Tree growth in boreal forests is limited by nitrogen (N) availability. Most boreal forest trees form symbiotic associations with ectomycorrhizal (ECM) fungi, which improve the uptake of inorganic N and also have the capacity to decompose soil organic matter (SOM) and to mobilize organic N ('ECM decomposition'). To study the effects of 'ECM decomposition' on ecosystem carbon (C) and N balances, we performed a sensitivity analysis on a model of C and N flows between plants, SOM, saprotrophs, ECM fungi, and inorganic N stores. The analysis indicates that C and N balances were sensitive to model parameters regulating ECM biomass and decomposition. Under low N availability, the optimal C allocation to ECM fungi, above which the symbiosis switches from mutualism to parasitism, increases with increasing relative involvement of ECM fungi in SOM decomposition. Under low N conditions, increased ECM organic N mining promotes tree growth but decreases soil C storage, leading to a negative correlation between C stores above- and below-ground. The interplay between plant production and soil C storage is sensitive to the partitioning of decomposition between ECM fungi and saprotrophs. Better understanding of interactions between functional guilds of soil fungi may significantly improve predictions of ecosystem responses to environmental change.

In boreal ecosystems plant production is often limited by low availability of nitrogen. Nitrogen retention in below-ground organic pools plays an important role in restricting recirculation to plants and thereby hampers forest production. Saprotrophic fungi are commonly assigned to different decomposer strategies, but how these relate to nitrogen cycling remains to be understood. Decomposition of Scots pine needle litter was studied in axenic microcosms with the ligninolytic litter decomposing basidiomycete Gymnopus androsaceus or the stress tolerant ascomycete Chalara longipes. Changes in chemical composition were followed by 13C CP/MAS NMR spectroscopy and nitrogen dynamics was assessed by the addition of a 15N tracer. Decomposition by C. longipes resulted in nitrogen retention in non-hydrolysable organic matter, enriched in aromatic and alkylic compounds, whereas the ligninolytic G. androsaceus was able to access this pool, counteracting nitrogen retention. Our observations suggest that differences in decomposing strategies between fungal species play an important role in regulating nitrogen retention and release during litter decomposition, implying that fungal community composition may impact nitrogen cycling at the ecosystem level.

Summary Microbial communities interplay with their environment through their functional traits that can be a response or an effect on the environment. Here, we explore how a functional trait—the decomposition of organic matter, can be addressed based on genetic markers and how the expression of these markers reflect ecological strategies of two fungal litter decomposer Gymnopus androsaceus and Chalara longipes. We sequenced the genomes of these two fungi, as well as their transcriptomes at different steps of Pinus sylvestris needles decomposition in microcosms. Our results highlighted that if the gene content of the two species could indicate similar potential decomposition abilities, the expression levels of specific gene families belonging to the glycoside hydrolase category reflected contrasting ecological strategies. Actually, C. longipes, the weaker decomposer in this experiment, turned out to have a high content of genes involved in cell wall polysaccharides decomposition but low expression levels, reflecting a versatile ecology compare to the more competitive G. androsaceus with high expression levels of keystone functional genes. Thus, we established that sequential expression of genes coding for different components of the decomposer machinery indicated adaptation to chemical changes in the substrate as decomposition progressed.

Many ecology textbooks present the interaction between mycorrhizal fungi and their host plants as the archetype of symbiosis or mutualism. However, mycorrhiza drains carbon directly from the plant and also competes with the plant for soil inorganic nitrogen. We developed hypotheses based on a simple model to qualitatively investigate when, in a nitrogen-limited system, the fungal partner returns sufficient extra nitrogen to compensate for the amount of carbon allocated to it by the plant. We showed when the mycorrhizal association can be beneficial to the plant, but also when mycorrhizal immobilization of soil inorganic nitrogen can be a limitation. The amount of carbon and nitrogen that the mycorrhizal fungus can obtain from soil organic matter, by producing extracellular enzymes, is also important. Saprotrophic capability decreases the value of the fungus to the plant, as fungal uptake of soil carbon augments the use of the plant-supplied carbon and increases the fungal requirement for N. The stoichiometric mismatch between low-N soil organic matter and high-N fungal biochemistry turned out to be a bottleneck in making the fungus a net provider of additional N to the plant. The most important properties determining the usefulness to a plant of a mycorrhizal symbiont are plant nitrogen use efficiency and the amount of inorganic N taken up per unit extra fungal growth. The fraction of carbon the fungus allocates to its own growth, relative to its investment in exocellular enzymes, is also a critical property. Our results show that plants could benefit from the association with the fungus, which could explain the ubiquitous nature of this association between fungi and plants.