Fire affects the taxonomic and functional composition of soil microbial communities, with cascading effects on grassland ecosystem functioning
Abstract
Fire is a crucial event regulating the structure and functioning of many ecosystems. Yet few studies have focused on how fire affects taxonomic and functional diversities of soil microbial communities, along with changes in plant communities and soil carbon (C) and nitrogen (N) dynamics. Here, we analyze these effects in a grassland ecosystem 9 months after an experimental fire at the Jasper Ridge Global Change Experiment site in California, USA. Fire altered soil microbial communities considerably, with community assembly process analysis showing that environmental selection pressure was higher in burned sites. However, a small subset of highly connected taxa was able to withstand the disturbance. In addition, fire decreased the relative abundances of most functional genes associated with C degradation and N cycling, implicating a slowdown of microbial processes linked to soil C and N dynamics. In contrast, fire stimulated above- and belowground plant growth, likely enhancing plant-microbe competition for soil inorganic N, which was reduced by a factor of about 2. To synthesize those findings, we performed structural equation modeling, which showed that plants but not microbial communities were responsible for significantly higher soil respiration rates in burned sites. Together, our results demonstrate that fire 'reboots' the grassland ecosystem bymore »
- Authors:
-
[1];
[2];
[3];
- Tsinghua Univ., Beijing (China). State Key Joint Lab. of Environment Simulation and Pollution Control, School of Environment
- Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics
- Carnegie Inst. for Science, Stanford, CA (United States)
- Western Michigan Univ., Kalamazoo MI (United States)
- Helmholtz Centre for Environmental Research– UFZ, Halle (Germany)
- Northern Arizona Univ., Flagstaff, AZ (United States). Center for Ecosystem Science and Society
- Inst. d'Ecologie et des Sciences de l'Environnement de Paris, Paris (France); Sorbonne Univ., Paris (France); Univ. Paris Diderot, Paris (France). Centre National de la Recherche Scientifique (CNRS), Inst. National de la Recherche Agronomique (INRA)
- Univ. de Lyon, Villeurbanne (France). Lab. d'Ecologie Microbienne, and Centre National de la Recherche Scientifique (CNRS), Inst. National de la Recherche Agronomique (INRA)
- Tsinghua Univ., Beijing (China). State Key Joint Lab. of Environment Simulation and Pollution Control, School of Environment; Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Science Foundation (NSF); National Natural Science Foundation of China (NSFC); Chinese Academy of Sciences (CAS); Packard Foundation; Morgan Family Foundation; French CNRS/INSU–EC2CO Program
- OSTI Identifier:
- 1580930
- Alternate Identifier(s):
- OSTI ID: 1572112
- Grant/Contract Number:
- AC02-05CH11231; 41430856; 41877048; 41825016; XDB15010102
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Global Change Biology
- Additional Journal Information:
- Journal Volume: 26; Journal Issue: 2; Journal ID: ISSN 1354-1013
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; Californian grasslands; climate change; fire; GeoChip; high‐throughput sequencing; microbial communities
Citation Formats
Yang, Sihang, Zheng, Qiaoshu, Yang, Yunfeng, Yuan, Mengting, Ma, Xingyu, Chiariello, Nona R., Docherty, Kathryn M., Field, Christopher B., Gutknecht, Jessica L. M., Hungate, Bruce A., Niboyet, Audrey, Le Roux, Xavier, and Zhou, Jizhong. Fire affects the taxonomic and functional composition of soil microbial communities, with cascading effects on grassland ecosystem functioning. United States: N. p., 2019.
Web. doi:10.1111/gcb.14852.
Yang, Sihang, Zheng, Qiaoshu, Yang, Yunfeng, Yuan, Mengting, Ma, Xingyu, Chiariello, Nona R., Docherty, Kathryn M., Field, Christopher B., Gutknecht, Jessica L. M., Hungate, Bruce A., Niboyet, Audrey, Le Roux, Xavier, & Zhou, Jizhong. Fire affects the taxonomic and functional composition of soil microbial communities, with cascading effects on grassland ecosystem functioning. United States. https://doi.org/10.1111/gcb.14852
Yang, Sihang, Zheng, Qiaoshu, Yang, Yunfeng, Yuan, Mengting, Ma, Xingyu, Chiariello, Nona R., Docherty, Kathryn M., Field, Christopher B., Gutknecht, Jessica L. M., Hungate, Bruce A., Niboyet, Audrey, Le Roux, Xavier, and Zhou, Jizhong. Mon .
"Fire affects the taxonomic and functional composition of soil microbial communities, with cascading effects on grassland ecosystem functioning". United States. https://doi.org/10.1111/gcb.14852. https://www.osti.gov/servlets/purl/1580930.
@article{osti_1580930,
title = {Fire affects the taxonomic and functional composition of soil microbial communities, with cascading effects on grassland ecosystem functioning},
author = {Yang, Sihang and Zheng, Qiaoshu and Yang, Yunfeng and Yuan, Mengting and Ma, Xingyu and Chiariello, Nona R. and Docherty, Kathryn M. and Field, Christopher B. and Gutknecht, Jessica L. M. and Hungate, Bruce A. and Niboyet, Audrey and Le Roux, Xavier and Zhou, Jizhong},
abstractNote = {Fire is a crucial event regulating the structure and functioning of many ecosystems. Yet few studies have focused on how fire affects taxonomic and functional diversities of soil microbial communities, along with changes in plant communities and soil carbon (C) and nitrogen (N) dynamics. Here, we analyze these effects in a grassland ecosystem 9 months after an experimental fire at the Jasper Ridge Global Change Experiment site in California, USA. Fire altered soil microbial communities considerably, with community assembly process analysis showing that environmental selection pressure was higher in burned sites. However, a small subset of highly connected taxa was able to withstand the disturbance. In addition, fire decreased the relative abundances of most functional genes associated with C degradation and N cycling, implicating a slowdown of microbial processes linked to soil C and N dynamics. In contrast, fire stimulated above- and belowground plant growth, likely enhancing plant-microbe competition for soil inorganic N, which was reduced by a factor of about 2. To synthesize those findings, we performed structural equation modeling, which showed that plants but not microbial communities were responsible for significantly higher soil respiration rates in burned sites. Together, our results demonstrate that fire 'reboots' the grassland ecosystem by differentially regulating plant and soil microbial communities, leading to significant changes in soil C and N dynamics.},
doi = {10.1111/gcb.14852},
journal = {Global Change Biology},
number = 2,
volume = 26,
place = {United States},
year = {2019},
month = {9}
}
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Works referenced in this record:
Changes in enzyme activities and microbial biomass of tallgrass prairie soil as related to burning and nitrogen fertilization
journal, May 1999
- Ajwa, H. A.; Dell, C. J.; Rice, C. W.
- Soil Biology and Biochemistry, Vol. 31, Issue 5
Tropical savannah woodland: effects of experimental fire on soil microorganisms and soil emissions of carbon dioxide
journal, May 2004
- Andersson, Michael; Michelsen, Anders; Jensen, Michael
- Soil Biology and Biochemistry, Vol. 36, Issue 5
Fire in the Earth System
journal, April 2009
- Bowman, D. M. J. S.; Balch, J. K.; Artaxo, P.
- Science, Vol. 324, Issue 5926
Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale
journal, March 2011
- Caruso, Tancredi; Chan, Yuki; Lacap, Donnabella C.
- The ISME Journal, Vol. 5, Issue 9
Metagenomic Assessment of the Potential Microbial Nitrogen Pathways in the Rhizosphere of a Mediterranean Forest After a Wildfire
journal, March 2015
- Cobo-Díaz, José F.; Fernández-González, Antonio J.; Villadas, Pablo J.
- Microbial Ecology, Vol. 69, Issue 4
The ecology of the microbiome: Networks, competition, and stability
journal, November 2015
- Coyte, K. Z.; Schluter, J.; Foster, K. R.
- Science, Vol. 350, Issue 6261
How surface fire in Siberian Scots pine forests affects soil organic carbon in the forest floor: Stocks, molecular structure, and conversion to black carbon (charcoal): SURFACE FIRE IN SIBERIAN SCOTS PINE FOREST
journal, March 2003
- Czimczik, Claudia I.; Preston, Caroline M.; Schmidt, Michael W. I.
- Global Biogeochemical Cycles, Vol. 17, Issue 1
Insidious effects of sequencing errors on perceived diversity in molecular surveys: Letters
journal, September 2010
- Dickie, Ian A.
- New Phytologist, Vol. 188, Issue 4
Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession
journal, March 2015
- Dini-Andreote, Francisco; Stegen, James C.; van Elsas, Jan Dirk
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 11
Soil microbial responses to fire and interacting global change factors in a California annual grassland
journal, October 2011
- Docherty, Kathryn M.; Balser, Teri C.; Bohannan, Brendan J. M.
- Biogeochemistry, Vol. 109, Issue 1-3
Search and clustering orders of magnitude faster than BLAST
journal, August 2010
- Edgar, Robert C.
- Bioinformatics, Vol. 26, Issue 19, p. 2460-2461
UCHIME improves sensitivity and speed of chimera detection
journal, June 2011
- Edgar, Robert C.; Haas, Brian J.; Clemente, Jose C.
- Bioinformatics, Vol. 27, Issue 16
Competition, Not Cooperation, Dominates Interactions among Culturable Microbial Species
journal, October 2012
- Foster, Kevin R.; Bell, Thomas
- Current Biology, Vol. 22, Issue 19
The Impact of Climate Change on Wildfire Severity: A Regional Forecast for Northern California
journal, May 2004
- Fried, Jeremy S.; Torn, Margaret S.; Mills, Evan
- Climatic Change, Vol. 64, Issue 1/2
Inter-annual variation in soil extra-cellular enzyme activity in response to simulated global change and fire disturbance
journal, August 2010
- Gutknecht, Jessica L. M.; Henry, Hugh A. L.; Balser, Teri C.
- Pedobiologia, Vol. 53, Issue 5
Post-fire vegetative dynamics as drivers of microbial community structure and function in forest soils
journal, December 2005
- Hart, Stephen C.; DeLuca, Thomas H.; Newman, Gregory S.
- Forest Ecology and Management, Vol. 220, Issue 1-3
Interactive Effects of Fire, Elevated Carbon Dioxide, Nitrogen Deposition, and precipitation on a California Annual Grassland
journal, November 2006
- Henry, Hugh A. L.; Chiariello, Nona R.; Vitousek, Peter M.
- Ecosystems, Vol. 9, Issue 7
Interactive effects of elevated CO2, N deposition and climate change on extracellular enzyme activity and soil density fractionation in a California annual grassland
journal, October 2005
- Henry, Hugh A. L.; Juarez, John D.; Field, Christopher B.
- Global Change Biology, Vol. 11, Issue 10
Keystone taxa predict compositional change in microbial communities
journal, June 2018
- Herren, Cristina M.; McMahon, Katherine D.
- Environmental Microbiology, Vol. 20, Issue 6
Mechanisms controlling soil carbon turnover and their potential application for enhancing carbon sequestration
journal, December 2006
- Jastrow, Julie D.; Amonette, James E.; Bailey, Vanessa L.
- Climatic Change, Vol. 80, Issue 1-2
The links between ecosystem multifunctionality and above- and belowground biodiversity are mediated by climate
journal, September 2015
- Jing, Xin; Sanders, Nathan J.; Shi, Yu
- Nature Communications, Vol. 6, Issue 1
Autogenic succession and deterministic recovery following disturbance in soil bacterial communities
journal, April 2017
- Jurburg, Stephanie D.; Nunes, Inês; Stegen, James C.
- Scientific Reports, Vol. 7, Issue 1
Fire-driven alien invasion in a fire-adapted ecosystem
journal, January 2012
- Keeley, Jon E.; Brennan, Teresa J.
- Oecologia, Vol. 169, Issue 4
Fire as an evolutionary pressure shaping plant traits
journal, August 2011
- Keeley, Jon E.; Pausas, Juli G.; Rundel, Philip W.
- Trends in Plant Science, Vol. 16, Issue 8
DETERMINANTS OF SOIL CO 2 FLUX FROM A SUB-HUMID GRASSLAND: EFFECT OF FIRE AND FIRE HISTORY
journal, August 1998
- Knapp, Alan K.; Conard, Shawn L.; Blair, John M.
- Ecological Applications, Vol. 8, Issue 3
Dynamics in microbial communities: unraveling mechanisms to identify principles
journal, December 2014
- Konopka, Allan; Lindemann, Stephen; Fredrickson, Jim
- The ISME Journal, Vol. 9, Issue 7
Metabolic modeling of species interaction in the human microbiome elucidates community-level assembly rules
journal, July 2013
- Levy, R.; Borenstein, E.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 31
Soil-surface carbon dioxide efflux and microbial biomass in relation to tree density 13 years after a stand replacing fire in a lodgepole pine ecosystem
journal, May 2003
- Litton, Creighton M.; Ryan, Michael G.; Knight, Dennis H.
- Global Change Biology, Vol. 9, Issue 5
The interactive effects of soil transplant into colder regions and cropping on soil microbiology and biogeochemistry: Effects of northward soil transplant and cropping
journal, February 2014
- Liu, Shanshan; Wang, Feng; Xue, Kai
- Environmental Microbiology, Vol. 17, Issue 3
Soil environmental factors rather than denitrification gene abundance control N2O fluxes in a wet sclerophyll forest with different burning frequency
journal, February 2013
- Liu, Xian; Chen, C. R.; Wang, W. J.
- Soil Biology and Biochemistry, Vol. 57
Charcoal and shrubs modify soil processes in ponderosa pine forests of western Montana
journal, August 2006
- MacKenzie, M. D.; DeLuca, T. H.
- Plant and Soil, Vol. 287, Issue 1-2
FLASH: fast length adjustment of short reads to improve genome assemblies
journal, September 2011
- Magoc, T.; Salzberg, S. L.
- Bioinformatics, Vol. 27, Issue 21
Taxonomical and functional microbial community selection in soybean rhizosphere
journal, February 2014
- Mendes, Lucas W.; Kuramae, Eiko E.; Navarrete, Acácio A.
- The ISME Journal, Vol. 8, Issue 8
Soil respiration dynamics in fire affected semi-arid ecosystems: Effects of vegetation type and environmental factors
journal, December 2016
- Muñoz-Rojas, Miriam; Lewandrowski, Wolfgang; Erickson, Todd E.
- Science of The Total Environment, Vol. 572
Fire effects on belowground sustainability: a review and synthesis
journal, September 1999
- Neary, Daniel G.; Klopatek, Carole C.; DeBano, Leonard F.
- Forest Ecology and Management, Vol. 122, Issue 1-2
Global Change Could Amplify Fire Effects on Soil Greenhouse Gas Emissions
journal, June 2011
- Niboyet, Audrey; Brown, Jamie R.; Dijkstra, Paul
- PLoS ONE, Vol. 6, Issue 6
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
Fire and Vegetation Effects on Productivity and Nitrogen Cycling Across a Forest–Grassland Continuum
journal, June 2001
- Reich, Peter B.; Peterson, David W.; Wedin, David A.
- Ecology, Vol. 82, Issue 6
Short-term effects of fire on soil nitrogen availability in Mediterranean grasslands and shrublands growing in old fields
journal, June 2001
- Romanyà, Joan; Casals, Pere; Vallejo, V. R.
- Forest Ecology and Management, Vol. 147, Issue 1
Comparison of nitrogen monoxide emissions from several African tropical ecosystems and influence of season and fire
journal, December 1998
- Serça, D.; Delmas, R.; Le Roux, X.
- Global Biogeochemical Cycles, Vol. 12, Issue 4
Postfire Soil N Cycling in Northern Conifer Forests Affected by Severe, Stand-Replacing Wildfires
journal, February 2005
- Smithwick, Erica A. H.; Turner, Monica G.; Mack, Michelle C.
- Ecosystems, Vol. 8, Issue 2
Quantifying community assembly processes and identifying features that impose them
journal, June 2013
- Stegen, James C.; Lin, Xueju; Fredrickson, Jim K.
- The ISME Journal, Vol. 7, Issue 11
Experimental fire increases soil carbon dioxide efflux in a grassland long-term multifactor global change experiment
journal, November 2016
- Strong, Aaron L.; Johnson, Tera P.; Chiariello, Nona R.
- Global Change Biology, Vol. 23, Issue 5
Wildfire reduces carbon dioxide efflux and increases methane uptake in ponderosa pine forest soils of the southwestern USA
journal, July 2010
- Sullivan, Benjamin W.; Kolb, Thomas E.; Hart, Stephen C.
- Biogeochemistry, Vol. 104, Issue 1-3
Impact of fire on active layer and permafrost microbial communities and metagenomes in an upland Alaskan boreal forest
journal, April 2014
- Taş, Neslihan; Prestat, Emmanuel; McFarland, Jack W.
- The ISME Journal, Vol. 8, Issue 9
Soil n and Plant Responses to Fire, Topography, and Supplemental n in Tallgrass Prairie
journal, September 1997
- Turner, Clarence L.; Blair, John M.; Schartz, Rita J.
- Ecology, Vol. 78, Issue 6
Inorganic nitrogen availability after severe stand-replacing fire in the Greater Yellowstone ecosystem
journal, March 2007
- Turner, M. G.; Smithwick, E. A. H.; Metzger, K. L.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 12
Precipitation variability and fire influence the temporal dynamics of soil CO2 efflux in an arid grassland
journal, January 2012
- Vargas, Rodrigo; Collins, Scott L.; Thomey, Michell L.
- Global Change Biology, Vol. 18, Issue 4
Interactive effects of wildfire and permafrost on microbial communities and soil processes in an Alaskan black spruce forest
journal, September 2008
- Waldrop, Mark P.; Harden, Jennifer W.
- Global Change Biology
Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes
journal, February 2013
- Wang, Jianjun; Shen, Ji; Wu, Yucheng
- The ISME Journal, Vol. 7, Issue 7
Normalization and microbial differential abundance strategies depend upon data characteristics
journal, March 2017
- Weiss, Sophie; Xu, Zhenjiang Zech; Peddada, Shyamal
- Microbiome, Vol. 5, Issue 1
Warming and Earlier Spring Increase Western U.S. Forest Wildfire Activity
journal, August 2006
- Westerling, A. L.
- Science, Vol. 313, Issue 5789
Water- and plant-mediated responses of soil respiration to topography, fire, and nitrogen fertilization in a semiarid grassland in northern China
journal, March 2008
- Xu, Wenhua; Wan, Shiqiang
- Soil Biology and Biochemistry, Vol. 40, Issue 3
Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland
journal, November 2012
- Yang, Yunfeng; Wu, Linwei; Lin, Qiaoyan
- Global Change Biology, Vol. 19, Issue 2
Changes in Nitrogen-Fixing and Ammonia-Oxidizing Bacterial Communities in Soil of a Mixed Conifer Forest after Wildfire
journal, May 2005
- Yeager, C. M.; Northup, D. E.; Grow, C. C.
- Applied and Environmental Microbiology, Vol. 71, Issue 5
Metabolic dependencies drive species co-occurrence in diverse microbial communities
journal, May 2015
- Zelezniak, Aleksej; Andrejev, Sergej; Ponomarova, Olga
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 20
DNA recovery from soils of diverse composition.
journal, January 1996
- Zhou, J.; Bruns, M. A.; Tiedje, J. M.
- Applied and environmental microbiology, Vol. 62, Issue 2
Positive and negative carbon mineralization priming effects among a variety of biochar-amended soils
journal, June 2011
- Zimmerman, Andrew R.; Gao, Bin; Ahn, Mi-Youn
- Soil Biology and Biochemistry, Vol. 43, Issue 6
High resilience of the mycorrhizal community to prescribed seasonal burnings in eastern Mediterranean woodlands
journal, January 2021
- Livne-Luzon, Stav; Shemesh, Hagai; Osem, Yagil
- Mycorrhiza, Vol. 31, Issue 2
Microbial community structure and functional properties in permanently and seasonally flooded areas in Poyang Lake
journal, March 2020
- Liu, Yang; Ren, Ze; Qu, Xiaodong
- Scientific Reports, Vol. 10, Issue 1
Global Change Could Amplify Fire Effects on Soil Greenhouse Gas Emissions
text, January 2011
- Niboyet, Audrey; Brown, Jamie R.; Dijkstra, Paul
- ETH Zurich
Fire and Vegetation Effects on Productivity and Nitrogen Cycling across a Forest-Grassland Continuum
journal, June 2001
- Reich, Peter B.; Peterson, David W.; Wedin, David A.
- Ecology, Vol. 82, Issue 6