michigan State University, East Lansing, Michigan, USA
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James M. Tiedje
jCenter for Microbial Ecology, Michigan State University, East Lansing, Michigan, USA
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Yunfeng Yang
fState Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, China
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Jizhong Zhou
aInstitute for Environmental Genomics, University of Oklahoma, Norman, Oklahoma, USA
bDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA
cSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, Oklahoma, USA
fState Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, China
kEarth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, California, USA
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Paul Keim
Northern Arizona University
Roles: Editor
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DOI: 10.1128/mBio.02521-18
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ABSTRACT

Tundra ecosystems are typically carbon (C) rich but nitrogen (N) limited. Since biological N2 fixation is the major source of biologically available N, the soil N2-fixing (i.e., diazotrophic) community serves as an essential N supplier to the tundra ecosystem. Recent climate warming has induced deeper permafrost thaw and adversely affected C sequestration, which is modulated by N availability. Therefore, it is crucial to examine the responses of diazotrophic communities to warming across the depths of tundra soils. Herein, we carried out one of the deepest sequencing efforts of nitrogenase gene (nifH) to investigate how 5 years of experimental winter warming affects Alaskan soil diazotrophic community composition and abundance spanning both the organic and mineral layers. Although soil depth had a stronger influence on diazotrophic community composition than warming, warming significantly (P < 0.05) enhanced diazotrophic abundance by 86.3% and aboveground plant biomass by 25.2%. Diazotrophic composition in the middle and lower organic layers, detected by nifH sequencing and a microarray-based tool (GeoChip), was markedly altered, with an increase of α-diversity. Changes in diazotrophic abundance and composition significantly correlated with soil moisture, soil thaw duration, and plant biomass, as shown by structural equation modeling analyses. Therefore, more abundant diazotrophic communities induced by warming may potentially serve as an important mechanism for supplementing biologically available N in this tundra ecosystem.

IMPORTANCE With the likelihood that changes in global climate will adversely affect the soil C reservoir in the northern circumpolar permafrost zone, an understanding of the potential role of diazotrophic communities in enhancing biological N2 fixation, which constrains both plant production and microbial decomposition in tundra soils, is important in elucidating the responses of soil microbial communities to global climate change. A recent study showed that the composition of the diazotrophic community in a tundra soil exhibited no change under a short-term (1.5-year) winter warming experiment. However, it remains crucial to examine whether the lack of diazotrophic community responses to warming is persistent over a longer time period as a possibly important mechanism in stabilizing tundra soil C. Through a detailed characterization of the effects of winter warming on diazotrophic communities, we showed that a long-term (5-year) winter warming substantially enhanced diazotrophic abundance and altered community composition, though soil depth had a stronger influence on diazotrophic community composition than warming. These changes were best explained by changes in soil moisture, soil thaw duration, and plant biomass. These results provide crucial insights into the potential factors that may impact future C and N availability in tundra regions.

  • Copyright © 2019 Feng et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Long-Term Warming in Alaska Enlarges the Diazotrophic Community in Deep Soils
Jiajie Feng, C. Ryan Penton, Zhili He, Joy D. Van Nostrand, Mengting M. Yuan, Liyou Wu, Cong Wang, Yujia Qin, Zhou J. Shi, Xue Guo, Edward A. G. Schuur, Yiqi Luo, Rosvel Bracho, Konstantinos T. Konstantinidis, James R. Cole, James M. Tiedje, Yunfeng Yang, Jizhong Zhou
mBio Feb 2019, 10 (1) e02521-18; DOI: 10.1128/mBio.02521-18

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Long-Term Warming in Alaska Enlarges the Diazotrophic Community in Deep Soils
Jiajie Feng, C. Ryan Penton, Zhili He, Joy D. Van Nostrand, Mengting M. Yuan, Liyou Wu, Cong Wang, Yujia Qin, Zhou J. Shi, Xue Guo, Edward A. G. Schuur, Yiqi Luo, Rosvel Bracho, Konstantinos T. Konstantinidis, James R. Cole, James M. Tiedje, Yunfeng Yang, Jizhong Zhou
mBio Feb 2019, 10 (1) e02521-18; DOI: 10.1128/mBio.02521-18
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KEYWORDS

climate warming
diazotrophs
gene sequencing
soil microbiology
tundra

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