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Research Article

Stimulation of soil respiration by elevated CO2 is enhanced under nitrogen limitation in a decade-long grassland study

Qun Gao, Gangsheng Wang, Kai Xue, Yunfeng Yang, Jianping Xie, View ORCID ProfileHao Yu, Shijie Bai, Feifei Liu, Zhili He, View ORCID ProfileDaliang Ning, View ORCID ProfileSarah E. Hobbie, View ORCID ProfilePeter B. Reich, and View ORCID ProfileJizhong Zhou
PNAS December 29, 2020 117 (52) 33317-33324; first published December 14, 2020; https://doi.org/10.1073/pnas.2002780117
Qun Gao
aState Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, 100084 Beijing, China;
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Gangsheng Wang
bInstitute for Environmental Genomics, University of Oklahoma, Norman, OK 73019;
cDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019;
dSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK 73019;
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Kai Xue
bInstitute for Environmental Genomics, University of Oklahoma, Norman, OK 73019;
cDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019;
dSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK 73019;
eCollege of Resources and Environment, University of Chinese Academy of Sciences, 100190 Beijing, China;
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Yunfeng Yang
aState Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, 100084 Beijing, China;
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  • For correspondence: yangyf@tsinghua.edu.cn jzhou@ou.edu
Jianping Xie
bInstitute for Environmental Genomics, University of Oklahoma, Norman, OK 73019;
cDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019;
dSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK 73019;
fSchool of Minerals Processing and Bioengineering, Central South University, 410083 Changsha, Hunan, China;
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Hao Yu
bInstitute for Environmental Genomics, University of Oklahoma, Norman, OK 73019;
cDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019;
dSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK 73019;
gCollege of Environmental Science and Engineering, Liaoning Technical University, 123000 Fuxin, Liaoning, China;
hKey Laboratory of Environmental Biotechnology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, 100085 Beijing, China;
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  • ORCID record for Hao Yu
Shijie Bai
bInstitute for Environmental Genomics, University of Oklahoma, Norman, OK 73019;
cDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019;
dSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK 73019;
iDeep Sea Science Division, Institute of Deep Sea Science and Engineering, Chinese Academy of Sciences, 572000 Sanya, Hainan, China;
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Feifei Liu
bInstitute for Environmental Genomics, University of Oklahoma, Norman, OK 73019;
cDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019;
dSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK 73019;
jGuangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Institute of Microbiology, Guangdong Academy of Sciences, 510070 Guangzhou, Guangdong, China;
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Zhili He
bInstitute for Environmental Genomics, University of Oklahoma, Norman, OK 73019;
cDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019;
dSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK 73019;
kEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Sun Yat-Sen University, 510006 Guangzhou, Guangdong, China;
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Daliang Ning
bInstitute for Environmental Genomics, University of Oklahoma, Norman, OK 73019;
cDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019;
dSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK 73019;
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  • ORCID record for Daliang Ning
Sarah E. Hobbie
lDepartment of Ecology, Evolution and Behavior, University of Minnesota, St Paul, MN 55108;
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Peter B. Reich
mDepartment of Forest Resources, University of Minnesota, St Paul, MN 55108;
nHawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW 2753, Australia;
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Jizhong Zhou
aState Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, 100084 Beijing, China;
bInstitute for Environmental Genomics, University of Oklahoma, Norman, OK 73019;
cDepartment of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019;
dSchool of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK 73019;
oEarth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA 94720
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  • ORCID record for Jizhong Zhou
  • For correspondence: yangyf@tsinghua.edu.cn jzhou@ou.edu
  1. Edited by David M. Karl, University of Hawaii at Manoa, Honolulu, HI, and approved October 27, 2020 (received for review February 17, 2020)

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Significance

The magnitude of CO2 efflux from soils (resulting from autotrophic and heterotrophic respiration) is one of the largest uncertainties in projecting future carbon–climate feedbacks. Despite research over several decades, the magnitude, direction, and duration of such feedbacks and their underlying microbial mechanisms are poorly understood, especially in the context of potentially interacting global environmental changes. In a decade-long experiment examining the interactive effects of CO2 and N enrichment, N limitation strengthened the stimulatory effects of elevated CO2 on soil respiration, primarily via N mining during the decomposition of more recalcitrant organic compounds. This study also provides a strategy for integrating genomics information into ecosystem and Earth system models to improve carbon-cycle predictions.

Abstract

Whether and how CO2 and nitrogen (N) availability interact to influence carbon (C) cycling processes such as soil respiration remains a question of considerable uncertainty in projecting future C–climate feedbacks, which are strongly influenced by multiple global change drivers, including elevated atmospheric CO2 concentrations (eCO2) and increased N deposition. However, because decades of research on the responses of ecosystems to eCO2 and N enrichment have been done largely independently, their interactive effects on soil respiratory CO2 efflux remain unresolved. Here, we show that in a multifactor free-air CO2 enrichment experiment, BioCON (Biodiversity, CO2, and N deposition) in Minnesota, the positive response of soil respiration to eCO2 gradually strengthened at ambient (low) N supply but not enriched (high) N supply for the 12-y experimental period from 1998 to 2009. In contrast to earlier years, eCO2 stimulated soil respiration twice as much at low than at high N supply from 2006 to 2009. In parallel, microbial C degradation genes were significantly boosted by eCO2 at low but not high N supply. Incorporating those functional genes into a coupled C–N ecosystem model reduced model parameter uncertainty and improved the projections of the effects of different CO2 and N levels on soil respiration. If our observed results generalize to other ecosystems, they imply widely positive effects of eCO2 on soil respiration even in infertile systems.

  • elevated CO2
  • nitrogen deposition
  • soil respiration
  • metagenomics
  • Earth ecosystem model

Footnotes

  • ↵1Q.G. and G.W. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: yangyf{at}tsinghua.edu.cn or jzhou{at}ou.edu.
  • Author contributions: Y.Y., S.E.H., P.B.R., and J.Z. designed research; Q.G., K.X., Y.Y., J.X., H.Y., S.B., F.L., Z.H., S.E.H., P.B.R., and J.Z. performed research; G.W. contributed new reagents/analytic tools; Q.G., G.W., and D.N. analyzed data; and Q.G., G.W., Y.Y., S.E.H., P.B.R., and J.Z. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2002780117/-/DCSupplemental.

Data Availability.

Genomic microarray data have been deposited in Gene Expression Omnibus (accession no. GSE98512).

Published under the PNAS license.

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Stimulation of soil respiration by elevated CO2 is enhanced under nitrogen limitation in a decade-long grassland study
Qun Gao, Gangsheng Wang, Kai Xue, Yunfeng Yang, Jianping Xie, Hao Yu, Shijie Bai, Feifei Liu, Zhili He, Daliang Ning, Sarah E. Hobbie, Peter B. Reich, Jizhong Zhou
Proceedings of the National Academy of Sciences Dec 2020, 117 (52) 33317-33324; DOI: 10.1073/pnas.2002780117

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Stimulation of soil respiration by elevated CO2 is enhanced under nitrogen limitation in a decade-long grassland study
Qun Gao, Gangsheng Wang, Kai Xue, Yunfeng Yang, Jianping Xie, Hao Yu, Shijie Bai, Feifei Liu, Zhili He, Daliang Ning, Sarah E. Hobbie, Peter B. Reich, Jizhong Zhou
Proceedings of the National Academy of Sciences Dec 2020, 117 (52) 33317-33324; DOI: 10.1073/pnas.2002780117
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