Ectomycorrhizal fungi take over decomposition when saprotrophs fail

Forest ecosystems change along fertility gradients, both at large climatic scales and locally, depending on mineralogy and hydrology. Changes in vegetation communities and traits along fertility gradients have been studied thoroughly, but corresponding changes in soil fungal communities are less well understood. In boreal coniferous forests, ectomycorrhizal fungi play a pivotal role, not only in tree nutrient uptake, but also in decomposition, and interact with free-living saprotrophs in complex manners.We conducted DNA-based analyses of soil fungal communities in a national forest inventory across Sweden. In a local fertility gradient, we analysed fungal decomposer traits by metatranscriptomics. In the national data set, changes in relative abundances of fungal guilds were assessed in almost 1600 sites along climate and soil fertility gradients. In the local study we sequenced mRNA from composite samples of the organic horizon in 16 plots with contrasting N content, pH and tree species. We specifically targeted expression of genes coding for cellulolytic and oxidative enzymes and analysed responsible fungal taxa.The abundance of free-living saprotrophic basidiomycetes with well-developed capacity to decompose recalcitrant organic substrates (e.g. Mycena species) declined in colder climate and in more acidic and nitrogen-poor soils. In the metatranscriptomes we found reduced expression of basidiomycete cellulase genes and indications of supressed growth of basidiomycete saprotrophs under more acidic and nitrogen poor conditions. In contrary, ectomycorrhizal species with well-developed oxidative enzyme systems, mainly members of the genus Cortinarius, increased in relative abundance towards colder climates and nitrogen-poor soils. In the metatranscriptomes, mycorrhizal Cortinarius species accounted for 60% of gene expression of extracellular peroxidases, which are central for decomposition in the boreal forest floor that is rich in lignin, melanin and tannins. Overall expression of peroxidase genes was upregulated in unfertile pine plots relative to more fertile spruce plots.Altogether, we see indications that saprotrophic basidiomycetes are severely hampered by the harsh conditions in the organic horizon of boreal forests and have major problems to maintain their role as major decomposers. When the saprotrophs fail, decomposition is instead maintained by certain ectomycorrhizal fungi, who use their direct supply of carbon from the tree roots to drive oxidative decomposition, presumably liberating tightly bound nutrients for themselves and their hosts. In line with this hypothesis, unfertile conditions trigger increased investment in oxidative enzymes. The mycorrhizal link between living roots and decomposition implies that organic matter turnover in boreal forests may be largely controlled by the trees, analogous to a strong and direct priming effect.