Ectomycorrhizal fungal communities and functional genes drive forest productivity

Mark A. Anthony, Thomas W. Crowther and Mike Dettwiler, Department of Environmental Systems Science, ETH Zürich, Zürich, Switzerland, Sietse van der Linde, Netherlands Food and Consumer Product Safety Authority, Wageningen, Netherlands, Laura Martinez-Suz, Comparative Plant and Fungal Biology, Royal Botanic Gardens, Kew, United Kingdom, Martin Bidartondo, Department of Life Sciences, Imperial College, London, United Kingdom, Filipa Cox, Department of Earth and Environmental Sciences, The University of Manchester, Manchester, United Kingdom, Marcus Schaub, Forest Dynamics, Swiss Federal Research Institute for Forest, Snow and Landscape Research (WSL), Birmensdorf, Switzerland, Pasi Rautio, Natural Resources Institute Finland, Rovaniemi, Finland, Marco Ferretti, Peter Waldner, Beat Frey and Oliver Schramm, Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Birmensdorf, Switzerland, Lars Vesterdal, Department of Geosciences and Natural Resource Management, University of Copenhagen, Copenhagen, Denmark, Bruno De Vos, Research Institute for Nature and Forest, Environment & Climate Unit, Geraardsbergen, Belgium, Nadine Eickenscheidt and Andreas Schmitz, State Agency for Nature, Environment and Consumer Protection of North Rhine-Westphalia, Recklinghausen, Germany, Henning Meesenburg, Northwest German Forest Research Station, Göttingen, Germany, Henning Andreae, Sachsenforst State Forest, Graupa, Germany, Frank Jacob, Sachenforst State Forest, Graupa, Germany, Hans-Peter Dietrich, Bavarian State Institute of Forestry, Freising, Germany, Arthur Gessler, Eidgenössische Technische Hochschule Zürich ETH, Zürich, Switzerland, Pim van den Bulk and Arjan Hensen, The Netherlands Organization for Applied Scientific Research at Petten, Petten, Netherlands, Colin Averill, Department of Environmental Systems Sciences, ETH Zürich, Zürich, Switzerland

Background/Question/Methods
Ectomycorrhizal fungi are central members of the forest fungal community, forming symbiosis with most trees in temperate and boreal forests and enhancing plant access to limiting soil nutrients. Decades of greenhouse studies have shown that tree seedlings acquire more nitrogen and grow faster in combination with specific ectomycorrhizal fungi, and that these effects are sustained when seedlings are out-planted into regenerating forests. Whether fungal effects observed between tree seedlings and individual ectomycorrhizal fungi scale up to affect the growth of mature trees and entire forests harboring diverse fungal communities remains unknown. In this study, we combined a continental set of European forest inventory data from the ICP forest network with molecular ectomycorrhizal fungal community surveys to identify potential fungal mediated effects on forest productivity and paired this alongside a tree growth response to microbiome manipulation study conducted under controlled conditions.
Results/Conclusions
We found that ectomycorrhizal fungal community composition was a key predictor of tree growth, and this effect was robust to statistically accounting for climate, nitrogen deposition, soil inorganic nitrogen availability, soil pH, and forest stand characteristics. We also linked ectomycorrhizal fungal community members with genomic functional potentials and found higher fungal energy production and inorganic nitrogen metabolism but lower organic nitrogen acquisition enzyme encoding gene proportions in fast versus slow growing forests. Lastly, we sampled soils from fast and slow growing forests and introduced their microbiomes into a sterilized growth medium to experimentally isolate microbiome effects on tree development. Consistent with our observational analysis, tree seedling growth was accelerated in tandem with microbiomes from fast growing compared to slow growing forests and was correlated with ectomycorrhizal community composition. By linking molecular community surveys and long-term forest inventory data in the field and pairing this with a microbiome manipulation study under controlled conditions, this work demonstrates an emerging link between the forest microbiome and forest productivity.