Marc Buée

In temperate European forests, soil fungal communities, dominated by saprotrophic and ectomycorrhizal (ECM) species, represent almost 25% of soil organic carbon (C) in the soil. However, the decomposition dynamics of fungal necromass, the bioavailability of its associated elements and its role in soil C stabilisation remain poorly understood. We investigated how intrinsic chemical properties—particularly melanin content, nitrogen (N) and phosphorus (P) levels—influence the microbial decomposition of fungal necromass in a temperate oak forest. We compared two types of fungal necromass: Laccaria bicolor (low melanin content) and Fomitiporia robusta (high melanin content). We monitored mass loss, stoichiometric ratios and microbial enzymatic activity over a six‐month period in soil. Additionally, we analysed bacterial and fungal community structures via DNA metabarcoding, and estimated microbial biomass using qPCR during the decomposition process. The highly melanised necromass showed limited mass loss and reduced enzymatic activity, indicating greater recalcitrance. Contrasting C:P and C:N ratio profiles during the decomposition of the two types of substrate suggest that melanin plays a key role in the decomposition dynamics of the fungal necromass, while P and N do not appear to be determining factors in this process. Copiotrophic bacteria and saprotrophic fungi dominated the early stages of decomposition, while in later stages, oligotrophic bacteria and certain ECM genera became dominant. Our findings confirm that fungal necromass decomposition is strongly influenced by its intrinsic chemical properties, and particularly by its melanin content. This substrate constitutes a unique ecological niche, shaping the succession of specialised microbial guilds (i.e. the fungal necrobiome). Finally, our results highlight the significant abundance of certain fungal guilds, such as ECM fungi, raising questions about the potential role of these symbiotic fungi in the decomposition of fungal necromass or their passive, but massive, colonisation of this soil micro‐niche. Read the free Plain Language Summary for this article on the Journal blog.

Summary In European forests, most tree species form symbioses with ectomycorrhizal (EM) and arbuscular mycorrhizal (AM) fungi. The EM fungi are classified into different morphological types based on the development and structure of their extraradical mycelium. These structures could be root extensions that help trees to acquire nutrients. However, the relationship between these morphological traits and functions involved in soil nutrient foraging is still under debate. We described the composition of mycorrhizal fungal communities under 23 tree species in a wide range of climates and humus forms in Europe and investigated the exploratory types of EM fungi. We assessed the response of this tree extended phenotype to humus forms, as an indicator of the functioning and quality of forest soils. We found a significant relationship between the relative proportion of the two broad categories of EM exploration types (short- or long-distance) and the humus form, showing a greater proportion of long-distance types in the least dynamic soils. As past land-use and host tree species are significant factors structuring fungal communities, we showed this relationship was modulated by host trait (gymnosperms versus angiosperms), soil depth and past land use (farmland or forest). We propose that this potential functional trait of EM fungi be used in future studies to improve predictive models of forest soil functioning and tree adaptation to environmental nutrient conditions.

Summary: Soil fungi belonging to different functional guilds, such as saprotrophs, pathogens, and mycorrhizal symbionts, play key roles in forest ecosystems. To date, no study has compared the actual gene expression of these guilds in different forest soils. We used metatranscriptomics to study the competition for organic resources by these fungal groups in boreal, temperate, and Mediterranean forest soils. Using a dedicated mRNA annotation pipeline combined with the JGI MycoCosm database, we compared the transcripts of these three fungal guilds, targeting enzymes involved in C‐ and N mobilization from plant and microbial cell walls. Genes encoding enzymes involved in the degradation of plant cell walls were expressed at a higher level in saprotrophic fungi than in ectomycorrhizal and pathogenic fungi. However, ectomycorrhizal and saprotrophic fungi showed similarly high expression levels of genes encoding enzymes involved in fungal cell wall degradation. Transcripts for N‐related transporters were more highly expressed in ectomycorrhizal fungi than in other groups. We showed that ectomycorrhizal and saprotrophic fungi compete for N in soil organic matter, suggesting that their interactions could decelerate C cycling. Metatranscriptomics provides a unique tool to test controversial ecological hypotheses and to better understand the underlying ecological processes involved in soil functioning and carbon stabilization.

Summary: Ectomycorrhizal (EcM) fungi play a crucial role in the mineral nitrogen (N) nutrition of their host trees. While it has been proposed that several EcM species also mobilize organic N, studies reporting the EcM ability to degrade N‐containing polymers, such as chitin, remain scarce. Here, we assessed the capacity of a representative collection of 16 EcM species to acquire ¹⁵N from ¹⁵N‐chitin. In addition, we combined genomics and transcriptomics to identify pathways involved in exogenous chitin degradation between these fungal strains. Boletus edulis, Imleria badia, Suillus luteus, and Hebeloma cylindrosporum efficiently mobilized N from exogenous chitin. EcM genomes primarily contained genes encoding for the direct hydrolysis of chitin. Further, we found a significant relationship between the capacity of EcM fungi to assimilate organic N from chitin and their genomic and transcriptomic potentials for chitin degradation. These findings demonstrate that certain EcM fungal species depolymerize chitin using hydrolytic mechanisms and that endochitinases, but not exochitinases, represent the enzymatic bottleneck of chitin degradation. Finally, this study shows that the degradation of exogenous chitin by EcM fungi might be a key functional trait of nutrient cycling in forests dominated by EcM fungi.

Invasive pathogens are a major threat to forest health especially in managed forest with low diversity. The die-back of European Fraxinus spp . caused by the fungus Hymenoscyphus fraxineus is the latest example of pathogen invasion causing widespread damage. Host resistance and environment, in particular stand factors were shown to strongly impact disease severity on European ash. The fact that H. fraxineus reproduce mostly through heterothallic sexual reproduction suggest that an Allee effect could limit the mating success at low host densities, thus limiting inoculum production and disease development. Populations of H. fraxineus were monitored during the fruiting period in a network of stands across a host density gradient in forest and non-forest environment. Ash dieback, basal area of ash, density of infected ash leaf debris (rachis) and apothecia in the litter and ascospores load in the air were determined in the different environments during two years. We showed significant differences between forest and non-forest environment with ash dieback, infection rate and inoculum production higher in forest settings. Host density significantly affected disease development, with crown dieback, density of infected rachis in the litter and inoculum production increasing with host density. We also demonstrated that fruiting rate, i.e. the number of apothecia per infected rachis dry weight, is strongly dependent on infected rachis density. Inoculum production is therefore limited at low host densities. Such a component Allee effect could be important in H. fraxineus epidemiology and invasion dynamic.

Global warming is pushing populations outside their range of physiological tolerance. According to the environmental envelope framework, the most vulnerable populations occur near the climatic edge of their species' distributions. In contrast, populations from the climatic center of the species range should be relatively buffered against climate warming. We tested this latter prediction using a combination of linear mixed effects and machine learning algorithms on an extensive, citizen‐scientist generated dataset on the fruitbody productivity of the Burgundy (aka summer) truffle (Tuber aestivum Vittad.), a keystone, ectomycorrhizal tree‐symbiont occurring on a wide range of temperate climates. T. aestivum's fruitbody productivity was monitored at 3‐week resolution over up to 8 continuous years at 20 sites distributed in the climatic center of its European distribution in southwest Germany and Switzerland. We found that T. aestivum fruitbody production is more sensitive to summer drought than would be expected from the breadth of its species' climatic niche. The monitored populations occurring nearly 5°C colder than the edge of their species' climatic distribution. However, interannual fruitbody productivity (truffle mass year⁻¹) fell by a median loss of 22% for every 1°C increase in summer temperature over a site's 30‐year mean. Among the most productive monitored populations, the temperature sensitivity was even higher, with single summer temperature anomalies of 3°C sufficient to stop fruitbody production altogether. Interannual truffle productivity was also related to the phenology of host trees, with ~22 g less truffle mass for each 1‐day reduction in the length of the tree growing season. Increasing summer drought extremes are therefore likely to reduce fruiting among summer truffle populations throughout Central Europe. Our results suggest that European T. aestivum may be a mosaic of vulnerable populations, sensitive to climate‐driven declines at lower thresholds than implied by its species distribution model.

Summary: In forests, bacteria and fungi are key players in wood degradation. Still, studies focusing on bacterial and fungal successions during the decomposition process depending on the wood types (i.e. sapwood and heartwood) remain scarce. This study aimed to understand the effect of wood type on the dynamics of microbial ecological guilds in wood decomposition. Using Illumina metabarcoding, bacterial and fungal communities were monitored every 3 months for 3 years from Quercus petraea wood discs placed on forest soil. Wood density and microbial enzymes involved in biopolymer degradation were measured. We observed rapid changes in the bacterial and fungal communities and microbial ecological guilds associated with wood decomposition throughout the experiment. Bacterial and fungal succession dynamics were very contrasted between sapwood and heartwood. The initial microbial communities were quickly replaced by new bacterial and fungal assemblages in the sapwood. Conversely, some initial functional guilds (i.e. endophytes and yeasts) persisted all along the experiment in heartwood and finally became dominant, possibly limiting the development of saprotrophic fungi. Our data also suggested a significant role of bacteria in nitrogen cycle during wood decomposition.

Environmental DNA contains information on the species interaction networks that support ecosystem functions and services. Next‐generation biomonitoring proposes the use of this data to reconstruct ecological networks in real time and then compute network‐level properties to assess ecosystem change. We investigated the relevance of this proposal by assessing: (i) the replicability of DNA‐based networks in the absence of ecosystem change, and (ii) the benefits and shortcomings of community‐ and network‐level properties for monitoring change. We selected crop‐associated microbial networks as a case study because they support disease regulation services in agroecosystems and analysed their response to change in agricultural practice between organic and conventional systems. Using two statistical methods of network inference, we showed that network‐level properties, especially β‐properties, could detect change. Moreover, consensus networks revealed robust signals of interactions between the most abundant species, which differed between agricultural systems. These findings complemented those obtained with community‐level data that showed, in particular, a greater microbial diversity in the organic system. The limitations of network‐level data included (i) the very high variability of network replicates within each system; (ii) the low number of network replicates per system, due to the large number of samples needed to build each network; and (iii) the difficulty in interpreting links of inferred networks. Tools and frameworks developed over the last decade to infer and compare microbial networks are therefore relevant to biomonitoring, provided that the DNA metabarcoding data sets are large enough to build many network replicates and progress is made to increase network replicability and interpretation.