Symbiotic niche mapping reveals functional specialization by two ectomycorrhizal fungi that expands the host plant niche

Van Nuland, Michael E.; Peay, Kabir G.

doi:10.1016/j.funeco.2020.100960

Symbiotic niche mapping reveals functional specialization by two ectomycorrhizal fungi that expands the host plant niche

Journal Article · Fri Jun 05 04:00:00 EDT 2020 · Fungal Ecology

DOI:https://doi.org/10.1016/j.funeco.2020.100960· OSTI ID:1802835

Van Nuland, Michael E. ^[1]; Peay, Kabir G. ^[2]

Stanford Univ., CA (United States); OSTI
Stanford Univ., CA (United States)

Mutualisms are ubiquitous in natural systems, but less is known about how these positive interactions influence species distributions compared with antagonistic interactions, such as competition and predation. The niche concept is one useful approach for thinking about factors that shape species ranges, which we apply here towards understanding how the nature of plant-mycorrhizal symbioses change across large environmental gradients. We used a continuous niche mapping approach to examine how two ectomycorrhizal fungi (Thelephora terrestris, Suillus pungens) impact pine seedling growth across a two-dimensional soil nitrogen (N) and phosphorus (P) gradient. We found that ectomycorrhizal fungi improved plant growth most in nutrient addition treatments with highly imbalanced N:P ratios, demonstrating that mycorrhizal benefits depend on interactions between niche axes. Nevertheless, T. terrestris (highN:lowP) and S. pungens (lowN:highP) benefited plants most at opposite ends of the resource ratio spectrum, consistent with niche partitioning and functional specialization. While ectomycorrhizal fungi are often thought of as being most beneficial for nitrogen uptake, our results suggest that members of the Thelephoraceae may specialize in improving plant P uptake. Ectomycorrhizal colonization by a single fungus increased plant niche volume (calculated as convex hull volumes of plant growth response surfaces across N and P gradients) compared to non-mycorrhizal control plants and shows the overall positive effects of mutualisms on plant niche volume. Despite plant host benefits in S. pungens and T. terrestris single species treatments, the presence of both fungi together decreased plant niche volume. The lack of functional complementarity, despite functional specialization, indicates that in some environments, either fungal competition or the cost of maintaining a suboptimal mycorrhizal partner can limit the benefits of a higher quality partner. The niche mapping approach we present has the potential to answer fundamental questions about the dimensions of functional diversity in ectomycorrhizal fungi and the distributions of mycorrhizal symbioses.

View Accepted Manuscript (DOE)

Research Organization:: Stanford University, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: SC0016097

OSTI ID:: 1802835

Alternate ID(s):: OSTI ID: 1780451

Journal Information:: Fungal Ecology, Journal Name: Fungal Ecology Journal Issue: C Vol. 46; ISSN 1754-5048

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (68)

Using niche breadth theory to explain generalization in mutualisms Batstone, Rebecca T.; Carscadden, Kelly A.; Afkhami, Michelle E. Ecology, Vol. 99, Issue 5 https://doi.org/10.1002/ecy.2188	journal	March 2018
Plant-mediated partner discrimination in ectomycorrhizal mutualisms Bogar, Laura; Peay, Kabir; Kornfeld, Ari Mycorrhiza, Vol. 29, Issue 2 https://doi.org/10.1007/s00572-018-00879-7	journal	January 2019
Exploration types of ectomycorrhizae Agerer, Reinhard Mycorrhiza, Vol. 11, Issue 2 https://doi.org/10.1007/s005720100108	journal	June 2001
Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types Hobbie, Erik A.; Agerer, Reinhard Plant and Soil, Vol. 327, Issue 1-2 https://doi.org/10.1007/s11104-009-0032-z	journal	June 2009
Positive interactions in communities Bertness, Mark D.; Callaway, Ragan Trends in Ecology & Evolution, Vol. 9, Issue 5 https://doi.org/10.1016/0169-5347(94)90088-4	journal	May 1994
Conditional outcomes in mutualistic interactions Bronstein, Judith L. Trends in Ecology & Evolution, Vol. 9, Issue 6 https://doi.org/10.1016/0169-5347(94)90246-1	journal	June 1994
Inclusion of facilitation into ecological theory Bruno, John F.; Stachowicz, John J.; Bertness, Mark D. Trends in Ecology & Evolution, Vol. 18, Issue 3 https://doi.org/10.1016/S0169-5347(02)00045-9	journal	March 2003
A molecular and phylogenetic analysis of the structure and specificity of Alnus rubra ectomycorrhizal assemblages Kennedy, Peter G.; Hill, Lee T. Fungal Ecology, Vol. 3, Issue 3 https://doi.org/10.1016/j.funeco.2009.08.005	journal	August 2010
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
Stayin' alive: survival of mycorrhizal fungal propagules from 6-yr-old forest soil Nguyen, Nhu H.; Hynson, Nicole A.; Bruns, Thomas D. Fungal Ecology, Vol. 5, Issue 6 https://doi.org/10.1016/j.funeco.2012.05.006	journal	December 2012
The role of ectomycorrhizal communities in forest ecosystem processes: New perspectives and emerging concepts Courty, Pierre-Emmanuel; Buée, Marc; Diedhiou, Abdala Gamby Soil Biology and Biochemistry, Vol. 42, Issue 5 https://doi.org/10.1016/j.soilbio.2009.12.006	journal	May 2010
Functional guild classification predicts the enzymatic role of fungi in litter and soil biogeochemistry Talbot, Jennifer M.; Martin, Francis; Kohler, Annegret Soil Biology and Biochemistry, Vol. 88 https://doi.org/10.1016/j.soilbio.2015.05.006	journal	September 2015
Generalized linear mixed models: a practical guide for ecology and evolution Bolker, Benjamin M.; Brooks, Mollie E.; Clark, Connie J. Trends in Ecology & Evolution, Vol. 24, Issue 3 https://doi.org/10.1016/j.tree.2008.10.008	journal	March 2009
Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity van der Heijden, Marcel G. A.; Klironomos, John N.; Ursic, Margot Nature, Vol. 396, Issue 6706 https://doi.org/10.1038/23932	journal	November 1998
Low diversity and high host preference of ectomycorrhizal fungi in Western Amazonia, a neotropical biodiversity hotspot Tedersoo, Leho; Sadam, Ave; Zambrano, Milton The ISME Journal, Vol. 4, Issue 4 https://doi.org/10.1038/ismej.2009.131	journal	December 2009
ClassII peroxidase-encoding genes are present in a phylogenetically wide range of ectomycorrhizal fungi Bödeker, Inga T. M.; Nygren, Cajsa M. R.; Taylor, Andy F. S. The ISME Journal, Vol. 3, Issue 12 https://doi.org/10.1038/ismej.2009.77	journal	July 2009
A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment van der Heijden, Marcel GA; Bruin, Susanne de; Luckerhoff, Ludo The ISME Journal, Vol. 10, Issue 2 https://doi.org/10.1038/ismej.2015.120	journal	July 2015
Competition–colonization tradeoffs structure fungal diversity Smith, Gabriel R.; Steidinger, Brian S.; Bruns, Thomas D. The ISME Journal, Vol. 12, Issue 7 https://doi.org/10.1038/s41396-018-0086-0	journal	February 2018
Climatic controls of decomposition drive the global biogeography of forest-tree symbioses Steidinger, B. S.; Crowther, T. W.; Liang, J. Nature, Vol. 569, Issue 7756 https://doi.org/10.1038/s41586-019-1128-0	journal	May 2019
Ectomycorrhizal diversity alters growth and nutrient acquisition of grey birch (Betula populifolia) seedlings in host-symbiont culture conditions Baxter, James W.; Dighton, John New Phytologist, Vol. 152, Issue 1 https://doi.org/10.1046/j.0028-646x.2001.00245.x	journal	October 2001
The molecular revolution in ectomycorrhizal ecology: peeking into the black-box: MOLECULAR APPROACHES FOR STUDIES OF EM ECOLOGY Horton, Thomas R.; Bruns, Thomas D. Molecular Ecology, Vol. 10, Issue 8 https://doi.org/10.1046/j.0962-1083.2001.01333.x	journal	August 2001
Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? Read, D. J.; Perez-Moreno, J. New Phytologist, Vol. 157, Issue 3 https://doi.org/10.1046/j.1469-8137.2003.00704.x	journal	March 2003
Resource limitation is a driver of local adaptation in mycorrhizal symbioses Johnson, N. C.; Wilson, G. W. T.; Bowker, M. A. Proceedings of the National Academy of Sciences, Vol. 107, Issue 5 https://doi.org/10.1073/pnas.0906710107	journal	January 2010
Comparative efficiency of the mycorrhizal fungi Laccaria laccata, Hebeloma crustuliniforme and Rhizopogon species on growth of radiata pine seedlings Levett, Chu-Chou; Grace, Lynette J. New Zealand Journal of Botany, Vol. 23, Issue 3 https://doi.org/10.1080/0028825X.1985.10425346	journal	July 1985
The Evolution of Cooperation Sachs, Joel L.; Mueller, Ulrich G.; Wilcox, Thomas P. The Quarterly Review of Biology, Vol. 79, Issue 2 https://doi.org/10.1086/383541	journal	June 2004
A Symbiotic View of Life: We Have Never Been Individuals Gilbert, Scott F.; Sapp, Jan; Tauber, Alfred I. The Quarterly Review of Biology, Vol. 87, Issue 4 https://doi.org/10.1086/668166	journal	December 2012
Rethinking Mutualism Stability: Cheaters and the Evolution of Sanctions Frederickson, Megan E. The Quarterly Review of Biology, Vol. 88, Issue 4 https://doi.org/10.1086/673757	journal	December 2013
Multiple Friends with Benefits: An Optimal Mutualist Management Strategy? Moeller, Holly V.; Neubert, Michael G. The American Naturalist, Vol. 187, Issue 1 https://doi.org/10.1086/684103	journal	January 2016
Soil moisture and chemistry influence diversity of ectomycorrhizal fungal communities associating with willow along an hydrologic gradient Erlandson, Sonya R.; Savage, Jessica A.; Cavender-Bares, Jeannine M. FEMS Microbiology Ecology, Vol. 92, Issue 1 https://doi.org/10.1093/femsec/fiv148	journal	November 2015
Concluding Remarks Hutchinson, G. E. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 22, Issue 0 https://doi.org/10.1101/SQB.1957.022.01.039	journal	January 1957
Identification of 100 fundamental ecological questions Sutherland, William J.; Freckleton, Robert P.; Godfray, H. Charles J. Journal of Ecology, Vol. 101, Issue 1 https://doi.org/10.1111/1365-2745.12025	journal	December 2012
Mutualist-mediated effects on species' range limits across large geographic scales Afkhami, Michelle E.; McIntyre, Patrick J.; Strauss, Sharon Y. Ecology Letters, Vol. 17, Issue 10 https://doi.org/10.1111/ele.12332	journal	July 2014
Lack of host specificity leads to independent assortment of dipterocarps and ectomycorrhizal fungi across a soil fertility gradient Peay, Kabir G.; Russo, Sabrina E.; McGuire, Krista L. Ecology Letters, Vol. 18, Issue 8 https://doi.org/10.1111/ele.12459	journal	June 2015
Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules: MEASURING MYCORRHIZAL FUNGAL DISPERSAL Peay, Kabir G.; Schubert, Max G.; Nguyen, Nhu H. Molecular Ecology, Vol. 21, Issue 16 https://doi.org/10.1111/j.1365-294X.2012.05666.x	journal	June 2012
A strong species?area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi Peay, Kabir G.; Bruns, Thomas D.; Kennedy, Peter G. Ecology Letters, Vol. 10, Issue 6 https://doi.org/10.1111/j.1461-0248.2007.01035.x	journal	June 2007
A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi Hoeksema, Jason D.; Chaudhary, V. Bala; Gehring, Catherine A. Ecology Letters, Vol. 13, Issue 3 https://doi.org/10.1111/j.1461-0248.2009.01430.x	journal	March 2010
Nitrogen availability is a primary determinant of conifer mycorrhizas across complex environmental gradients: Effects of nitrogen on mycorrhizas Cox, Filipa; Barsoum, Nadia; Lilleskov, Erik A. Ecology Letters, Vol. 13, Issue 9 https://doi.org/10.1111/j.1461-0248.2010.01494.x	journal	June 2010
A conceptual framework for the evolution of ecological specialisation: Evolution of ecological specialisation Poisot, Timothée; Bever, James D.; Nemri, Adnane Ecology Letters, Vol. 14, Issue 9 https://doi.org/10.1111/j.1461-0248.2011.01645.x	journal	June 2011
An Evaluation of Techniques for Measuring Vesicular Arbuscular Mycorrhizal Infection in Roots Giovannetti, M.; Mosse, B. New Phytologist, Vol. 84, Issue 3 https://doi.org/10.1111/j.1469-8137.1980.tb04556.x	journal	March 1980
Effects of ectomycorrhiza on host growth and carbon balance in a semi-hydroponic cultivation system Nylund, Jan-Erik; Wallander, Hakan New Phytologist, Vol. 112, Issue 3 https://doi.org/10.1111/j.1469-8137.1989.tb00328.x	journal	July 1989
Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests: Methods Courty, Pierre-Emmanuel; Pritsch, Karin; Schloter, Michael New Phytologist, Vol. 167, Issue 1 https://doi.org/10.1111/j.1469-8137.2005.01401.x	journal	March 2005
A single European aspen (Populus tremula) tree individual may potentially harbour dozens of Cenococcum geophilum ITS genotypes and hundreds of species of ectomycorrhizal fungi: Ectomycorrhizal fungi of a single aspen tree Bahram, Mohammad; Põlme, Sergei; Kõljalg, Urmas FEMS Microbiology Ecology, Vol. 75, Issue 2 https://doi.org/10.1111/j.1574-6941.2010.01000.x	journal	November 2010
Ectomycorrhizal fungal richness declines towards the host species’ range edge Lankau, Richard A.; Keymer, Daniel P. Molecular Ecology, Vol. 25, Issue 13 https://doi.org/10.1111/mec.13628	journal	July 2016
Biogeography of ectomycorrhizal fungi associated with alders ( Alnus spp.) in relation to biotic and abiotic variables at the global scale Põlme, Sergei; Bahram, Mohammad; Yamanaka, Takashi New Phytologist, Vol. 198, Issue 4 https://doi.org/10.1111/nph.12170	journal	February 2013
The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests Phillips, Richard P.; Brzostek, Edward; Midgley, Meghan G. New Phytologist, Vol. 199, Issue 1 https://doi.org/10.1111/nph.12221	journal	April 2013
Ectomycorrhizal fungi - potential organic matter decomposers, yet not saprotrophs Lindahl, Björn D.; Tunlid, Anders New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13201	journal	December 2014
Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors Shah, Firoz; Nicolás, César; Bentzer, Johan New Phytologist, Vol. 209, Issue 4 https://doi.org/10.1111/nph.13722	journal	November 2015
Experimental soil warming shifts the fungal community composition at the alpine treeline Solly, Emily F.; Lindahl, Björn D.; Dawes, Melissa A. New Phytologist, Vol. 215, Issue 2 https://doi.org/10.1111/nph.14603	journal	May 2017
Suilloid fungi as global drivers of pine invasions Policelli, Nahuel; Bruns, Thomas D.; Vilgalys, Rytas New Phytologist, Vol. 222, Issue 2 https://doi.org/10.1111/nph.15660	journal	January 2019
Ectomycorrhizal Fungal Protein Degradation Ability Predicted by Soil Organic Nitrogen Availability Rineau, Francois; Stas, Jelle; Nguyen, Nhu H. Applied and Environmental Microbiology, Vol. 82, Issue 5 https://doi.org/10.1128/AEM.03191-15	journal	December 2015
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
Evolutionary studies of ectomycorrhizal fungi: recent advances and future directions Bruns, Thomas D.; Shefferson, Richard P. Canadian Journal of Botany, Vol. 82, Issue 8 https://doi.org/10.1139/b04-021	journal	August 2004
The Mutualistic Niche: Mycorrhizal Symbiosis and Community Dynamics Peay, Kabir G. Annual Review of Ecology, Evolution, and Systematics, Vol. 47, Issue 1 https://doi.org/10.1146/annurev-ecolsys-121415-032100	journal	November 2016
Colonization-Competition Tradeoffs as a Mechanism Driving Successional Dynamics in Ectomycorrhizal Fungal Communities Kennedy, Peter G.; Higgins, Logan M.; Rogers, Rachel H. PLoS ONE, Vol. 6, Issue 9 https://doi.org/10.1371/journal.pone.0025126	journal	September 2011
Frontiers of Ecology Thompson, John N.; Reichman, O. J.; Morin, Peter J. BioScience, Vol. 51, Issue 1 https://doi.org/10.1641/0006-3568(2001)051[0015:FOE]2.0.CO;2	journal	January 2001
Mutualism, Facilitation, and the Structure of Ecological Communities Stachowicz, John J. BioScience, Vol. 51, Issue 3 https://doi.org/10.1641/0006-3568(2001)051[0235:MFATSO]2.0.CO;2	journal	January 2001
A Trait-Based test for Habitat Filtering: Convex hull Volume Cornwell, William K.; Schwilk, Dylan W.; Ackerly, David D. Ecology, Vol. 87, Issue 6 https://doi.org/10.1890/0012-9658(2006)87[1465:ATTFHF]2.0.CO;2	journal	June 2006
The Economics of Mutualisms: Optimal Utilization of Mycorrhizal Mutualistic Partners by Plants Kummel, Miroslav; Salant, Stephen W. Ecology, Vol. 87, Issue 4 https://doi.org/10.1890/0012-9658(2006)87[892:TEOMOU]2.0.CO;2	journal	April 2006
Variation in Plant Response to Native and Exotic Arbuscular Mycorrhizal Fungi Klironomos, John N. Ecology, Vol. 84, Issue 9 https://doi.org/10.1890/02-0413	journal	September 2003
Evidence of dispersal limitation in soil microorganisms: Isolation reduces species richness on mycorrhizal tree islands Peay, Kabir G.; Garbelotto, Matteo; Bruns, Thomas D. Ecology, Vol. 91, Issue 12 https://doi.org/10.1890/09-2237.1	journal	December 2010
Causes and implications of the correlation between forest productivity and tree mortality rates Stephenson, Nathan L.; van Mantgem, Phillip J.; Bunn, Andrew G. Ecological Monographs, Vol. 81, Issue 4 https://doi.org/10.1890/10-1077.1	journal	November 2011
A single ectomycorrhizal fungal species can enable a Pinus invasion Hayward, Jeremy; Horton, Thomas R.; Pauchard, Aníbal Ecology, Vol. 96, Issue 5 https://doi.org/10.1890/14-1100.1	journal	May 2015
Can Fertilization of Soil Select Less Mutualistic Mycorrhizae? Johnson, Nancy Collins Ecological Applications, Vol. 3, Issue 4 https://doi.org/10.2307/1942106	journal	November 1993
Fecundity Allocation in Herbaceous Plants Aarssen, L. W.; Taylor, D. R. Oikos, Vol. 65, Issue 2 https://doi.org/10.2307/3545013	journal	November 1992
Is Biomass a Reliable Estimate of Plant Fitness? Younginger, Brett S.; Sirová, Dagmara; Cruzan, Mitchell B. Applications in Plant Sciences, Vol. 5, Issue 2 https://doi.org/10.3732/apps.1600094	journal	February 2017
Landscape-Scale Vegetation Change Following Fire in Point Reyes, California, USA Forrestel, Alison B.; Moritz, Max A.; Stephens, Scott L. Fire Ecology, Vol. 7, Issue 2 https://doi.org/10.4996/fireecology.0702114	journal	August 2011
Competition-function tradeoffs in ectomycorrhizal fungi Moeller, Holly V.; Peay, Kabir G. PeerJ, Vol. 4 https://doi.org/10.7717/peerj.2270	journal	January 2016
A brief introduction to mixed effects modelling and multi-model inference in ecology Harrison, Xavier A.; Donaldson, Lynda; Correa-Cano, Maria Eugenia PeerJ, Vol. 6 https://doi.org/10.7717/peerj.4794	journal	January 2018

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