Changes in Fungal Community Composition in Response to Elevated Atmospheric CO2 and Nitrogen Fertilization Varies with Soil Horizon
Abstract
Increasing levels of atmospheric carbon dioxide (CO2) and rates of nitrogen (N)-deposition to forest ecosystems are predicted to alter the structure and function of soil fungal communities, but the spatially heterogeneous distribution of soil fungi has hampered investigations aimed at understanding such impacts. We hypothesized that soil physical and chemical properties and fungal community composition would be differentially impacted by elevated atmospheric CO2 (eCO2) and N-fertilization in spatially separated field samples, in the forest floor, 0–2, 2–5, and 5–10 cm depth intervals in a loblolly pine Free-Air Carbon Dioxide Enrichment (FACE) experiment. In all soils, quantitative PCR-based estimates of fungal biomass were highest in the forest floor. Fungal richness, based on pyrosequencing of the fungal ribosomal large subunit gene, increased in response to N-fertilization in 0–2 cm and forest floor intervals. Composition shifted in forest floor, 0–2 and 2–5 cm intervals in response to N-fertilization, but the shift was most distinct in the 0–2 cm interval, in which the largest number of statistically significant changes in soil chemical parameters (i.e., phosphorus, organic matter, calcium, pH) was also observed. In the 0–2 cm interval, increased recovery of sequences from the Thelephoraceae, Tricholomataceae, Hypocreaceae, Clavicipitaceae, and Herpotrichiellaceae families and decreased recovery ofmore »
- Authors:
-
- Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
- Duke University, Durham, NC (United States)
- Publication Date:
- Research Org.:
- Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1628085
- Grant/Contract Number:
- AC52-06NA25396
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Volume: 4; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; soil fungi; elevated CO2; nitrogen fertilization; forest floor; soil chemistry; Ascomycota; basidiomycota; agaricales
Citation Formats
Weber, Carolyn F., Vilgalys, Rytas, and Kuske, Cheryl R. Changes in Fungal Community Composition in Response to Elevated Atmospheric CO2 and Nitrogen Fertilization Varies with Soil Horizon. United States: N. p., 2013.
Web. doi:10.3389/fmicb.2013.00078.
Weber, Carolyn F., Vilgalys, Rytas, & Kuske, Cheryl R. Changes in Fungal Community Composition in Response to Elevated Atmospheric CO2 and Nitrogen Fertilization Varies with Soil Horizon. United States. https://doi.org/10.3389/fmicb.2013.00078
Weber, Carolyn F., Vilgalys, Rytas, and Kuske, Cheryl R. Tue .
"Changes in Fungal Community Composition in Response to Elevated Atmospheric CO2 and Nitrogen Fertilization Varies with Soil Horizon". United States. https://doi.org/10.3389/fmicb.2013.00078. https://www.osti.gov/servlets/purl/1628085.
@article{osti_1628085,
title = {Changes in Fungal Community Composition in Response to Elevated Atmospheric CO2 and Nitrogen Fertilization Varies with Soil Horizon},
author = {Weber, Carolyn F. and Vilgalys, Rytas and Kuske, Cheryl R.},
abstractNote = {Increasing levels of atmospheric carbon dioxide (CO2) and rates of nitrogen (N)-deposition to forest ecosystems are predicted to alter the structure and function of soil fungal communities, but the spatially heterogeneous distribution of soil fungi has hampered investigations aimed at understanding such impacts. We hypothesized that soil physical and chemical properties and fungal community composition would be differentially impacted by elevated atmospheric CO2 (eCO2) and N-fertilization in spatially separated field samples, in the forest floor, 0–2, 2–5, and 5–10 cm depth intervals in a loblolly pine Free-Air Carbon Dioxide Enrichment (FACE) experiment. In all soils, quantitative PCR-based estimates of fungal biomass were highest in the forest floor. Fungal richness, based on pyrosequencing of the fungal ribosomal large subunit gene, increased in response to N-fertilization in 0–2 cm and forest floor intervals. Composition shifted in forest floor, 0–2 and 2–5 cm intervals in response to N-fertilization, but the shift was most distinct in the 0–2 cm interval, in which the largest number of statistically significant changes in soil chemical parameters (i.e., phosphorus, organic matter, calcium, pH) was also observed. In the 0–2 cm interval, increased recovery of sequences from the Thelephoraceae, Tricholomataceae, Hypocreaceae, Clavicipitaceae, and Herpotrichiellaceae families and decreased recovery of sequences from the Amanitaceae correlated with N-fertilization. In this same depth interval, Amanitaceae, Tricholomataceae, and Herpotriciellaceae sequences were recovered less frequently from soils exposed to eCO2 relative to ambient conditions. These results demonstrated that vertical stratification should be taken into consideration in future efforts to elucidate environmental impacts on fungal communities and their feedbacks on ecosystem processes.},
doi = {10.3389/fmicb.2013.00078},
journal = {Frontiers in Microbiology},
number = ,
volume = 4,
place = {United States},
year = {Tue Apr 09 00:00:00 EDT 2013},
month = {Tue Apr 09 00:00:00 EDT 2013}
}
Works referenced in this record:
Elevated Atmospheric CO2 Alters Soil Microbial Communities Associated with Trembling Aspen (Populus tremuloides) Roots
journal, July 2005
- Janus, Lori R.; Angeloni, Nicholas L.; McCormack, John
- Microbial Ecology, Vol. 50, Issue 1
Fungal community composition and metabolism under elevated CO2 and O3
journal, October 2005
- Chung, Haegeun; Zak, Donald R.; Lilleskov, Erik A.
- Oecologia, Vol. 147, Issue 1
Expression of genes involved in symbiotic carbon and nitrogen transport in Pinus taeda mycorrhizal roots exposed to CO2 enrichment and nitrogen fertilization
journal, May 2009
- Parrent, Jeri Lynn; Vilgalys, Rytas
- Mycorrhiza, Vol. 19, Issue 7
Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages
journal, September 2009
- Tedersoo, Leho; May, Tom W.; Smith, Matthew E.
- Mycorrhiza, Vol. 20, Issue 4
Microbial Cycling of C and N in Northern Hardwood Forests Receiving Chronic Atmospheric NO3− Deposition
journal, March 2006
- Zak, Donald R.; Holmes, William E.; Tomlinson, Matthew J.
- Ecosystems, Vol. 9, Issue 2
Independent, Interactive, and Species-Specific Responses of Leaf Litter Decomposition to Elevated CO2 and O3 in a Northern Hardwood Forest
journal, April 2008
- Parsons, William F. J.; Bockheim, James G.; Lindroth, Richard L.
- Ecosystems, Vol. 11, Issue 4
Effects of elevated CO2 on foliar quality and herbivore damage in a scrub oak ecosystem
journal, February 2005
- Hall, Myra C.; Stiling, Peter; Moon, Daniel C.
- Journal of Chemical Ecology, Vol. 31, Issue 2
Mycorrhizal dynamics under elevated CO2 and nitrogen fertilization in a warm temperate forest
journal, December 2007
- Garcia, Maria O.; Ovasapyan, Tatevik; Greas, Mary
- Plant and Soil, Vol. 303, Issue 1-2
Effect of moisture content, temperature and nitrogen fertilization on carbon dioxide evolution from field soils
journal, January 1978
- Kowalenko, C. G.; Ivarson, K. C.; cameron, D. R.
- Soil Biology and Biochemistry, Vol. 10, Issue 5
Chronic nitrogen additions reduce total soil respiration and microbial respiration in temperate forest soils at the Harvard Forest
journal, July 2004
- Bowden, Richard D.; Davidson, Eric; Savage, Kathleen
- Forest Ecology and Management, Vol. 196, Issue 1
Low levels of nitrogen addition stimulate decomposition by boreal forest fungi
journal, February 2009
- Allison, Steven D.; LeBauer, David S.; Ofrecio, M. Rosario
- Soil Biology and Biochemistry, Vol. 41, Issue 2
Resistance of microbial and soil properties to warming treatment seven years after boreal fire
journal, October 2010
- Allison, Steven D.; McGuire, Krista L.; Treseder, Kathleen K.
- Soil Biology and Biochemistry, Vol. 42, Issue 10
Nitrogen fertilization inhibits soil microbial respiration regardless of the form of nitrogen applied
journal, December 2010
- Ramirez, Kelly S.; Craine, Joseph M.; Fierer, Noah
- Soil Biology and Biochemistry, Vol. 42, Issue 12
Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes
journal, September 2000
- Hibbett, David S.; Gilbert, Luz-Beatriz; Donoghue, Michael J.
- Nature, Vol. 407, Issue 6803
The fate of carbon in grasslands under carbon dioxide enrichment
journal, August 1997
- Hungate, Bruce A.; Holland, Elisabeth A.; Jackson, Robert B.
- Nature, Vol. 388, Issue 6642
Disruption of root carbon transport into forest humus stimulates fungal opportunists at the expense of mycorrhizal fungi
journal, March 2010
- Lindahl, Björn D.; de Boer, Wietse; Finlay, Roger D.
- The ISME Journal, Vol. 4, Issue 7
Soil bacterial and fungal communities across a pH gradient in an arable soil
journal, May 2010
- Rousk, Johannes; Bååth, Erland; Brookes, Philip C.
- The ISME Journal, Vol. 4, Issue 10
Variable effects of nitrogen additions on the stability and turnover of soil carbon
journal, October 2002
- Neff, Jason C.; Townsend, Alan R.; Gleixner, Gerd
- Nature, Vol. 419, Issue 6910
In situ litter decomposition and litter quality in a Mojave Desert ecosystem: effects of elevated atmospheric CO 2 and interannual climate variability: CO 2 EFFECTS ON ARID LAND LITTER DECOMPOSITION
journal, July 2003
- Weatherly, Heather E.; Zitzer, Stephen F.; Coleman, James S.
- Global Change Biology, Vol. 9, Issue 8
The impact of elevated CO2 and global climate change on arbuscular mycorrhizas: a mycocentric approach: REVIEW Mycorrhizas and global change
journal, July 2000
- Fitter, A. H.; Heinemeyer, A.; Staddon, P. L.
- New Phytologist, Vol. 147, Issue 1
Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition: REVIEW Mycorrhizal fungi and soil carbon
journal, July 2000
- Treseder, K. K.; Allen, M. F.
- New Phytologist, Vol. 147, Issue 1
The diversity and biogeography of soil bacterial communities
journal, January 2006
- Fierer, N.; Jackson, R. B.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 3
Carbon allocation, root exudation and mycorrhizal colonization of Pinus echinata seedlings grown under CO2 enrichment
journal, September 1987
- Norby, R. J.; O'Neill, E. G.; Hood, W. G.
- Tree Physiology, Vol. 3, Issue 3
A general biogeochemical model describing the responses of the C and N cycles in terrestrial ecosystems to changes in CO2, climate, and N deposition
journal, July 1991
- Rastetter, E. B.; Ryan, M. G.; Shaver, G. R.
- Tree Physiology, Vol. 9, Issue 1-2
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
Effects of Ammonium Nitrate, Triple Superphosphate, and Muriate of Potash on Reaction of Yahola loam in a Factorial Fertilizer Experiment
journal, September 1961
- Alben, A. O.
- Soil Science, Vol. 92, Issue 3
Linking microbial activity and soil organic matter transformations in forest soils under elevated CO2
journal, February 2005
- Billings, S. A.; Ziegler, S. E.
- Global Change Biology, Vol. 11, Issue 2
Altered patterns of soil carbon substrate usage and heterotrophic respiration in a pine forest with elevated CO 2 and N fertilization
journal, May 2008
- Billings, Sharon A.; Ziegler, Susan E.
- Global Change Biology, Vol. 14, Issue 5
Elevated atmospheric CO 2 affects soil microbial diversity associated with trembling aspen
journal, April 2008
- Lesaulnier, Celine; Papamichail, Dimitris; McCorkle, Sean
- Environmental Microbiology, Vol. 10, Issue 4
The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling
journal, November 2008
- Nemergut, Diana R.; Townsend, Alan R.; Sattin, Sarah R.
- Environmental Microbiology, Vol. 10, Issue 11
Community structure of arbuscular mycorrhizal fungi at different soil depths in extensively and intensively managed agroecosystems
journal, December 2004
- Oehl, Fritz; Sieverding, Ewald; Ineichen, Kurt
- New Phytologist, Vol. 165, Issue 1
Re-assessment of plant carbon dynamics at the Duke free-air CO2 enrichment site: interactions of atmospheric [CO2] with nitrogen and water availability over stand development
journal, November 2009
- McCarthy, Heather R.; Oren, Ram; Johnsen, Kurt H.
- New Phytologist, Vol. 185, Issue 2
A Coherent Signature of Anthropogenic Nitrogen Deposition to Remote Watersheds of the Northern Hemisphere
journal, December 2011
- Holtgrieve, G. W.; Schindler, D. E.; Hobbs, W. O.
- Science, Vol. 334, Issue 6062
Simulated Atmospheric N Deposition Alters Fungal Community Composition and Suppresses Ligninolytic Gene Expression in a Northern Hardwood Forest
journal, June 2011
- Edwards, Ivan P.; Zak, Donald R.; Kellner, Harald
- PLoS ONE, Vol. 6, Issue 6
Communities of Arbuscular Mycorrhizal Fungi Detected in Forest Soil Are Spatially Heterogeneous but Do Not Vary throughout the Growing Season
journal, August 2012
- Davison, John; Öpik, Maarja; Zobel, Martin
- PLoS ONE, Vol. 7, Issue 8
Nitrogen Deposition Modifies soil Carbon Storage Through Changes in Microbial Enzymatic Activity
journal, August 2004
- Waldrop, Mark P.; Zak, Donald R.; Sinsabaugh, Robert L.
- Ecological Applications, Vol. 14, Issue 4
Soil carbon sequestration in prairie grasslands increased by chronic nitrogen addition
journal, September 2012
- Fornara, Dario A.; Tilman, David
- Ecology, Vol. 93, Issue 9
The Myth of Nitrogen Fertilization for Soil Carbon Sequestration
journal, January 2007
- Khan, S. A.; Mulvaney, R. L.; Ellsworth, T. R.
- Journal of Environment Quality, Vol. 36, Issue 6
Spatial Distribution of Ammonium and Calcium in Optimally Fertilized Pine Plantation Soils
journal, November 2005
- Edwards, Ivan; Gillespie, Andrew; Chen, Jennifer
- Soil Science Society of America Journal, Vol. 69, Issue 6
Vertical distribution of fungal communities in tallgrass prairie soil
journal, September 2010
- Jumpponen, Ari; Jones, Kenneth L.; Blair, John
- Mycologia, Vol. 102, Issue 5
Works referencing / citing this record:
Composition of the soil fungal community is more sensitive to phosphorus than nitrogen addition in the alpine meadow on the Qinghai-Tibetan Plateau
journal, August 2016
- He, Dan; Xiang, Xingjia; He, Jin-Sheng
- Biology and Fertility of Soils, Vol. 52, Issue 8
Don't put all your eggs in one basket: a cost-effective and powerful method to optimize primer choice for rRNA environmental community analyses using the Fluidigm Access Array
journal, February 2016
- Brown, Shawn P.; Ferrer, Astrid; Dalling, James W.
- Molecular Ecology Resources, Vol. 16, Issue 4
Short-Term Transcriptional Response of Microbial Communities to Nitrogen Fertilization in a Pine Forest Soil
journal, May 2018
- Albright, Michaeline B. N.; Johansen, Renee; Lopez, Deanna
- Applied and Environmental Microbiology, Vol. 84, Issue 15
Fungi exposed to chronic nitrogen enrichment are less able to decay leaf litter
posted_content, August 2016
- van Diepen, Linda T. A.; Frey, Serita D.; Landis, Elizabeth A.
- Ecology
Fungal Communities and Functional Guilds Shift Along an Elevational Gradient in the Southern Appalachian Mountains
journal, December 2017
- Veach, Allison M.; Stokes, C. Elizabeth; Knoepp, Jennifer
- Microbial Ecology, Vol. 76, Issue 1
Direct and indirect effects of elevated CO2 and nitrogen addition on soil microbial communities in the rhizosphere of Bothriochloa ischaemum
journal, May 2019
- Xiao, Lie; Liu, Guobin; Li, Peng
- Journal of Soils and Sediments, Vol. 19, Issue 11
Mineral vs. Organic Amendments: Microbial Community Structure, Activity and Abundance of Agriculturally Relevant Microbes Are Driven by Long-Term Fertilization Strategies
journal, September 2016
- Francioli, Davide; Schulz, Elke; Lentendu, Guillaume
- Frontiers in Microbiology, Vol. 7
High-yield grass Pennisetum sinese Roxb plantation and organic manure alter bacterial and fungal communities structure in an ecological agriculture farm
journal, May 2020
- He, Yan; Lu, Lu; Peng, Chao
- AMB Express, Vol. 10, Issue 1
Contrasting soil fungal community responses to experimental nitrogen addition using the large subunit rRNA taxonomic marker and cellobiohydrolase I functional marker
journal, August 2014
- Mueller, Rebecca C.; Balasch, Monica M.; Kuske, Cheryl R.
- Molecular Ecology, Vol. 23, Issue 17
Response of microbial diversity to C:N:P stoichiometry in fine root and microbial biomass following afforestation
journal, March 2017
- Ren, Chengjie; Chen, Ji; Deng, Jian
- Biology and Fertility of Soils, Vol. 53, Issue 4
Simple measurements in a complex system: soil community responses to nitrogen amendment in a Pinus taeda forest
journal, April 2019
- Kuske, Cheryl R.; Sinsabaugh, Robert L.; Gallegos‐Graves, La Verne
- Ecosphere, Vol. 10, Issue 4
Long‐term effects of nitrogen and phosphorus fertilization on soil microbial community structure and function under continuous wheat production
journal, August 2019
- Li, Yunliang; Tremblay, Julien; Bainard, Luke D.
- Environmental Microbiology, Vol. 22, Issue 3
Fungal community composition in soils subjected to long-term chemical fertilization is most influenced by the type of organic matter: Fertilizer organic matter influences soil fungal community
journal, September 2016
- Sun, Ruibo; Dsouza, Melissa; Gilbert, Jack A.
- Environmental Microbiology, Vol. 18, Issue 12
Impact of agro-farming activities on microbial diversity of acidic red soils in a Camellia Oleifera Forest
journal, January 2019
- Li, Jun; Wu, Zelong; Yuan, Jun
- Revista Brasileira de Ciência do Solo, Vol. 43
An evolutionary signal to fungal succession during plant litter decay
journal, September 2019
- Vivelo, Sasha; Bhatnagar, Jennifer M.
- FEMS Microbiology Ecology, Vol. 95, Issue 10
Long-term effects of grassland management on soil microbial abundance: implications for soil carbon and nitrogen storage
journal, October 2018
- Egan, Gary; Zhou, Xue; Wang, Dongmei
- Biogeochemistry, Vol. 141, Issue 2
CdS nanoparticles alleviate photo-induced stress in Geobacter co-cultures
journal, January 2019
- Chen, Shanshan; Deng, Chengsheng; Liu, Xing
- Environmental Science: Nano, Vol. 6, Issue 6
Fungal Community Structure in Disease Suppressive Soils Assessed by 28S LSU Gene Sequencing
journal, April 2014
- Penton, C. Ryan; Gupta, V. V. S. R.; Tiedje, James M.
- PLoS ONE, Vol. 9, Issue 4
Fungi exposed to chronic nitrogen enrichment are less able to decay leaf litter
journal, January 2017
- van Diepen, Linda T. A.; Frey, Serita D.; Landis, Elizabeth A.
- Ecology, Vol. 98, Issue 1
Different Selectivity in Fungal Communities Between Manure and Mineral Fertilizers: A Study in an Alkaline Soil After 30 Years Fertilization
journal, October 2018
- Wang, Ying; Ji, Hongfei; Hu, Yaxian
- Frontiers in Microbiology, Vol. 9
The Abundance of Fungi, Bacteria and Denitrification Genes during Insect Outbreaks in Scots Pine Forests
journal, August 2018
- Grüning, Maren; Beule, Lukas; Meyer, Stephanie
- Forests, Vol. 9, Issue 8
eDNA from roots: a robust tool for determining Phytophthora communities in natural ecosystems
journal, March 2018
- Khaliq, Ihsanul; Hardy, Giles E. St J.; White, Diane
- FEMS Microbiology Ecology, Vol. 94, Issue 5
Differential mechanisms underlying responses of soil bacterial and fungal communities to nitrogen and phosphorus inputs in a subtropical forest
journal, January 2019
- Li, Yong; Tian, Dashuan; Wang, Jinsong
- PeerJ, Vol. 7
An evolutionary signal to fungal succession during plant litter decay
journal, September 2019
- Vivelo, Sasha; Bhatnagar, Jennifer M.
- FEMS Microbiology Ecology, Vol. 95, Issue 10
Highly diversified fungi are associated with the achlorophyllous orchid Gastrodia flavilabella
journal, March 2015
- Liu, Tsunglin; Li, Ching-Min; Han, Yue-Lun
- BMC Genomics, Vol. 16, Issue 1
Forest floor community metatranscriptomes identify fungal and bacterial responses to N deposition in two maple forests
journal, April 2015
- Hesse, Cedar N.; Mueller, Rebecca C.; Vuyisich, Momchilo
- Frontiers in Microbiology, Vol. 6
Different Selectivity in Fungal Communities Between Manure and Mineral Fertilizers: A Study in an Alkaline Soil After 30 Years Fertilization
journal, October 2018
- Wang, Ying; Ji, Hongfei; Hu, Yaxian
- Frontiers in Microbiology, Vol. 9
Interaction Between Conservation Tillage and Nitrogen Fertilization Shapes Prokaryotic and Fungal Diversity at Different Soil Depths: Evidence From a 23-Year Field Experiment in the Mediterranean Area
journal, September 2019
- Piazza, Gaia; Ercoli, Laura; Nuti, Marco
- Frontiers in Microbiology, Vol. 10
Differential mechanisms underlying responses of soil bacterial and fungal communities to nitrogen and phosphorus inputs in a subtropical forest
journal, January 2019
- Li, Yong; Tian, Dashuan; Wang, Jinsong
- PeerJ, Vol. 7