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 for this article on the Journal blog.

Soil microbial communities are central to ecosystem functioning, influencing organic matter decomposition, nutrient cycling, and plant nutrition. Plant microbiomes, including mycorrhizal symbioses, play a key role in plant nutrient uptake and are strongly influenced by soil management. Land-use change, agroforestry management, and landscape structure can strongly impact the composition of soil microbial communities and plant development. In France, the structure of wine-growing landscapes can be highly heterogeneous. However, the combined effects of agroforestry practices and landscape heterogeneity on soil microbial communities in viticultural systems remain poorly documented. To better understand these effects, we conducted a controlled experiment using soils collected from a vineyard and an adjacent forest within the same landscape. Specifically, we compared vineyard soil, forest soil and their mixture to assess how their associated microbiota influence vine growth, plant-driven microbiota recruitment, and microbial activities. Although physicochemical analyses showed that forest soil contained substantially higher levels of organic matter (283.7 vs 54.3 g·kg−1 dry soil) and nitrogen (13.3 vs 3.2 g·kg−1), the enzymatic activity patterns differed between soils, with vineyard and mixed soils exhibiting higher functional activity than forest soil. We found that vine growth and nitrogen status were significantly influenced by soil origin. Plants grown in mixed soil exhibited greater aboveground biomass and development (fresh weight ∼32 g·plant−1; length ∼57 cm) than those grown in vineyard soil (∼19 g·plant−1; ∼28 cm) or forest soil (25.60 g·plant−1; ∼32.16 cm). Moreover, fungal and bacterial diversity analyses revealed distinct microbial community compositions, with vineyard soils hosting taxa adapted to disturbed environments, whereas forest soils harbored greater microbial richness. Overall, these results indicate that differences in vine growth cannot be explained solely by soil organic matter content and may also reflect differences in soil microbial communities, especially in the mixed soil treatment.

Plants shape and interact continuously with their rhizospheric microbiota, which play a key role in plant health and resilience. However, plant-associated microbial community can be shaped by several factors including plant phenotype and cropping system. Thus, understanding the interplay between microbiome assembly during the onset of plant-pathogen interactions and long-lasting resistance traits in ligneous plants remains a major challenge. To date, such attempts were mainly investigated in herbaceous plants, due to their phenotypic characteristics and their short life cycle. However, only few studies have focused on the microbial structure, dynamic and their drivers in perennial ligneous plants. Ligneous plants coevolved in interaction with specific fungal and bacterial communities that differ from those of annual plants. The specificities of such ligneous plants in shaping their own functional microbial communities could be dependent on their high heterozygosis, physiological and molecular status associated to seasonality and their aging processes, root system and above-ground architectures, long-lasting climatic variations, and specific cultural practices. This article provides an overview of the specific characteristics of perennial ligneous plants that are likely to modulate symbiotic interactions in the rhizosphere, thus affecting the plant’s fitness and systemic immunity. Plant and microbial traits contributing to the establishment of plant-microbiome interactions and the adaptation of this holobiont are also discussed.

Hymenoscyphus fraxineus causes ash dieback in Europe. It overwinters on ash leaf residue (rachis) within the forest litter. In late spring, the fungus produces apothecia on the rachises and releases ascospores to infect leaves. Previous studies reported that H. fraxineus was able to produce apothecia on the rachis for 5 years after the leaf infection under artificial conditions. However, ash litter is known to decompose rapidly in situ. We therefore monitored the decomposition kinetics of ash leaf debris and the persistence of the pathogen, as well as its ability to produce apothecia in the forest litter. For this, leaves shed in autumn in stands affected by ash dieback were placed in mesh bags and left in the forest litter for 6, 18 and 30 months. At each sampling period, litter mass loss and level of colonization of the rachises by H. fraxineus were measured, as was the pathogen's ability to produce apothecia on them. Despite high fragmentation, about 14% of the rachis dry weight remained in the mesh bags after 30 months, and the pathogen retained the ability to produce apothecia on these rachises. A simulation estimating the age composition of the colonized rachises present in the litter during the fruiting period was developed from these results. It shows that the persistence of H. fraxineus in old rachises of the litter represents a reservoir of inoculum that could compensate for poor colonization of autumn leaves and revive local outbreaks after years of unfavourable weather for the development of the pathogen.

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.

Despite the critical role of microorganisms in plant and fungal residue decomposition, our understanding of their full diversity remains limited. This is due largely to the rapid microbial succession during decomposition, a scarcity of studies including multiple sampling times, and the omission of a species richness index encompassing all decay stages. To address these gaps, we conducted a meta-analysis of 12 studies, each examining bacterial and fungal communities at multiple time points during decomposition. We aimed to determine the overall microbial diversity involved in decomposition processes by aggregating microbial richness at different time points. By comparing cumulative microbial OTU (operational taxonomic unit) richness with single time point microbial richness, we show that the cumulative richness was 2–5 times greater, indicating that a high yet frequently overlooked diversity of microorganisms is involved in the decomposition process. This pattern was consistent across different organic matter types (plant and fungal residues) for both major microbial domains (bacteria and fungi). Moreover, the appearance rate of novel OTUs generally decreased over time for most organic matter types, except for dead wood, which accumulated new fungal OTUs at a notable pace. Our results collectively emphasize the importance of considering various microbial domains, organic matter types, and time points to successfully characterize the diversity of microorganisms involved in decomposition. Further, given the hidden cumulative number of bacterial and fungal species held within plant and fungal residues across decay stages, we propose that these substrates are crucial microbial reservoirs to include to accurately assess global terrestrial microbial diversity.

Background and AimsIn temperate forests, fungi are the main actors in leaf litter decomposition. Still, we have minimal knowledge of their influence on changes in leaf litter chemistry. Thus, we aimed to determine the main drivers behind leaf litter chemical transformation during decomposition.MethodsWe monitored the development of fungal communities, extracellular enzyme activities, and litter chemical properties during a long-term (768 days) transplantation experiment of two chemically-contrasted intraspecific oak leaf litters.ResultsInitial differences in substrate chemistry between native and transplanted Quercus petraea litters incubated at the same forest site largely persisted throughout the decomposition process, indicating that initial substrate quality constrained litter chemical transformation. The two litter types also maintained distinct fungal communities despite similar enzyme profiles. This suggests that fungi act more as constrained mediators rather than controllers of chemical changes during litter decay. Further, the litter elemental (i.e., nutrient composition) and organic (i.e., lignin and carbohydrate composition) chemistries tended respectively to diverge and converge over time between the native and transplanted litter types.ConclusionThe results highlight that leaf litter chemical transformation is a dynamic process mediated-but not oriented- by fungal communities. The factors influencing changes in leaf litter's organic and elemental chemical properties may be decoupled, with potentially contrasting consequences on forest carbon stocks and soil fertility.

Invasive pathogens are a major threat to forest health especially in managed forest with a low diversity of tree species. The dieback of Fraxinus spp. caused by the fungus Hymenoscyphus fraxineus that occurs in Europe is the latest example of pathogen invasion causing widespread damage in forests. Ash dieback severity has been shown to be strongly affected by environment, in particular by stands features such as overall tree density or proportion of ashes. 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 vegetation period in a network of stands across a host density gradient in forest and non-forest environment (hedges and small woods). 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.

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 15 N from 15 N‐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.

Major advances over the past decade in molecular ecology are providing access to soil fungal diversity in forest ecosystems worldwide, but the diverse functions and metabolic capabilities of this microbial community remain largely elusive. We conducted a field survey in montane old-growth broadleaved and conifer forests, to investigate the relationship between soil fungal diversity and functional genetic traits. To assess the extent to which variation in community composition was associated with dominant tree species (oak, spruce, and fir) and environmental variations in the old-growth forests in the Jade Dragon Snow Mountain in Yunnan Province, we applied rDNA metabarcoding. We also assessed fungal gene expression in soil using mRNA sequencing and specifically assessed the expression of genes related to organic matter decomposition and nutrient acquisition in ectomycorrhizal and saprotrophic fungi. Our taxonomic profiling revealed striking shifts in the composition of the saprotrophic and ectomycorrhizal guilds among the oak-, fir-, and spruce-dominated forests. The core fungal microbiome comprised only 20

The growing demand for renewable materials and energy leads to intensified forest management practices. Therefore, combining high forest productivity and soil carbon storage capacity with lower quantities of organic matter (OM) left on the ground to decompose represents a major challenge. Although microbial communities drive processes responsible for organic carbon stabilization in soil, we have limited knowledge of how the inputs of superficial OM affect the richness and composition of soil microbial communities. This study determined the impacts of OM removal on soil bacteria and fungi at six sites across French temperate forests using high-throughput amplicon sequencing. After three years of OM manipulation, we measured an alteration of the bacterial copiotrophic and fungal saprotrophic abundance and richness. Furthermore, aboveground OM removal reshaped microbial communities toward bacterial oligotrophic and fungal ectomycorrhizal-dominated populations, which are less efficient for OM decomposition. Finally, we proposed that understanding the response of soil microbial communities to variations in OM inputs should help anticipate future functional changes in forest ecosystems submitted to the intensification of silvicultural practices.

Plant-associated microorganisms have been shown to aid plants in coping with drought. However, the underlying mechanisms are poorly understood and there is uncertainty regarding which microbial taxa and functions are mostly involved. We explored these issues in Neotropical rainforests and identified foliar microorganisms that may play a role in drought tolerance of trees. Our objectives were to (i) test the relationship between drought tolerance traits in Neotropical trees and the diversity and composition of their foliar fungal and bacterial communities and (ii) identify leaf microbial taxa positively or negatively associated with drought tolerance traits. Our results showed that the composition of leaf fungal communities but not bacterial communities was related to drought tolerance. We identified 27 fungal amplicon sequence variants whose relative abundance covaried with drought tolerance traits. Most variants were assigned to fungal clades often described as plant pathogens and increased in abundance with drought susceptibility. This greater relative abundance of leaf pathogens in the most drought-susceptible trees might increase their vulnerability to climate change. Moreover, we identified the Strelitziana and Ochroconis fungal genera as potential candidates for future culture-dependent studies aimed at understanding and improving drought tolerance in Neotropical forests. [Formula: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .

Replacement of primary old-growth forests by secondary woodlands in threatened subtropical biomes drives important changes at the level of the overstory, understory and forest floor, but the impact on belowground microbial biodiversity is yet poorly documented. In the present study, we surveyed by metabarcoding sequencing, the diversity and composition of soil bacteria and fungi in the old-growth forest, dominated by stone oaks (Lithocarpus spp.) and in the secondary Yunnan pine woodland of an iconic site for biodiversity research, the Ailaoshan National Nature Reserve (Ailao Mountains, Yunnan province, China). We assessed the effect of forest replacement and other environmental factors, including soil horizons, soil physicochemical characteristics and seasonality (monsoon vs. dry seasons). We showed that tree composition and variation in soil properties were major drivers for both bacterial and fungal communities, with a significant influence from seasonality. Ectomycorrhizal Operational Taxonomic Units (OTUs) dominated the functional fungal guilds. Species richness and diversity of the bacterial and fungal communities were higher in the pine woodland compared to the primary Lithocarpus forest, although prominent OTUs were different. The slightly lower complexity of the microbiome in the primary forest stands likely resulted from environmental filtering under relatively stable conditions over centuries, when compared to the secondary pine woodlands. In the old-growth forest, we found a higher number of species, but that communities were homogeneously distributed, whereas in the pine woodlands, there is a slightly lower number of species present but the communities are heterogeneously distributed. The present surveys of the bacterial and fungal diversity will serve as references in future studies aiming to assess the impact of the climate change on soil microbial diversity in both old-growth forests and secondary woodlands in Ailaoshan.

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.