Plant invasion impacts on fungal community structure and function depend on soil warming and nitrogen enrichment

Anthony, M. A.; Stinson, K. A.; Moore, J. A. M.; Frey, S. D.

doi:10.1007/s00442-020-04797-4

Plant invasion impacts on fungal community structure and function depend on soil warming and nitrogen enrichment

Journal Article · Tue Nov 03 00:00:00 EST 2020 · Oecologia

DOI:https://doi.org/10.1007/s00442-020-04797-4· OSTI ID:1747028

^[1]; Stinson, K. A. ^[2]; Moore, J. A. M. ^[3]; Frey, S. D. ^[4]

ETH Zurich (Switzerland); Univ. of New Hampshire, Durham, NH (United States)
Univ. of Massachusetts, Amherst, MA (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of New Hampshire, Durham, NH (United States)
Univ. of New Hampshire, Durham, NH (United States)

The impacts of invasive species on biodiversity may be mitigated or exacerbated by abiotic environmental changes. Invasive plants can restructure soil fungal communities with important implications for native biodiversity and nutrient cycling, yet fungal responses to invasion may depend on numerous anthropogenic stressors. In this study, we experimentally invaded a long-term soil warming and simulated nitrogen deposition experiment with the widespread invasive plant Alliaria petiolata (garlic mustard) and tested the responses of soil fungal communities to invasion, abiotic factors, and their interaction. We focused on the phytotoxic garlic mustard because it suppresses native mycorrhizae across forests of North America. We found that invasion in combination with warming, but not under ambient conditions or elevated nitrogen, significantly reduced soil fungal biomass and ectomycorrhizal relative abundances and increased relative abundances of general soil saprotrophs and fungal genes encoding for hydrolytic enzymes. These results suggest that warming potentially exacerbates fungal responses to plant invasion. Soils collected from uninvaded and invaded plots across eight forests spanning a 4 °C temperature gradient further demonstrated that the magnitude of fungal responses to invasion was positively correlated with mean annual temperature. Our study is one of the first empirical tests to show that the impacts of invasion on fungal communities depends on additional anthropogenic pressures and were greater in concert with warming than under elevated nitrogen or ambient conditions.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: National Science Foundation; USDOD Strategic Environmental Research and Development Program (SERDP); USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1747028

Journal Information:: Oecologia, Journal Name: Oecologia Journal Issue: 4 Vol. 194; ISSN 0029-8549

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

References (67)

Fungal community homogenization, shift in dominant trophic guild, and appearance of novel taxa with biotic invasion Anthony, M. A.; Frey, S. D.; Stinson, K. A. Ecosphere, Vol. 8, Issue 9 https://doi.org/10.1002/ecs2.1951	journal	September 2017
Ecology of Microbial Cellulose Degradation Ljungdahl, Lars G.; Eriksson, Karl-Erik Advances in Microbial Ecology https://doi.org/10.1007/978-1-4615-9412-3_6	book	January 1985
Effects of Exotic Plant Invasions on Soil Nutrient Cycling Processes Ehrenfeld, Joan G. Ecosystems, Vol. 6, Issue 6 https://doi.org/10.1007/s10021-002-0151-3	journal	October 2003
Climate change increases risk of plant invasion in the Eastern United States Bradley, Bethany A.; Wilcove, David S.; Oppenheimer, Michael Biological Invasions, Vol. 12, Issue 6 https://doi.org/10.1007/s10530-009-9597-y	journal	October 2009
Differences in arbuscular mycorrhizal fungal communities associated with sugar maple seedlings in and outside of invaded garlic mustard forest patches Barto, E. Kathryn; Antunes, Pedro M.; Stinson, Kristina Biological Invasions, Vol. 13, Issue 12 https://doi.org/10.1007/s10530-011-9945-6	journal	February 2011
Low allelochemical concentrations detected in garlic mustard-invaded forest soils inhibit fungal growth and AMF spore germination Cantor, Aaron; Hale, Alison; Aaron, Justin Biological Invasions, Vol. 13, Issue 12 https://doi.org/10.1007/s10530-011-9986-x	journal	March 2011
Long-term legacies and partial recovery of mycorrhizal communities after invasive plant removal Lankau, Richard A.; Bauer, Jonathan T.; Anderson, M. Rebecca Biological Invasions, Vol. 16, Issue 9 https://doi.org/10.1007/s10530-014-0642-0	journal	February 2014
Fungal communities do not recover after removing invasive Alliaria petiolata (garlic mustard) Anthony, M. A.; Stinson, K. A.; Trautwig, A. N. Biological Invasions, Vol. 21, Issue 10 https://doi.org/10.1007/s10530-019-02031-8	journal	June 2019
Nitrogen Cycles: Past, Present, and Future Galloway, J. N.; Dentener, F. J.; Capone, D. G. Biogeochemistry, Vol. 70, Issue 2 https://doi.org/10.1007/s10533-004-0370-0	journal	September 2004
Chronic nitrogen additions suppress decomposition and sequester soil carbon in temperate forests Frey, S. D.; Ollinger, S.; Nadelhoffer, K. Biogeochemistry, Vol. 121, Issue 2 https://doi.org/10.1007/s10533-014-0004-0	journal	July 2014
The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil Olsson, Pål Axel; Bååth, Erland; Jakobsen, Iver Mycological Research, Vol. 99, Issue 5 https://doi.org/10.1016/S0953-7562(09)80723-5	journal	May 1995
Appropriate experimental ecosystem warming methods by ecosystem, objective, and practicality Aronson, Emma L.; McNulty, Steven G. Agricultural and Forest Meteorology, Vol. 149, Issue 11 https://doi.org/10.1016/j.agrformet.2009.06.007	journal	November 2009
Trade-offs between gene expression, growth and phenotypic diversity in microbial populations Kim, Juhyun; Darlington, Alexander; Salvador, Manuel Current Opinion in Biotechnology, Vol. 62 https://doi.org/10.1016/j.copbio.2019.08.004	journal	April 2020
Comparison of temperature effects on soil respiration and bacterial and fungal growth rates PietikÃ¥inen, Janna; Pettersson, Marie; BÃ¥Ã¥th, Erland FEMS Microbiology Ecology, Vol. 52, Issue 1 https://doi.org/10.1016/j.femsec.2004.10.002	journal	March 2005
Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests Frey, Serita D.; Knorr, Melissa; Parrent, Jeri L. Forest Ecology and Management, Vol. 196, Issue 1 https://doi.org/10.1016/j.foreco.2004.03.018	journal	July 2004
Tree seedling responses to multiple environmental stresses: Interactive effects of soil warming, nitrogen fertilization, and plant invasion Wheeler, J. A.; Frey, S. D.; Stinson, K. A. Forest Ecology and Management, Vol. 403 https://doi.org/10.1016/j.foreco.2017.08.010	journal	November 2017
Conservation of ectomycorrhizal fungi: exploring the linkages between functional and taxonomic responses to anthropogenic N deposition Lilleskov, E. A.; Hobbie, E. A.; Horton, T. R. Fungal Ecology, Vol. 4, Issue 2 https://doi.org/10.1016/j.funeco.2010.09.008	journal	April 2011
FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild Nguyen, Nhu H.; Song, Zewei; Bates, Scott T. Fungal Ecology, Vol. 20 https://doi.org/10.1016/j.funeco.2015.06.006	journal	April 2016
Chronic nitrogen additions fundamentally restructure the soil fungal community in a temperate forest Morrison, Eric W.; Frey, Serita D.; Sadowsky, Jesse J. Fungal Ecology, Vol. 23 https://doi.org/10.1016/j.funeco.2016.05.011	journal	October 2016
Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium(III) reduction with chemiluminescence detection Braman, Robert S.; Hendrix, Steven A. Analytical Chemistry, Vol. 61, Issue 24 https://doi.org/10.1021/ac00199a007	journal	December 1989
Forest Invasibility in Communities in Southeastern New York Howard, Timothy G.; Gurevitch, Jessica; Hyatt, Laura Biological Invasions, Vol. 6, Issue 4 https://doi.org/10.1023/B:BINV.0000041559.67560.7e	journal	January 2004
Artificial climate warming positively affects arbuscular mycorrhizae but decreases soil aggregate water stability in an annual grassland Rillig, Matthias C.; Wright, Sara F.; Shaw, M. Rebecca Oikos, Vol. 97, Issue 1 https://doi.org/10.1034/j.1600-0706.2002.970105.x	journal	April 2002
The temperature response of soil microbial efficiency and its feedback to climate Frey, Serita D.; Lee, Juhwan; Melillo, Jerry M. Nature Climate Change, Vol. 3, Issue 4 https://doi.org/10.1038/nclimate1796	journal	January 2013
Negative impact of nitrogen deposition on soil buffering capacity Bowman, William D.; Cleveland, Cory C.; Halada, Ĺuboš Nature Geoscience, Vol. 1, Issue 11 https://doi.org/10.1038/ngeo339	journal	November 2008
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Quantifying the benefit of a proteome reserve in fluctuating environments Mori, Matteo; Schink, Severin; Erickson, David W. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01242-8	journal	October 2017
Environment and host as large-scale controls of ectomycorrhizal fungi van der Linde, Sietse; Suz, Laura M.; Orme, C. David L. Nature, Vol. 558, Issue 7709 https://doi.org/10.1038/s41586-018-0189-9	journal	June 2018
Soil bacterial quantification approaches coupling with relative abundances reflecting the changes of taxa Zhang, Zhaojing; Qu, Yuanyuan; Li, Shuzhen Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-05260-w	journal	July 2017
Responses of the biennial forest herb Alliaria petiolata to variation in population density, nutrient addition and light availability Meekins, J. Forrest; McCarthy, Brian C. Journal of Ecology, Vol. 88, Issue 3 https://doi.org/10.1046/j.1365-2745.2000.00461.x	journal	June 2000
Reductions in grassland species evenness increase dicot seedling invasion and spittle bug infestation Wilsey, Brian J.; Polley, H. Wayne Ecology Letters, Vol. 5, Issue 5 https://doi.org/10.1046/j.1461-0248.2002.00372.x	journal	September 2002
Climate change both facilitates and inhibits invasive plant ranges in New England Merow, Cory; Bois, Sarah Treanor; Allen, Jenica M. Proceedings of the National Academy of Sciences, Vol. 114, Issue 16 https://doi.org/10.1073/pnas.1609633114	journal	March 2017
Global rise in emerging alien species results from increased accessibility of new source pools Seebens, Hanno; Blackburn, Tim M.; Dyer, Ellie E. Proceedings of the National Academy of Sciences, Vol. 115, Issue 10 https://doi.org/10.1073/pnas.1719429115	journal	February 2018
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Long-term warming alters richness and composition of taxonomic and functional groups of arctic fungi Geml, József; Morgado, Luis N.; Semenova, Tatiana A. FEMS Microbiology Ecology, Vol. 91, Issue 8 https://doi.org/10.1093/femsec/fiv095	journal	August 2015
MycoCosm portal: gearing up for 1000 fungal genomes Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1183	journal	December 2013
Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data Bengtsson-Palme, Johan; Ryberg, Martin; Hartmann, Martin Methods in Ecology and Evolution https://doi.org/10.1111/2041-210X.12073	journal	July 2013
Influence of multiple global change drivers on terrestrial carbon storage: additive effects are common Yue, Kai; Fornara, Dario A.; Yang, Wanqin Ecology Letters, Vol. 20, Issue 5 https://doi.org/10.1111/ele.12767	journal	March 2017
Ectomycorrhizal fungal response to warming is linked to poor host performance at the boreal‐temperate ecotone Fernandez, Christopher W.; Nguyen, Nhu H.; Stefanski, Artur Global Change Biology, Vol. 23, Issue 4 https://doi.org/10.1111/gcb.13510	journal	September 2016
Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities Lekberg, Ylva; Koide, Roger T.; Rohr, Jason R. Journal of Ecology, Vol. 95, Issue 1 https://doi.org/10.1111/j.1365-2745.2006.01193.x	journal	January 2007
The invasive plant Alliaria petiolata (garlic mustard) inhibits ectomycorrhizal fungi in its introduced range Wolfe, Benjamin E.; Rodgers, Vikki L.; Stinson, Kristina A. Journal of Ecology, Vol. 96, Issue 4 https://doi.org/10.1111/j.1365-2745.2008.01389.x	journal	July 2008
The UNITE database for molecular identification of fungi - recent updates and future perspectives: Letters Abarenkov, Kessy; Henrik Nilsson, R.; Larsson, Karl-Henrik New Phytologist, Vol. 186, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.03160.x	journal	March 2010
The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota) Öpik, M.; Vanatoa, A.; Vanatoa, E. New Phytologist, Vol. 188, Issue 1 https://doi.org/10.1111/j.1469-8137.2010.03334.x	journal	June 2010
Resistance and recovery of soil microbial communities in the face of Alliaria petiolata invasions Lankau, Richard A. New Phytologist, Vol. 189, Issue 2 https://doi.org/10.1111/j.1469-8137.2010.03481.x	journal	October 2010
Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi: PCR primers for arbuscular mycorrhizal fungi Lee, Jaikoo; Lee, Sangsun; Young, J. Peter W. FEMS Microbiology Ecology, Vol. 65, Issue 2 https://doi.org/10.1111/j.1574-6941.2008.00531.x	journal	August 2008
New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities Ihrmark, Katarina; Bödeker, Inga T. M.; Cruz-Martinez, Karelyn FEMS Microbiology Ecology, Vol. 82, Issue 3 https://doi.org/10.1111/j.1574-6941.2012.01437.x	journal	July 2012
Evenness-invasibility relationships differ between two extinction scenarios in tallgrass prairie Losure, David A.; Wilsey, Brian J.; Moloney, Kirk A. Oikos, Vol. 116, Issue 1 https://doi.org/10.1111/j.2006.0030-1299.15341.x	journal	January 2007
Plant litter chemistry and microbial priming regulate the accrual, composition and stability of soil carbon in invaded ecosystems Tamura, Mioko; Tharayil, Nishanth New Phytologist, Vol. 203, Issue 1 https://doi.org/10.1111/nph.12795	journal	April 2014
Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world Melillo, J. M.; Frey, S. D.; DeAngelis, K. M. Science, Vol. 358, Issue 6359 https://doi.org/10.1126/science.aan2874	journal	October 2017
The role of multiple global change factors in driving soil functions and microbial biodiversity Rillig, Matthias C.; Ryo, Masahiro; Lehmann, Anika Science, Vol. 366, Issue 6467 https://doi.org/10.1126/science.aay2832	journal	November 2019
Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Simon, L.; Lalonde, M.; Bruns, T. D. Applied and Environmental Microbiology, Vol. 58, Issue 1 https://doi.org/10.1128/AEM.58.1.291-295.1992	journal	January 1992
rRNA Operon Copy Number Reflects Ecological Strategies of Bacteria Klappenbach, J. A.; Dunbar, J. M.; Schmidt, T. M. Applied and Environmental Microbiology, Vol. 66, Issue 4 https://doi.org/10.1128/AEM.66.4.1328-1333.2000	journal	April 2000
Fungal Traits That Drive Ecosystem Dynamics on Land Treseder, Kathleen K.; Lennon, Jay T. Microbiology and Molecular Biology Reviews, Vol. 79, Issue 2 https://doi.org/10.1128/MMBR.00001-15	journal	May 2015
Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Simon, L.; Lalonde, M.; Bruns, T. D. Applied and Environmental Microbiology, Vol. 58, Issue 1 https://doi.org/10.1128/aem.58.1.291-295.1992	journal	January 1992
Invasive Plants Rapidly Reshape Soil Properties in a Grassland Ecosystem Gibbons, Sean M.; Lekberg, Ylva; Mummey, Daniel L. mSystems, Vol. 2, Issue 2 https://doi.org/10.1128/mSystems.00178-16	journal	March 2017
Invasive Plant Suppresses the Growth of Native Tree Seedlings by Disrupting Belowground Mutualisms Stinson, Kristina A.; Campbell, Stuart A.; Powell, Jeff R. PLoS Biology, Vol. 4, Issue 5 https://doi.org/10.1371/journal.pbio.0040140	journal	April 2006
Forest Processes and Global Environmental Change: Predicting the Effects of Individual and Multiple Stressors Aber, John; Neilson, Ronald P.; McNULTY, Steve BioScience, Vol. 51, Issue 9 https://doi.org/10.1641/0006-3568(2001)051[0735:FPAGEC]2.0.CO;2	journal	January 2001
Ready or Not, Garlic Mustard Is Moving In: Alliaria petiolata as a Member of Eastern North American Forests Rodgers, Vikki L.; Stinson, Kristina A.; Finzi, Adrien C. BioScience, Vol. 58, Issue 5 https://doi.org/10.1641/B580510	journal	May 2008
Impacts of Garlic Mustard Invasion on a Forest Understory Community Stinson, Kristina; Kaufman, Sylvan; Durbin, Luke Northeastern Naturalist, Vol. 14, Issue 1 https://doi.org/10.1656/1092-6194(2007)14[73:IOGMIO]2.0.CO;2	journal	March 2007
Effect of Garlic Mustard [Alliaria petiolata (Beib. Cavara & Grande)] Extracts on Plants and Arbuscular Mycorrhizal (AM) Fungi Roberts, Karl J.; Anderson, Roger C. The American Midland Naturalist, Vol. 146, Issue 1 https://doi.org/10.1674/0003-0031(2001)146[0146:EOGMAP]2.0.CO;2	journal	July 2001
Consequences of Dominance: a Review of Evenness Effects on Local and Regional Ecosystem Processes Hillebrand, Helmut; Bennett, Danuta M.; Cadotte, Marc W. Ecology, Vol. 89, Issue 6 https://doi.org/10.1890/07-1053.1	journal	June 2008
SIMULATED ATMOSPHERIC NO ₃ ⁻ DEPOSITION INCREASES SOIL ORGANIC MATTER BY SLOWING DECOMPOSITION Zak, Donald R.; Holmes, William E.; Burton, Andrew J. Ecological Applications, Vol. 18, Issue 8 https://doi.org/10.1890/07-1743.1	journal	December 2008
Seasonal dynamics of soil respiration and N mineralization in chronically warmed and fertilized soils Contosta, A. R.; Frey, S. D.; Cooper, A. B. Ecosphere, Vol. 2, Issue 3 https://doi.org/10.1890/ES10-00133.1	journal	March 2011
Inertia in Plant Community Structure: State Changes After Cessation of Nutrient-Enrichment Stress Milchunas, D. G.; Lauenroth, W. K. Ecological Applications, Vol. 5, Issue 2 https://doi.org/10.2307/1942035	journal	May 1995
Gas exchange, growth, and defense responses of invasive Alliaria petiolata (Brassicaceae) and native Geum vernum (Rosaceae) to elevated atmospheric CO ₂ and warm spring temperatures Anderson, Laurel J.; Cipollini, Don American Journal of Botany, Vol. 100, Issue 8 https://doi.org/10.3732/ajb.1300014	journal	August 2013
Consequences of Dominance: a Review of Evenness Effects on Local and Regional Ecosystem Processes Hillebrand, Helmut; Bennett, Danuta M.; Cadotte, Marc W. Figshare https://doi.org/10.6084/m9.figshare.c.3300380.v1	collection	January 2016

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59 BASIC BIOLOGICAL SCIENCES
Arbuscular mycorrhizal fungi
ectomycorrhizal fungi
invasive species
nitrogen deposition
soil warming

Plant invasion impacts on fungal community structure and function depend on soil warming and nitrogen enrichment

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References (67)

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