Explaining the large-scale diversity of soil organisms that drive biogeochemical processes—and their responses to environmental change—is critical. However, identifying consistent drivers of belowground diversity and abundance for some soil organisms at large spatial scales remains problematic. Here we investigate a major guild, the ectomycorrhizal fungi, across European forests at a spatial scale and resolution that is—to our knowledge—unprecedented, to explore key biotic and abiotic predictors of ectomycorrhizal diversity and to identify dominant responses and thresholds for change across complex environmental gradients. We show the effect of 38 host, environment, climate and geographical variables on ectomycorrhizal diversity, and define thresholds of community change for key variables. We quantify host specificity and reveal plasticity in functional traits involved in soil foraging across gradients. We conclude that environmental and host factors explain most of the variation in ectomycorrhizal diversity, that the environmental thresholds used as major ecosystem assessment tools need adjustment and that the importance of belowground specificity and plasticity has previously been underappreciated.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Canadell, J. G. et al. Contributions to accelerating atmospheric CO2 growth from economic activity, carbon intensity, and efficiency of natural sinks. Proc. Natl Acad. Sci. USA 104, 18866–18870 (2007).
Galloway, J. N. et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892 (2008).
Commission of the European Communities. Communication from the Commission to the Council, the European Parliament, the European Economic and Social Committee and the Committee of the Regions – Thematic Strategy for Soil Protection (COM(2006) 231) http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:52006DC0231 (2006).
Janssens, I. A. et al. Reduction of forest soil respiration in response to nitrogen deposition. Nat. Geosci. 3, 315–322 (2010).
Johnson, N. C. & Jansa, J. in Mycorrhizal Mediation of Soil: Fertility, Structure, and Carbon Storage (eds Johnson, N. C. et al.) 1–6 (Elsevier, Amsterdam, 2017).
van der Heijden, M. G. A., Martin, F. M., Selosse, M.-A. & Sanders, I. R. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol. 205, 1406–1423 (2015).
Averill, C., Turner, B. L. & Finzi, A. C. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505, 543–545 (2014).
Clemmensen, K. E. et al. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339, 1615–1618 (2013).
Bennett, J. A. et al. Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355, 181–184 (2017).
Terrer, C., Vicca, S., Hungate, B. A., Phillips, R. P. & Prentice, I. C. Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353, 72–74 (2016).
Smith, S. E. & Read, D. E. Mycorrhizal Symbiosis 3rd edn (Academic, London, 2008).
Veresoglou, S. D. et al. Exploring continental-scale stand health – N:P ratio relationships for European forests. New Phytol. 202, 422–430 (2014).
Jonard, M. et al. Tree mineral nutrition is deteriorating in Europe. Glob. Change Biol. 21, 418–430 (2015).
Levin, S. A. Multiple scales and the maintenance of biodiversity. Ecosystems 3, 498–506 (2000).
Lilleskov, E. A. & Parrent, J. L. Can we develop general predictive models of mycorrhizal fungal community-environment relationships? New Phytol. 174, 250–256 (2007).
Suz, L. M. et al. Environmental drivers of ectomycorrhizal communities in Europe’s temperate oak forests. Mol. Ecol. 23, 5628–5644 (2014).
Peay, K. G. & Matheny, P. B. in Molecular Mycorrhizal Symbiosis (ed. Martin, F.) 341–361 (John Wiley & Sons, Hoboken, 2016).
Cox, F., Barsoum, N., Lilleskov, E. A. & Bidartondo, M. I. Nitrogen availability is a primary determinant of conifer mycorrhizas across complex environmental gradients. Ecol. Lett. 13, 1103–1113 (2010).
Cudlin, P. et al. Fine roots and ectomycorrhizas as indicators of environmental change. Plant Biosyst. 141, 406–425 (2007).
Tedersoo, L. et al. Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol. Ecol. 21, 4160–4170 (2012).
Ostonen, I. et al. Adaptive root foraging strategies along a boreal–temperate forest gradient. New Phytol. 215, 977–991 (2017).
Kauserud, H. et al. Warming-induced shift in European mushroom fruiting phenology. Proc. Natl Acad. Sci. USA 109, 14488–14493 (2012).
Peay, K. G., Bruns, T. D., Kennedy, P. G., Bergemann, S. E. & Garbelotto, M. A strong species–area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi. Ecol. Lett. 10, 470–480 (2007).
Peay, K. G., Bidartondo, M. I. & Arnold, A. E. Not every fungus is everywhere: scaling to the biogeography of fungal–plant interactions across roots, shoots and ecosystems. New Phytol. 185, 878–882 (2010).
Suz, L. M. et al. Monitoring ectomycorrhizal fungi at large scales for science, forest management, fungal conservation and environmental policy. Ann. For. Sci. 72, 877–885 (2015).
Peay, K. G., Kennedy, P. G., Davies, S. J., Tan, S. & Bruns, T. D. Potential link between plant and fungal distributions in a dipterocarp rainforest: community and phylogenetic structure of tropical ectomycorrhizal fungi across a plant and soil ecotone. New Phytol. 185, 529–542 (2010).
Taylor, D. L. et al. A first comprehensive census of fungi in soil reveals both hyperdiversity and fine-scale niche partitioning. Ecol. Monogr. 84, 3–20 (2014).
Bahram, M., Peay, K. G. & Tedersoo, L. Local-scale biogeography and spatiotemporal variability in communities of mycorrhizal fungi. New Phytol. 205, 1454–1463 (2015).
Kennedy, P. G., Garibay-Orijel, R., Higgins, L. M. & Angeles-Arguiz, R. Ectomycorrhizal fungi in Mexican Alnus forests support the host co-migration hypothesis and continental-scale patterns in phylogeography. Mycorrhiza 21, 559–568 (2011).
Kennedy, P. G. et al. Scaling up: examining the macroecology of ectomycorrhizal fungi. Mol. Ecol. 21, 4151–4154 (2012).
Põlme, S. et al. Biogeography of ectomycorrhizal fungi associated with alders (Alnus spp.) in relation to biotic and abiotic variables at the global scale. New Phytol. 198, 1239–1249 (2013).
Talbot, J. M. et al. Endemism and functional convergence across the North American soil mycobiome. Proc. Natl Acad. Sci. USA 111, 6341–6346 (2014).
Tedersoo, L. et al. Global diversity and geography of soil fungi. Science 346, 1256688 (2014).
Molina, R. & Horton, T. R. in Mycorrhizal Networks (ed. Horton, T. R.) 1–39 (Springer Science + Business Media Dordrecht, Dordrecht, 2015).
de Witte, L. C., Rosenstock, N. P., van der Linde, S. & Braun, S. Nitrogen deposition changes ectomycorrhizal communities in Swiss beech forests. Sci. Total Environ. 605–606, 1083–1096 (2017).
Pardo, L. H. et al. Effects of nitrogen deposition and empirical nitrogen critical loads for ecoregions of the United States. Ecol. Appl. 21, 3049–3082 (2011).
Hettelingh, J.-P. et al. in Critical Loads and Dynamic Risk Assessments: Nitrogen, Acidity and Metals in Terrestrial and Aquatic Ecosystems (eds de Vries, W. et al.) 613–635 (Springer Science + Business Media Dordrecht, Dordrecht, 2015).
Reis, S. et al. From acid rain to climate change. Science 338, 1153–1154 (2012).
Lilleskov, E. A., Hobbie, E. A. & Horton, T. R. Conservation of ectomycorrhizal fungi: exploring the linkages between functional and taxonomic responses to anthropogenic N deposition. Fung. Ecol. 4, 174–183 (2011).
Hendershot, J. N., Read, Q. D., Henning, J. A., Sanders, N. J. & Classen, A. T. Consistently inconsistent drivers of microbial diversity and abundance at macroecological scales. Ecology 98, 1757–1763 (2017).
Thompson, L. R. et al. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature 551, 457–463 (2017).
Glassman, S. I. et al. A continental view of pine-associated ectomycorrhizal fungal spore banks: a quiescent functional guild with a strong biogeographic pattern. New Phytol. 205, 1619–1631 (2015).
Gardes, M. & Bruns, T. D. Community structure of ectomycorrhizal fungi in a Pinus muricata forest: above- and below-ground views. Can. J. Bot. 74, 1572–1583 (1996).
Anderson, I. C. & Cairney, J. W. G. Ectomycorrhizal fungi: exploring the mycelial frontier. FEMS Microbiol. Rev. 31, 388–406 (2007).
Buée, M., Sentausa, E. & Murat, C. in Molecular Mycorrhizal Symbiosis (ed. Martin, F.) 323–406 (John Wiley & Sons, Hoboken, 2016).
Tedersoo, L. & Nilsson, R. H. in Molecular Mycorrhizal Symbiosis (ed. Martin, F.) 299–322 (John Wiley & Sons, Hoboken, 2016).
Newton, A. C. & Haigh, J. M. Diversity of ectomycorrhizal fungi in Britain: a test of the species–area relationship, and the role of host specificity. New Phytol. 138, 619–627 (1998).
Peay, K. G. The mutualistic niche: mycorrhizal symbiosis and community dynamics. Annu. Rev. Ecol. Evol. Syst. 47, 143–164 (2016).
Taylor, A. F. S., Fransson, P. M., Högberg, P., Högberg, M. N. & Plamboeck, A. H. Species level patterns in 13C and 15N abundance of ectomycorrhizal and saprotrophic fungal sporocarps. New Phytol. 159, 757–774 (2003).
Hortal, S. et al. Role of plant–fungal nutrient trading and host control in determining the competitive success of ectomycorrhizal fungi. ISME J. 11, 2666–2676 (2017).
Tripler, C. E., Kaushal, S. S., Likens, G. E. & Walter, M. T. Patterns in potassium dynamics in forest ecosystems. Ecol. Lett. 9, 451–466 (2006).
Agerer, R. Exploration types of ectomycorrhizae. Mycorrhiza 11, 107–114 (2001).
Boddy, L. et al. Climate variation effects on fungal fruiting. Fung. Ecol. 10, 20–33 (2014).
Wallander, H. A new hypothesis to explain allocation of dry matter between mycorrhizal fungi and pine seedlings in relation to nutrient supply. Plant Soil 168, 243–248 (1995).
van Strien, A. J., Boomsluiter, M., Noordeloos, M. E., Verweij, R. J. T. & Kuyper, T. W. Woodland ectomycorrhizal fungi benefit from large-scale reduction in nitrogen deposition in the Netherlands. J. Appl. Ecol. 55, 290–298 (2018).
Arnolds, E. Decline of ectomycorrhizal fungi in Europe. Agric. Ecosyst. Environ. 35, 209–244 (1991).
Lilleskov, E. A. in The Fungal Community (eds Dighton, J. et al.) 769–801 (CRC, Boca Raton, 2005).
Kiers, T. E., Palmer, T. M., Ives, A. R., Bruno, J. F. & Bronstein, J. L. Mutualisms in a changing world: an evolutionary perspective. Ecol. Lett. 13, 1459–1474 (2010).
Bobbink, R. & Hettelingh, J.-P. in Review and Revision of Empirical Critical Loads and Dose-Response Relationships (RIVM Report 680359002) (eds Bobbink, R. & Hettelingh, J.-P.) 135–171 (Coordination Centre for Effects, National Institute for Public Health and the Environment (RIVM), Bilthoven, 2011).
Giordani, P. et al. Detecting the nitrogen critical loads on European forests by means of epiphytic lichens. A signal-to-noise evaluation. For. Ecol. Manage. 311, 29–40 (2014).
Leppänen, S. M., Salemaa, M., Smolander, A., Mäkipää, R. & Tiirola, M. Nitrogen fixation and methanotrophy in forest mosses along a N deposition gradient. Environ. Exp. Bot. 90, 62–69 (2013).
Güsewell, S. N: Pratios in terrestrial plants: variation and functional significance. New Phytol. 164, 243–266 (2004).
Cools, N. & De Vos, B. Availability and evaluation of European forest soil monitoring data in the study on the effects of air pollution on forests. iForest 4, 205–211 (2011).
Hazard, C. & Johnson, D. Does genotypic and species diversity of mycorrhizal plants and fungi affect ecosystem function? New Pythol. https://doi.org/10.1111/nph.15010 (2018).
Chen, W. et al. Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees. Proc. Natl Acad. Sci. USA 113, 8741–8746 (2016).
Ferretti, M. & Fischer, R. (eds) Forest Monitoring: Methods for Terrestrial Investigations in Europe with an Overview of North America and Asia Forest Monitoring (Developments in Environmental Science Vol. 12) (Elsevier, Amsterdam, 2013).
de Vries, W. et al. Intensive monitoring of forest ecosystems in Europe: 1. Objectives, set-up and evaluation strategy. For. Ecol. Manage. 174, 77–95 (2003).
Dirnböck, T. et al. Forest floor vegetation response to nitrogen deposition in Europe. Glob. Change Biol. 20, 429–440 (2014).
MCPFE Liaison Unit Warsaw, UNECE & FAO. State of Europe’s Forests: the MCPFE Report on Sustainable Forest Management in Europe (Ministerial Conference on the Protection of Forests in Europe, Warsaw, 2007).
Gardes, M. & Bruns, T. D. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol. Ecol. 2, 113–118 (1993).
White, T. J., Bruns, T., Lee, S. & Taylor, J. in PCR Protocols: a Guide to Methods and Applications (eds Innis, M. A. et al.) 315–322 (Academic, New York, 1990).
UNECE ICP Forests Programme Co-ordinating Centre (ed.). Manual on Methods and Critera for Harmonized Sampling, Assessment, Monitoring and Analysis of the Effects of Air Pollution on Forests (Thünen Institute for Forest Ecosystems, Eberswalde, 2016).
IUSS Working Group WRB. World Reference Base for Soil Resources 2014, Update 2015. International Soil Classification System for Naming Soils and Creating Legends for Soil Maps (World Soil Resources Reports 106) (FAO, Rome, 2015).
Eichhorn, J. et al. in Manual on Methods and Critera for Harmonized Sampling, Assessment, Monitoring and Analysis of the Effects of Air Pollution on Forests (ed. UNECE ICP Forests Programme Co-ordinating Centre) 54 (Thünen Institute for Forest Ecosystems, Eberswalde, 2016).
Rautio, P., Fürst, A., Stefan, K. & Bartels, U. in Manual on Methods and Critera for Harmonized Sampling, Assessment, Monitoring and Analysis of the Effects of Air Pollution on Forests (ed. UNECE ICP Forests Programme Co-ordinating Centre) 19 (Thünen Institute for Forest Ecosystems, Eberswalde, 2016).
Waldner, P., et al. Detection of temporal trends in atmospheric deposition of inorganic nitrogen and sulphate to forests in Europe. Atmos. Environ. 95, 363–374 (2014).
Raspe, S., Beuker, E., Preuhsler, T. & Bastrup-Birk, A. in Manual on Methods and Critera for Harmonized Sampling, Assessment, Monitoring and Analysis of the Effects of Air Pollution on Forests (ed. UNECE ICP Forests Programme Co-ordinating Centre) 35 (Thünen Institute for Forest Ecosystems, Eberswalde, 2016).
Ewing, B. & Green, P. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8, 186–194 (1998).
Kearse, M. et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012).
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2584 (2016).
Kõljalg, U. et al. Towards a unified paradigm for sequence-based identification of fungi. Mol. Ecol. 22, 5271–5277 (2013).
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).
Rinaldi, A. C., Comandini, O. & Kuyper, T. W. Ectomycorrhizal fungal diversity: separating the wheat from the chaff. Fungal Divers. 33, 1–45 (2008).
Tedersoo, L., May, T. W. & Smith, M. E. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20, 217–263 (2010).
Legendre, P. & Gallagher, E. D. Ecologically meaningful transformations for ordination of species data. Oecologia 129, 271–280 (2001).
R Core Team. R: A language and environment for statistical computing. http://www.R-project.org/ (R Foundation for Statistical Computing, Vienna, 2016).
Borcard, D., Legendre, P. & Drapeau, P. Partialling out the spatial component of ecological variation. Ecology 73, 1045–1055 (1992).
Legendre, P. & Legendre, L. Numerical Ecology 2nd edn (Springer, Amsterdam, 1998).
Blanchet, F. G., Legendre, P. & Borcard, D. Forward selection of explanatory variables. Ecology 89, 2623–2632 (2008).
Nychka, D., Furrer, R., Paige, J. & Sain, S. fields: tools for spatial data. http://www.image.ucar.edu/fields (2015).
Lee, C.-R. et al. On the post-glacial spread of human commensal Arabidopsis thaliana. Nat. Commun. 8, 14458 (2017).
Lamb, A. M. et al. Climate-driven mitochondrial selection: a test in Australian songbirds. Mol. Ecol. 27, 898–918 (2018).
Kalogirou, S. lctools: local correlation, spatial inequalities, geographically weighted regression and other tools. https://CRAN.R-project.org/package=lctools (2016).
Baker, M. E. & King, R. S. A new method for detecting and interpreting biodiversity and ecological community thresholds. Methods Ecol. Evol. 1, 25–37 (2010).
Dore, A. J. et al. Evaluation of the performance of different atmospheric chemical transport models and inter-comparison of nitrogen and sulphur deposition estimates for the UK. Atmos. Environ. 119, 131–143 (2015).
We acknowledge funding from NERC grant NE/K006339/1 to M.I.B. and C.D.L.O. Analysis was partly based on the ICP Forests PCC Database (http://icp-forests.net). ICP Forests FSCC provided the first level II soil survey data. ICP Forests PCC and observers, technicians and scientists performed long-term sampling, analyses and environmental data handling largely funded by national institutions and ministries, supported by governmental bodies, services and landowners, and partially EU-funded under Regulation (EC) No. 2152/2003 (Forest Focus), project LIFE07ENV/D/000218 (FutMon), and through SWETHRO. Co-financing for D.Ž. and T.G. was provided by P4-0107 (RS Higher Education, Science and Technology Ministry). We thank D. Devey and L. Csiba for laboratory assistance; S. Boersma, F. van der Linde, H. van der Linde, J. van der Linde, C. Gonzales, A. Lenz, R. Lenz, S. Wipf, L. Garfoot, B. Spake, W. Rimington, J. Kowal, T. Solovieva, D. Gane, M. Terrington, J. Alden, A. Otway, V. Kemp, M. Edgar, Y. Lin, A. Drew, E. Booth, P. Cachera, R. De-Kayne, J. Downie, A. Tweedy, E. Moratto, E. Ek, P. Helminen, R. Lievonen, P. Närhi, A. Ryynänen, M. Rupel, J. Draing and F. Heun for field and laboratory work; R. Castilho for bioinformatics; K.-H. Larsson, P.-A. Moreau, J. Nuytinck and M. Ryberg for taxonomy; and N. Barsoum, E. Lilleskov, D. Read and T. Kuyper for discussions throughout.
Nature thanks A. Dahlberg, P. Kennedy, F. Teste and the other anonymous reviewer(s) for their contribution to the peer review of this work.
The authors declare no competing interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data figures and tables
Extended Data Fig. 1 Global non-metric multidimensional scaling ordination of community composition.
Plots shown with host trees: brown squares, beech; blue circles, oak; green triangles, pine; yellow diamonds, spruce. Isoclines depict the forest-floor pH and arrows show the direction and strength of correlation of the most-influential environmental variables according to their R2 values (>0.4). A, MAT; B, mean minimum annual air temperature; C, growing season length; D, NH4 throughfall deposition; E, NTFD.
a, c, e, g, Analyses of individual OTU abundances in response to N:PF (a), forest-floor pH (c), KTFD (e) and MAT (g). Black symbols correspond to taxa declining with the increasing variable (z−) and open symbols depict increasing taxa (z+). Symbol size is proportional to magnitude of response (z-score). Horizontal lines represent 5th and 95th quantiles of values resulting in the largest change in taxon z-scores among 1,000 bootstrap replicates. Tree shapes indicate host generalist, conifer- or broad-leaf-specific. b, d, f, h, Community-level output of accumulated z-scores per plot is shown in response to N:PF (b), forest-floor pH (d), KTFD (f) and MAT (h).
a, c, e, g, i, Analyses in response to NTFD (a), N:PF (c), forest-floor pH (e), KTFD (g) and MAT (i). Black symbols correspond to taxa that declined with the increasing variable (z−) and open symbols depict increasing taxa (z+). Symbol size is proportional to magnitude of response (z-score). Horizontal lines represent 5th and 95th quantiles of values resulting in the largest change in taxon z-scores among 1,000 bootstrap replicates. b, d, f, h, j, The community-level output of the accumulated z-scores per plot is shown in response to NTFD (b), N:PF (d), forest-floor pH (f), KTFD (h) and MAT (j).
This file contains an html5 file with an interactive version of the Krona chart in Figure 2.
This file contains Supplementary Tables 1-2. Supplementary Table 1 contains a summary of recent large scale biogeograhical ectomycorrhiza publications and Supplementary Table 2 contains a summary of the variables measured on the ICP Forests Level II plots, that were used in this study.
About this article
Cite this article
van der Linde, S., Suz, L.M., Orme, C.D.L. et al. Environment and host as large-scale controls of ectomycorrhizal fungi. Nature 558, 243–248 (2018). https://doi.org/10.1038/s41586-018-0189-9