Summary: Ectomycorrhizal fungi are thought to have a key role in mobilizing organic nitrogen that is trapped in soil organic matter (SOM). However, the extent to which ectomycorrhizal fungi decompose SOM and the mechanism by which they do so remain unclear, considering that they have lost many genes encoding lignocellulose‐degrading enzymes that are present in their saprotrophic ancestors. Spectroscopic analyses and transcriptome profiling were used to examine the mechanisms by which five species of ectomycorrhizal fungi, representing at least four origins of symbiosis, decompose SOM extracted from forest soils. In the presence of glucose and when acquiring nitrogen, all species converted the organic matter in the SOM extract using oxidative mechanisms. The transcriptome expressed during oxidative decomposition has diverged over evolutionary time. Each species expressed a different set of transcripts encoding proteins associated with oxidation of lignocellulose by saprotrophic fungi. The decomposition ‘toolbox’ has diverged through differences in the regulation of orthologous genes, the formation of new genes by gene duplications, and the recruitment of genes from diverse but functionally similar enzyme families. The capacity to oxidize SOM appears to be common among ectomycorrhizal fungi. We propose that the ancestral decay mechanisms used primarily to obtain carbon have been adapted in symbiosis to scavenge nutrients instead.

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.

Summary: Soils in boreal forests contain large stocks of carbon. Plants are the main source of this carbon through tissue residues and root exudates. A major part of the exudates are allocated to symbiotic ectomycorrhizal fungi. In return, the plant receives nutrients, in particular nitrogen from the mycorrhizal fungi. To capture the nitrogen, the fungi must at least partly disrupt the recalcitrant organic matter–protein complexes within which the nitrogen is embedded. This disruption process is poorly characterized. We used spectroscopic analyses and transcriptome profiling to examine the mechanism by which the ectomycorrhizal fungus Paxillus involutus degrades organic matter when acquiring nitrogen from plant litter. The fungus partially degraded polysaccharides and modified the structure of polyphenols. The observed chemical changes were consistent with a hydroxyl radical attack, involving Fenton chemistry similar to that of brown‐rot fungi. The set of enzymes expressed by Pa. involutus during the degradation of the organic matter was similar to the set of enzymes involved in the oxidative degradation of wood by brown‐rot fungi. However, Pa. involutus lacked transcripts encoding extracellular enzymes needed for metabolizing the released carbon. The saprotrophic activity has been reduced to a radical‐based biodegradation system that can efficiently disrupt the organic matter–protein complexes and thereby mobilize the entrapped nutrients. We suggest that the released carbon then becomes available for further degradation and assimilation by commensal microbes, and that these activities have been lost in ectomycorrhizal fungi as an adaptation to symbiotic growth on host photosynthate. The interdependence of ectomycorrhizal symbionts and saprophytic microbes would provide a key link in the turnover of nutrients and carbon in forest ecosystems.

Many trees form ectomycorrhizal symbiosis with fungi. During symbiosis, the tree roots supply sugar to the fungi in exchange for nitrogen, and this process is critical for the nitrogen and carbon cycles in forest ecosystems. However, the extents to which ectomycorrhizal fungi can liberate nitrogen and modify the soil organic matter and the mechanisms by which they do so remain unclear since they have lost many enzymes for litter decomposition that were present in their free-living, saprotrophic ancestors. Using time-series spectroscopy and transcriptomics, we examined the ability of two ectomycorrhizal fungi from two independently evolved ectomycorrhizal lineages to mobilize soil organic nitrogen. Both species oxidized the organic matter and accessed the organic nitrogen. The expression of those events was controlled by the availability of glucose and inorganic nitrogen. Despite those similarities, the decomposition mechanisms, including the type of genes involved as well as the patterns of their expression, differed markedly between the two species. Our results suggest that in agreement with their diverse evolutionary origins, ectomycorrhizal fungi use different decomposition mechanisms to access organic nitrogen entrapped in soil organic matter. The timing and magnitude of the expression of the decomposition activity can be controlled by the below-ground nitrogen quality and the above-ground carbon supply.

The majority of nitrogen in forest soils is found in organic matter–protein complexes. Ectomycorrhizal fungi (EMF) are thought to have a key role in decomposing and mobilizing nitrogen from such complexes. However, little is known about the mechanisms governing these processes, how they are regulated by the carbon in the host plant and the availability of more easily available forms of nitrogen sources. Here we used spectroscopic analyses and transcriptome profiling to examine how the presence or absence of glucose and/or ammonium regulates decomposition of litter material and nitrogen mobilization by the ectomycorrhizal fungus Paxillus involutus. We found that the assimilation of nitrogen and the decomposition of the litter material are triggered by the addition of glucose. Glucose addition also resulted in upregulation of the expression of genes encoding enzymes involved in oxidative degradation of polysaccharides and polyphenols, peptidases, nitrogen transporters and enzymes in pathways of the nitrogen and carbon metabolism. In contrast, the addition of ammonium to organic matter had relatively minor effects on the expression of transcripts and the decomposition of litter material, occurring only when glucose was present. On the basis of spectroscopic analyses, three major types of chemical modifications of the litter material were observed, each correlated with the expression of specific sets of genes encoding extracellular enzymes. Our data suggest that the expression of the decomposition and nitrogen assimilation processes of EMF can be tightly regulated by the host carbon supply and that the availability of inorganic nitrogen as such has limited effects on saprotrophic activities.