Functional ecology of ectomycorrhizal fungi: peroxidases, decomposition, spatial community patterns

Boreal forest ecosystems constitute a globally important carbon (C) sink, due to accumulation of complex organic matter, persistent to decomposition. Nitrogen (N) is immobilized in these complex compounds and, thereby, unavailable to the plant community. Fungal peroxidases (ClassII) are oxidative enzymes, predominantly studied in white-rot wood decomposers and known to efficiently mineralize phenolic complexes, such as lignin, to CO2. Peroxidase activity is also commonly measured in forest soil, where typical white-rotters are absent and ectomycorrhizal fungi predominate. Peroxidase activity is known to increases under low inorganic N availability. The aim of this study was to explore the ectomycorrhizal decomposer potential in boreal forest ecosystems. The central hypothesis is that ectomycorrhizal fungi produce ClassII peroxidases to mobilize N, bound to phenolic complexes in boreal forest litter and humus. Genes coding for ClassII peroxidases were found to be widely spread among ectomycorrhizal taxa, particularly within the genus of Cortinarius. Gene transcription of peroxidases in forest humus could be linked directly to the species Cortinarius semisanguineus. In a field experiment, colorimetric enzyme assays showed a halving of peroxidase activity in short-term response to N-amendment. In non-treated control samples, Cortinarius species and other rhizomorph forming ectomycorrhizal fungi were co-localized with peroxidase activity hotspots. Ectomycorrhizal Cortinarius species may, thus, be key players in N-acquisition, from organic macromolecules, and central decomposers of complex organic matter in boreal forest ecosystems. Root-associated fungi, including ectomycorrhizal ones, were able to compete with free-living saprotrophs for colonization of litter. However, they were less efficient decomposers than specialized litter saprotrophs. It is concluded that some mycorrhizal fungi may release C while foraging for N. They may also indirectly act to preserve soil C by suppressing more efficient saprotrophic decomposers. The findings highlight ectomycorrhizal fungi as central regulators of C dynamics in boreal forests. Ectomycorrhizal symbiosis, thus, constitutes a direct link between above-ground photosynthesis and below-ground decomposition.