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Title: Microbial functional genes commonly respond to elevated carbon dioxide

Abstract

Atmospheric CO2 concentration is increasing, largely due to anthropogenic activities. Previous studies of individual free-air CO2 enrichment (FACE) experimental sites have shown significant impacts of elevated CO2 (eCO2) on soil microbial communities; however, no common microbial response patterns have yet emerged, challenging our ability to predict ecosystem functioning and sustainability in the future eCO2 environment. Here we analyzed 66 soil microbial communities from five FACE sites, and showed common microbial response patterns to eCO2, especially for key functional genes involved in carbon and nitrogen fixation (e.g., pcc/acc for carbon fixation, nifH for nitrogen fixation), carbon decomposition (e.g., amyA and pulA for labile carbon decomposition, mnp and lcc for recalcitrant carbon decomposition), and greenhouse gas emissions (e.g., mcrA for methane production, norB for nitrous oxide production) across five FACE sites. Also, the relative abundance of those key genes was generally increased and directionally associated with increased biomass, soil carbon decomposition, and soil moisture. In addition, a further literature survey of more disparate FACE experimental sites indicated increased biomass, soil carbon decay, nitrogen fixation, methane and nitrous oxide emissions, plant and soil carbon and nitrogen under eCO2. A conceptual framework was developed to link commonly responsive functional genes with ecosystem processes, suchmore » as pcc/acc vs. soil carbon storage, amyA/pulA/mnp/lcc vs. soil carbon decomposition, and nifH vs. nitrogen availability, suggesting that such common responses of microbial functional genes may have the potential to predict ecosystem functioning and sustainability in the future eCO2 environment.« less

Authors:
ORCiD logo [1];  [2];  [3];  [4];  [5];  [6];  [7]; ORCiD logo [8];  [5];  [5];  [9];  [10];  [5];  [11]; ORCiD logo [12]; ORCiD logo [13];  [14];  [10];  [15];  [16] more »;  [17];  [18] « less
  1. Sun Yat-Sen Univ., Guangzhou (China). Southern Marine Science and Engineering Guangdong Lab. (Zhuhai); Univ. of Oklahoma, Norman, OK (United States); Hunan Agricultural Univ., Changsha (China)
  2. Univ. of Oklahoma, Norman, OK (United States); Chinese Academy of Sciences (CAS), Beijing (China). Research Center for Eco-Environmental Sciences
  3. Univ. of Oklahoma, Norman, OK (United States); Guangdong Inst. of Microbiology, Guangzhou (China)
  4. Univ. of Oklahoma, Norman, OK (United States); Hunan Agricultural Univ., Changsha (China)
  5. Univ. of Oklahoma, Norman, OK (United States)
  6. Univ. of Oklahoma, Norman, OK (United States); Ningbo Univ. (China)
  7. Univ. of Oklahoma, Norman, OK (United States); Harbin Inst. of Technology (China); Liaoning Technical Univ., Fuxin (China)
  8. Sun Yat-Sen Univ., Guangzhou (China). Southern Marine Science and Engineering Guangdong Lab. (Zhuhai); Univ. of Oklahoma, Norman, OK (United States);
  9. Univ. of Oklahoma, Norman, OK (United States); Univ. of California, Berkeley, CA (United States)
  10. Univ. of Western Sydney, NSW (Australia); Univ. of Wyoming, Laramie, WY (United States)
  11. Univ. of Minnesota, St. Paul, MN (United States)
  12. Univ. of Western Sydney, NSW (Australia); Univ. of St. Paul, Minneapolis, MN (United States)
  13. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  14. Univ. of Illinois at Urbana-Champaign, IL (United States)
  15. Colorado State Univ., Fort Collins, CO (United States). Natural Resource Ecology Lab.
  16. Hunan Agricultural Univ., Changsha (China)
  17. Sun Yat-Sen Univ., Guangzhou (China). Southern Marine Science and Engineering Guangdong Lab. (Zhuhai); Univ. of Oklahoma, Norman, OK (United States)
  18. Univ. of Oklahoma, Norman, OK (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Tsinghua Univ., Beijing (China). State Key Joint Lab. of Environment Simulation and Pollution Control
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); US Dept. of Agriculture (USDA); National Science Foundation (NSF)
OSTI Identifier:
1764543
Alternate Identifier(s):
OSTI ID: 1820786
Grant/Contract Number:  
AC02-05CH11231; FG02-96ER62291; FC02-06ER64158; AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Environment International
Additional Journal Information:
Journal Volume: 144; Journal ID: ISSN 0160-4120
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Soil microbial community; functional gene; common/specific response; elevated carbon dioxide; global change

Citation Formats

He, Zhili, Deng, Ye, Xu, Meiying, Li, Juan, Liang, Junyi, Xiong, Jinbo, Yu, Hao, Wu, Bo, Wu, Liyou, Xue, Kai, Shi, Shengjing, Carrillo, Yolima, Van Nostrand, Joy D., Hobbie, Sarah E., Reich, Peter B., Schadt, Christopher W., Kent, Angela D., Pendall, Elise, Wallenstein, Matthew, Luo, Yiqi, Yan, Qingyun, and Zhou, Jizhong. Microbial functional genes commonly respond to elevated carbon dioxide. United States: N. p., 2020. Web. doi:10.1016/j.envint.2020.106068.
He, Zhili, Deng, Ye, Xu, Meiying, Li, Juan, Liang, Junyi, Xiong, Jinbo, Yu, Hao, Wu, Bo, Wu, Liyou, Xue, Kai, Shi, Shengjing, Carrillo, Yolima, Van Nostrand, Joy D., Hobbie, Sarah E., Reich, Peter B., Schadt, Christopher W., Kent, Angela D., Pendall, Elise, Wallenstein, Matthew, Luo, Yiqi, Yan, Qingyun, & Zhou, Jizhong. Microbial functional genes commonly respond to elevated carbon dioxide. United States. https://doi.org/10.1016/j.envint.2020.106068
He, Zhili, Deng, Ye, Xu, Meiying, Li, Juan, Liang, Junyi, Xiong, Jinbo, Yu, Hao, Wu, Bo, Wu, Liyou, Xue, Kai, Shi, Shengjing, Carrillo, Yolima, Van Nostrand, Joy D., Hobbie, Sarah E., Reich, Peter B., Schadt, Christopher W., Kent, Angela D., Pendall, Elise, Wallenstein, Matthew, Luo, Yiqi, Yan, Qingyun, and Zhou, Jizhong. Sat . "Microbial functional genes commonly respond to elevated carbon dioxide". United States. https://doi.org/10.1016/j.envint.2020.106068. https://www.osti.gov/servlets/purl/1764543.
@article{osti_1764543,
title = {Microbial functional genes commonly respond to elevated carbon dioxide},
author = {He, Zhili and Deng, Ye and Xu, Meiying and Li, Juan and Liang, Junyi and Xiong, Jinbo and Yu, Hao and Wu, Bo and Wu, Liyou and Xue, Kai and Shi, Shengjing and Carrillo, Yolima and Van Nostrand, Joy D. and Hobbie, Sarah E. and Reich, Peter B. and Schadt, Christopher W. and Kent, Angela D. and Pendall, Elise and Wallenstein, Matthew and Luo, Yiqi and Yan, Qingyun and Zhou, Jizhong},
abstractNote = {Atmospheric CO2 concentration is increasing, largely due to anthropogenic activities. Previous studies of individual free-air CO2 enrichment (FACE) experimental sites have shown significant impacts of elevated CO2 (eCO2) on soil microbial communities; however, no common microbial response patterns have yet emerged, challenging our ability to predict ecosystem functioning and sustainability in the future eCO2 environment. Here we analyzed 66 soil microbial communities from five FACE sites, and showed common microbial response patterns to eCO2, especially for key functional genes involved in carbon and nitrogen fixation (e.g., pcc/acc for carbon fixation, nifH for nitrogen fixation), carbon decomposition (e.g., amyA and pulA for labile carbon decomposition, mnp and lcc for recalcitrant carbon decomposition), and greenhouse gas emissions (e.g., mcrA for methane production, norB for nitrous oxide production) across five FACE sites. Also, the relative abundance of those key genes was generally increased and directionally associated with increased biomass, soil carbon decomposition, and soil moisture. In addition, a further literature survey of more disparate FACE experimental sites indicated increased biomass, soil carbon decay, nitrogen fixation, methane and nitrous oxide emissions, plant and soil carbon and nitrogen under eCO2. A conceptual framework was developed to link commonly responsive functional genes with ecosystem processes, such as pcc/acc vs. soil carbon storage, amyA/pulA/mnp/lcc vs. soil carbon decomposition, and nifH vs. nitrogen availability, suggesting that such common responses of microbial functional genes may have the potential to predict ecosystem functioning and sustainability in the future eCO2 environment.},
doi = {10.1016/j.envint.2020.106068},
journal = {Environment International},
number = ,
volume = 144,
place = {United States},
year = {Sat Aug 29 00:00:00 EDT 2020},
month = {Sat Aug 29 00:00:00 EDT 2020}
}

Works referenced in this record:

PROGRESSIVE NITROGEN LIMITATION OF ECOSYSTEM PROCESSES UNDER ELEVATED CO 2 IN A WARM-TEMPERATE FOREST
journal, January 2006

  • Finzi, Adrien C.; Moore, David J. P.; DeLucia, Evan H.
  • Ecology, Vol. 87, Issue 1
  • DOI: 10.1890/04-1748

Impacts of 3 years of elevated atmospheric CO 2 on rhizosphere carbon flow and microbial community dynamics
journal, November 2012

  • Drigo, Barbara; Kowalchuk, George A.; Knapp, Brigitte A.
  • Global Change Biology, Vol. 19, Issue 2
  • DOI: 10.1111/gcb.12045

Elevated carbon dioxide accelerates the spatial turnover of soil microbial communities
journal, October 2015

  • Deng, Ye; He, Zhili; Xiong, Jinbo
  • Global Change Biology, Vol. 22, Issue 2
  • DOI: 10.1111/gcb.13098

Structural and functional diversity of soil microbes is affected by elevated [CO2] and N addition in a poplar plantation
journal, April 2007

  • Lagomarsino, Alessandra; Knapp, Brigitte A.; Moscatelli, M. Cristina
  • Journal of Soils and Sediments, Vol. 7, Issue 6
  • DOI: 10.1065/jss2007.04.223

Unexpected reversal of C 3 versus C 4 grass response to elevated CO 2 during a 20-year field experiment
journal, April 2018


DNA recovery from soils of diverse composition.
journal, January 1996


Decade-long soil nitrogen constraint on the CO2 fertilization of plant biomass
journal, September 2012

  • Reich, Peter B.; Hobbie, Sarah E.
  • Nature Climate Change, Vol. 3, Issue 3
  • DOI: 10.1038/nclimate1694

Increased soil emissions of potent greenhouse gases under increased atmospheric CO2
journal, July 2011

  • van Groenigen, Kees Jan; Osenberg, Craig W.; Hungate, Bruce A.
  • Nature, Vol. 475, Issue 7355
  • DOI: 10.1038/nature10176

Altered soil microbial community at elevated CO2 leads to loss of soil carbon
journal, March 2007

  • Carney, K. M.; Hungate, B. A.; Drake, B. G.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 12
  • DOI: 10.1073/pnas.0610045104

Elevated Carbon Dioxide Alters the Structure of Soil Microbial Communities
journal, February 2012

  • Deng, Ye; He, Zhili; Xu, Meiying
  • Applied and Environmental Microbiology, Vol. 78, Issue 8
  • DOI: 10.1128/AEM.06924-11

Elevated-CO2 Response of Stomata and Its Dependence on Environmental Factors
journal, May 2016


Microbial Functional Gene Diversity Predicts Groundwater Contamination and Ecosystem Functioning
journal, February 2018


Elevated CO2 shifts the functional structure and metabolic potentials of soil microbial communities in a C4 agroecosystem
journal, March 2015

  • Xiong, Jinbo; He, Zhili; Shi, Shengjing
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep09316

Empirical Evaluation of a New Method for Calculating Signal-to-Noise Ratio for Microarray Data Analysis
journal, March 2008

  • He, Z.; Zhou, J.
  • Applied and Environmental Microbiology, Vol. 74, Issue 10
  • DOI: 10.1128/AEM.02536-07

Elevated atmospheric carbon dioxide increases soil carbon
journal, December 2005


The phylogenetic composition and structure of soil microbial communities shifts in response to elevated carbon dioxide
journal, July 2011


Common bacterial responses in six ecosystems exposed to 10 years of elevated atmospheric carbon dioxide: Soil bacterial response in six ecosystems
journal, January 2012


Future carbon dioxide concentration decreases canopy evapotranspiration and soil water depletion by field-grown maize
journal, March 2013

  • Hussain, Mir Zaman; VanLoocke, Andy; Siebers, Matthew H.
  • Global Change Biology, Vol. 19, Issue 5
  • DOI: 10.1111/gcb.12155

Short-term responses and resistance of soil microbial community structure to elevated CO2 and N addition in grassland mesocosms
journal, April 2017

  • Simonin, Marie; Nunan, Naoise; Bloor, Juliette M. G.
  • FEMS Microbiology Letters, Vol. 364, Issue 9
  • DOI: 10.1093/femsle/fnx077

GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity
journal, April 2010


Applications of functional gene microarrays for profiling microbial communities
journal, June 2012


Elevated CO2 Increases Nitrogen Fixation at the Reproductive Phase Contributing to Various Yield Responses of Soybean Cultivars
journal, September 2017


The effects of elevated CO2 on symbiotic N2 fixation: a link between the carbon and nitrogen cycles in grassland ecosystems
journal, July 1995

  • Soussana, J. F.; Hartwig, U. A.
  • Plant and Soil, Vol. 187, Issue 2
  • DOI: 10.1007/BF00017097

Root exudates: the hidden part of plant defense
journal, February 2014


Climate warming reduces gut microbiota diversity in a vertebrate ectotherm
journal, May 2017

  • Bestion, Elvire; Jacob, Staffan; Zinger, Lucie
  • Nature Ecology & Evolution, Vol. 1, Issue 6
  • DOI: 10.1038/s41559-017-0161

Impacts of elevated CO 2 concentration on the productivity and surface energy budget of the soybean and maize agroecosystem in the Midwest USA
journal, July 2013

  • Twine, Tracy E.; Bryant, Jarod J.; T. Richter, Katherine
  • Global Change Biology, Vol. 19, Issue 9
  • DOI: 10.1111/gcb.12270

Elevated atmospheric CO2 levels affect community structure of rice root-associated bacteria
journal, February 2015


Elevated atmospheric CO 2 increases microbial growth rates in soil: results of three CO 2 enrichment experiments
journal, February 2010


Climate change goes underground: effects of elevated atmospheric CO2 on microbial community structure and activities in the rhizosphere
journal, March 2008

  • Drigo, Barbara; Kowalchuk, George A.; van Veen, Johannes A.
  • Biology and Fertility of Soils, Vol. 44, Issue 5
  • DOI: 10.1007/s00374-008-0277-3

Will Elevated Carbon Dioxide Concentration Amplify the Benefits of Nitrogen Fixation in Legumes?
journal, September 2009

  • Rogers, Alistair; Ainsworth, Elizabeth A.; Leakey, Andrew D. B.
  • Plant Physiology, Vol. 151, Issue 3
  • DOI: 10.1104/pp.109.144113

Soil microbial response in tallgrass prairie to elevated CO2
journal, March 1994

  • Rice, Charles W.; Garcia, Fernando O.; Hampton, Colleen O.
  • Plant and Soil, Vol. 165, Issue 1
  • DOI: 10.1007/BF00009963

Microbial Biogeography: From Taxonomy to Traits
journal, May 2008


Metagenomic reconstruction of nitrogen cycling pathways in a CO2-enriched grassland ecosystem
journal, March 2017


Soil carbon sequestration in a pine forest after 9 years of atmospheric CO 2 enrichment
journal, December 2008


Impact of anthropogenic CO2 emissions on global human nutrition
journal, August 2018


Elevated CO2 increases root exudation from loblolly pine (Pinus taeda) seedlings as an N-mediated response
journal, October 2009

  • Phillips, R. P.; Bernhardt, E. S.; Schlesinger, W. H.
  • Tree Physiology, Vol. 29, Issue 12
  • DOI: 10.1093/treephys/tpp083

Stochasticity, succession, and environmental perturbations in a fluidic ecosystem
journal, February 2014

  • Zhou, Jizhong; Deng, Ye; Zhang, Ping
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 9
  • DOI: 10.1073/pnas.1324044111

Stoichiometry constrains microbial response to root exudation- insights from a model and a field experiment in a temperate forest
journal, January 2013


Litterfall 15 N abundance indicates declining soil nitrogen availability in a free-air CO 2 enrichment experiment
journal, January 2011

  • Garten, Charles T.; Iversen, Colleen M.; Norby, Richard J.
  • Ecology, Vol. 92, Issue 1
  • DOI: 10.1890/10-0293.1

ELEVATED CO 2 STIMULATES NET ACCUMULATIONS OF CARBON AND NITROGEN IN LAND ECOSYSTEMS: A META-ANALYSIS
journal, January 2006

  • Luo, Yiqi; Hui, Dafeng; Zhang, Deqiang
  • Ecology, Vol. 87, Issue 1
  • DOI: 10.1890/04-1724

C4 grasses prosper as carbon dioxide eliminates desiccation in warmed semi-arid grassland
journal, August 2011

  • Morgan, Jack A.; LeCain, Daniel R.; Pendall, Elise
  • Nature, Vol. 476, Issue 7359
  • DOI: 10.1038/nature10274

Evolutionary Divergences in Root Exudate Composition among Ecologically-Contrasting Helianthus Species
journal, January 2016


Assessing the effect of elevated carbon dioxide on soil carbon: a comparison of four meta-analyses
journal, August 2009


Contrasting effects of elevated CO2 and warming on nitrogen cycling in a semiarid grassland
journal, May 2010


Detecting Nitrous Oxide Reductase (nosZ) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle
journal, June 2014


Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition
journal, April 2001

  • Reich, Peter B.; Knops, Jean; Tilman, David
  • Nature, Vol. 410, Issue 6830
  • DOI: 10.1038/35071062

Atmospheric CO 2 and soil extracellular enzyme activity: a meta-analysis and CO 2 gradient experiment
journal, August 2011

  • Kelley, Alexia M.; Fay, Philip A.; Polley, H. Wayne
  • Ecosphere, Vol. 2, Issue 8
  • DOI: 10.1890/ES11-00117.1

The soil microbiome at the Gi-FACE experiment responds to a moisture gradient but not to CO2 enrichment
journal, September 2016

  • de Menezes, Alexandre B.; Müller, Christoph; Clipson, Nicholas
  • Microbiology, Vol. 162, Issue 9
  • DOI: 10.1099/mic.0.000341

Nitrogen limitation constrains sustainability of ecosystem response to CO2
journal, April 2006

  • Reich, Peter B.; Hobbie, Sarah E.; Lee, Tali
  • Nature, Vol. 440, Issue 7086
  • DOI: 10.1038/nature04486

Microbial utilization of rice root exudates: 13C labeling and PLFA composition
journal, March 2016


Shifts in microbial communities in soil, rhizosphere and roots of two major crop systems under elevated CO2 and O3
journal, November 2017


Interactive Effects of Time, CO2, N, and Diversity on Total Belowground Carbon Allocation and Ecosystem Carbon Storage in a Grassland Community
journal, September 2009


CO2 enhancement of forest productivity constrained by limited nitrogen availability
journal, October 2010

  • Norby, R. J.; Warren, J. M.; Iversen, C. M.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 45
  • DOI: 10.1073/pnas.1006463107

Plant host habitat and root exudates shape soil bacterial community structure
journal, August 2008

  • Haichar, Feth el Zahar; Marol, Christine; Berge, Odile
  • The ISME Journal, Vol. 2, Issue 12
  • DOI: 10.1038/ismej.2008.80

Soil Conditions Rather Than Long-Term Exposure to Elevated CO2 Affect Soil Microbial Communities Associated with N-Cycling
journal, October 2017

  • Brenzinger, Kristof; Kujala, Katharina; Horn, Marcus A.
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.01976

Processes regulating progressive nitrogen limitation under elevated carbon dioxide: a meta-analysis
journal, January 2016


Terrestrial ecosystem carbon dynamics and climate feedbacks
journal, January 2008


Elevated CO 2 causes a change in microbial communities of rhizosphere and bulk soil of salt marsh system
journal, December 2016


Microarray-Based Analysis of Subnanogram Quantities of Microbial Community DNAs by Using Whole-Community Genome Amplification
journal, July 2006

  • Wu, L.; Liu, X.; Schadt, C. W.
  • Applied and Environmental Microbiology, Vol. 72, Issue 7
  • DOI: 10.1128/AEM.02738-05

The Diversity and Co-occurrence Patterns of N2-Fixing Communities in a CO2-Enriched Grassland Ecosystem
journal, August 2015


Distinct responses of soil microbial communities to elevated CO2 and O3 in a soybean agro-ecosystem
journal, October 2013


Faster Decomposition Under Increased Atmospheric CO2 Limits Soil Carbon Storage
journal, April 2014