Summary The extent to which ectomycorrhizal (ECM) fungi enable plants to access organic nitrogen (N) bound in soil organic matter (SOM) and transfer this growth‐limiting nutrient to their plant host, has important implications for our understanding of plant–fungal interactions, and the cycling and storage of carbon (C) and N in terrestrial ecosystems. Empirical evidence currently supports a range of perspectives, suggesting that ECM vary in their ability to provide their host with N bound in SOM, and that this capacity can both positively and negatively influence soil C storage. To help resolve the multiplicity of observations, we gathered a group of researchers to explore the role of ECM fungi in soil C dynamics, and propose new directions that hold promise to resolve competing hypotheses and contrasting observations. In this Viewpoint, we summarize these deliberations and identify areas of inquiry that hold promise for increasing our understanding of these fundamental and widespread plant symbionts and their role in ecosystem‐level biogeochemistry.

Contents Summary68I.Introduction68II.Have ECM fungi retained genes with lignocellulolytic potential from saprotrophic ancestors?69III.Are genes with saprotrophic function expressed by ECM fungi when in symbiosis?71IV.Do transcribed enzymes operate to obtain N from SOM?71V.Is the organic N derived from SOM transferred to the plant host?71VI.Concluding remarks72Acknowledgements72References72 Summary The view that ectomycorrhizal (ECM) fungi commonly participate in the enzymatic liberation of nitrogen (N) from soil organic matter (SOM) has recently been invoked as a key mechanism governing the biogeochemical cycles of forest ecosystems. Here, we provide evidence that not all evolutionary lineages of ECM have retained the genetic potential to produce extracellular enzymes that degrade SOM, calling into question the ubiquity of the proposed mechanism. Further, we discuss several untested conditions that must be empirically validated before it is certain that any lineage of ECM fungi actively expresses extracellular enzymes in order to degrade SOM and transfer N contained therein to its host plant.

Interactions between soil nitrogen (N) availability, fungal community composition, and soil organic matter (SOM) regulate soil carbon (C) dynamics in many forest ecosystems, but context dependency in these relationships has precluded general predictive theory. We found that ectomycorrhizal (ECM) fungi with peroxidases decreased with increasing inorganic N availability across a natural inorganic N gradient in northern temperate forests, whereas ligninolytic fungal saprotrophs exhibited no response. Lignin‐derived SOM and soil C were negatively correlated with ECM fungi with peroxidases and were positively correlated with inorganic N availability, suggesting decay of lignin‐derived SOM by these ECM fungi reduced soil C storage. The correlations we observed link SOM decay in temperate forests to tradeoffs in tree N nutrition and ECM composition, and we propose SOM varies along a single continuum across temperate and boreal ecosystems depending upon how tree allocation to functionally distinct ECM taxa and environmental stress covary with soil N availability.

Plant–mycorrhizal interactions mediate plant nitrogen (N) limitation and can inform model projections of the duration and strength of the effect of increasing CO2 on plant growth. We present dendrochronological evidence of a positive, but context-dependent fertilization response of Quercus rubra L. to increasing ambient CO2 (iCO2) along a natural soil nutrient gradient in a mature temperate forest. We investigated this heterogeneous response by linking metagenomic measurements of ectomycorrhizal (ECM) fungal N-foraging traits and dendrochronological models of plant uptake of inorganic N and N bound in soil organic matter (N-SOM). N-SOM putatively enhanced tree growth under conditions of low inorganic N availability, soil conditions where ECM fungal communities possessed greater genomic potential to decay SOM and obtain N-SOM. These trees were fertilized by 38 years of iCO2. In contrast, trees occupying inorganic N rich soils hosted ECM fungal communities with reduced SOM decay capacity and exhibited neutral growth responses to iCO2. This study elucidates how the distribution of N-foraging traits among ECM fungal communities govern tree access to N-SOM and subsequent growth responses to iCO2.