Ectomycorrhizal Cortinariaceae species dominate class II peroxidase gene expression in a boreal forest soil

Boreal forest ecosystems constitute a large terrestrial reservoir of carbon. In these nitrogen-limited environments, release of nutrients through decomposition of soil organic matter is of fundamental importance. Fungi, particularly saprotrophic Agaricomycetes, are thought to drive this process using lignocellulolytic enzymes to degrade plant litter. However, some ectomycorrhizal fungal lineages have retained ancestral decomposition capabilities, yet evidence of their direct involvement in decomposition under field conditions is scarce. We used metatranscriptomics to examine the involvement of ectomycorrhizal fungi in the production of class II peroxidases in the soil of a Swedish boreal forest. We compared nutrient-poor plots with more fertile ones and related the peroxidase-expressing community to the total and cellulose-degrading fungal communities. We found that overall expression of class II peroxidase genes was upregulated in nutrient-poor soil, with ectomycorrhizal species in the Cortinariaceae family accounting for most of the transcripts. Among cellulose-degrading fungi, there was a shift from saprotrophic Agaricomycetes in nutrient-rich soil to dominance by Ascomycetes under nutrient-poor conditions. Symbiosis may enable ectomycorrhizal fungi to use tree photoassimilates to drive energetically costly oxidation belowground. Ectomycorrhiza-driven oxidation may, thereby, enable trees to indirectly regulate decomposition and nutrient cycling to maintain ecosystem productivity on unfertile soils.