Temperature affects the timing and duration of fungal fruiting patterns across major terrestrial biomes.

The Earth's ecosystems are affected by a complex interplay of biotic and abiotic factors. While global temperatures increase, associated changes in the fruiting behaviour of fungi remain unknown. Here, we analyse 6.1 million fungal fruit body (mushroom) records and show that the major terrestrial biomes exhibit similarities and differences in fruiting events. We observed one main fruiting peak in most years across all biomes. However, in boreal and temperate biomes, there was a substantial number of years with a second peak, indicating spring and autumn fruiting. Distinct fruiting peaks are spatially synchronized in boreal and temperate biomes, but less defined and longer in the humid tropics. The timing and duration of fungal fruiting were significantly related to temperature mean and variability. Temperature-dependent aboveground fungal fruiting behaviour, which is arguably also representative of belowground processes, suggests that the observed biome-specific differences in fungal phenology will change in space and time when global temperatures continue to increase.

Symbiotic status alters fungal eco-evolutionary offspring trajectories.

Despite host-fungal symbiotic interactions being ubiquitous in all ecosystems, understanding how symbiosis has shaped the ecology and evolution of fungal spores that are involved in dispersal and colonization of their hosts has been ignored in life-history studies. We assembled a spore morphology database covering over 26,000 species of free-living to symbiotic fungi of plants, insects and humans and found more than eight orders of variation in spore size. Evolutionary transitions in symbiotic status correlated with shifts in spore size, but the strength of this effect varied widely among phyla. Symbiotic status explained more variation than climatic variables in the current distribution of spore sizes of plant-associated fungi at a global scale while the dispersal potential of their spores is more restricted compared to free-living fungi. Our work advances life-history theory by highlighting how the interaction between symbiosis and offspring morphology shapes the reproductive and dispersal strategies among living forms.

eDNA metabarcoding reveals high soil fungal diversity and variation in community composition among Spanish cliffs.

Environments characterized by physical extremes harbor unique species diversity with particular adaptations. Cliffs are harsh environments for organisms but host a great diversity of specialized plants with many endemics, rare and even endangered species. It is, however, less known which fungal diversity the cliff habitats contain and whether it differs among different cliff locations. We thus sampled soil from three separate cliff locations in the North, Centre, and South of Spain and used eDNA metabarcoding to determine fungal diversity. To better understand whether cliff specialist plants may promote particular fungal communities, we have sampled soil from crevices with cliff specialist plants and no apparent plants as controls. Major lifestyles found in cliff soils were saprotrophs, and major fungal orders were Dothideomycetes, Sordariomycetes, and Eurotiomycetes, while the amount of symbiotrophic fungi was relatively low. We found no significant differences in fungal amplicon sequence variant (ASV) richness among the three sampled locations, but the sites were significantly different in their community composition and their main indicator species. Overall, there were no significant differences in fungal ASV richness or composition between soils from cliff specialist plants and soils without plants, suggesting a unique fungal diversity in cliff soils independent from specialized plants. However, preliminary findings on soils of the specialist cliff plant Sedum dasyphyllum against control soils suggest that the presence of a specialist plant may be a relevant factor affecting the specificity of the fungal community in cliff soils. Our results indicate the existence of particular cliff fungal communities in each location, and that, despite limited and poorly developed soils and harsh conditions, cliffs can harbor a great diversity of fungal species, comparable to other ecosystems of Spain. This study points out that some fungi may be cliff-specific, shaping particular communities that mediate plant adaptations to cliffs' extreme conditions.

Fungal fruit body assemblages are tougher in harsh microclimates.

Forest species are affected by macroclimate, however, the microclimatic variability can be more extreme and change through climate change. Fungal fruiting community composition was affected by microclimatic differences. Here we ask whether differences in the fruiting community can be explained by morphological traits of the fruit body, which may help endure harsh conditions. We used a dead wood experiment and macrofungal fruit body size, color, and toughness. We exposed logs of two host tree species under closed and experimentally opened forest canopies in a random-block design for four years and identified all visible fruit bodies of two fungal lineages (Basidio- and Ascomycota). We found a consistently higher proportion of tough-fleshed species in harsher microclimates under open canopies. Although significant, responses of community fruit body size and color lightness were inconsistent across lineages. We suggest the toughness-protection hypothesis, stating that tough-fleshed fruit bodies protect from microclimatic extremes by reducing dehydration. Our study suggests that the predicted increase of microclimatic harshness with climate change will likely decrease the presence of soft-fleshed fruit bodies. Whether harsh microclimates also affect the mycelium of macrofungi with different fruit body morphology would complement our findings and increase predictability under climate change.

Organic Nitrogen Supplementation Increases Vegetative and Reproductive Biomass in a Versatile White Rot Fungus.

The Black Poplar Mushroom Cyclocybe aegerita (syn. Agrocybe aegerita) is a white-rot fungus that naturally fruits from woody substrates, including buried wood. It is known for its substrate versatility and is equipped with a respective carbohydrate-active enzyme repertoire being intermediate between typical white-rot fungi and plant litter decomposers. Given relative nitrogen scarcity in wood, mobilization of nitrogen from surrounding litter is known as a way to meet nitrogen requirements for cellular homeostasis and reproduction of wood decay fungi. However, the effect of added nitrogen on vegetative and reproductive biomass has not yet been studied in a uniform minimalistic laboratory setup. For C. aegerita, such a growth and fruiting setup has been developed. In the present study, this white-rot fungus has been grown with and without additional ß-adenosine, an organic nitrogen source present in plant litter. Elevated ß-adenosine levels increased aerial mycelium weight by 30% (1 × ß-adenosine) and 55% (10 × ß-adenosine), reproductive biomass by 75% (1 × ß-adenosine) and by 100% (10 × ß-adenosine), number of primordia by 127% (10 × ß-adenosine) and accelerated primordium formation by 1.6 days (10 × ß-adenosine), compared to the control treatment. These findings imply that C. aegerita invests additional organic nitrogen resources into direct vegetative and reproductive biomass build-up at the same time. Colonization of niches with accessory nitrogen sources, like buried wood, which is near the plant litter layer, may thus provide an evolutionary fitness advantage. Globally anthropogenically altered nitrogen dynamics may affect hyphal-driven processes as well as fruit body-driven food webs.

Transcriptional response of mushrooms to artificial sun exposure.

Climate change causes increased tree mortality leading to canopy loss and thus sun-exposed forest floors. Sun exposure creates extreme temperatures and radiation, with potentially more drastic effects on forest organisms than the current increase in mean temperature. Such conditions might potentially negatively affect the maturation of mushrooms of forest fungi. A failure of reaching maturation would mean no sexual spore release and, thus, entail a loss of genetic diversity. However, we currently have a limited understanding of the quality and quantity of mushroom-specific molecular responses caused by sun exposure. Thus, to understand the short-term responses toward enhanced sun exposure, we exposed mushrooms of the wood-inhabiting forest species Lentinula edodes, while still attached to their mycelium and substrate, to artificial solar light (ca. 30°C and 100,000 lux) for 5, 30, and 60 min. We found significant differentially expressed genes at 30 and 60 min. Eukaryotic Orthologous Groups (KOG) class enrichment pointed to defense mechanisms. The 20 most significant differentially expressed genes showed the expression of heat-shock proteins, an important family of proteins under heat stress. Although preliminary, our results suggest mushroom-specific molecular responses to tolerate enhanced sun exposure as expected under climate change. Whether mushroom-specific molecular responses are able to maintain fungal fitness under opening forest canopies remains to be tested.

Stochastic Dispersal Rather Than Deterministic Selection Explains the Spatio-Temporal Distribution of Soil Bacteria in a Temperate Grassland.

Spatial and temporal processes shaping microbial communities are inseparably linked but rarely studied together. By Illumina 16S rRNA sequencing, we monitored soil bacteria in 360 stations on a 100 square meter plot distributed across six intra-annual samplings in a rarely managed, temperate grassland. Using a multi-tiered approach, we tested the extent to which stochastic or deterministic processes influenced the composition of local communities. A combination of phylogenetic turnover analysis and null modeling demonstrated that either homogenization by unlimited stochastic dispersal or scenarios, in which neither stochastic processes nor deterministic forces dominated, explained local assembly processes. Thus, the majority of all sampled communities (82%) was rather homogeneous with no significant changes in abundance-weighted composition. However, we detected strong and uniform taxonomic shifts within just nine samples in early summer. Thus, community snapshots sampled from single points in time or space do not necessarily reflect a representative community state. The potential for change despite the overall homogeneity was further demonstrated when the focus shifted to the rare biosphere. Rare OTU turnover, rather than nestedness, characterized abundance-independent ß-diversity. Accordingly, boosted generalized additive models encompassing spatial, temporal and environmental variables revealed strong and highly diverse effects of space on OTU abundance, even within the same genus. This pure spatial effect increased with decreasing OTU abundance and frequency, whereas soil moisture - the most important environmental variable - had an opposite effect by impacting abundant OTUs more than the rare ones. These results indicate that - despite considerable oscillation in space and time - the abundant and resident OTUs provide a community backbone that supports much higher ß-diversity of a dynamic rare biosphere. Our findings reveal complex interactions among space, time, and environmental filters within bacterial communities in a long-established temperate grassland.

Diversity of Trametes (Polyporales, Basidiomycota) in tropical Benin and description of new species Trametes parvispora.

Trametes is a globally distributed genus of white-rot polypores and well sampled in temperate and boreal areas. However, the diversity, taxonomy, and phylogenetic positions of Trametes spp. are poorly known in tropical Africa. This study aims at documenting the diversity of Trametes species in Benin (tropical Africa) and their phylogenetic positions with a focus on the T. elegans species complex. Therefore, we collected specimens of Trametes from different forest types across Benin. To infer phylogenetic relationships between Trametes species, we investigated sequences of five gene regions and added available sequences from GenBank. Using Maximum likelihood and Bayesian phylogeny inference methods, we found eight supported species clades. For the T. elegans species complex, we re-establish the name Trametes palisotii for species previously known as T. elegans in tropical Africa. Furthermore, we propose Trametes parvispora as a species new to science and provide the description of this species. Our molecular phylogeny of Trametes with a focus on tropical Benin contributes to taxonomic clarity of an important wood-decay fungal genus, which is the basis for biodiversity assessments of Trametes in the tropics.

Bark coverage shifts assembly processes of microbial decomposer communities in dead wood.

Bark protects living trees against environmental influences but may promote wood decomposition by fungi and bacteria after tree death. However, the mechanisms by which bark determines the assembly process and biodiversity of decomposers remain unknown. Therefore, we partially or completely removed bark from experimentally felled trees and tested with null modelling whether assembly processes were determined by bark coverage and if biodiversity of molecularly sampled fungi and bacteria generally benefited from increasing bark cover. The community composition of fungi, wood-decaying fungi (subset of all fungi) and bacteria clearly separated between completely debarked, partly debarked and control trees. Bacterial species richness was higher on control trees than on either partly or completely debarked trees, whereas the species richness of all fungi did not differ. However, the species richness of wood-decaying fungi was higher on partially and completely debarked trees than on control trees. Deterministic assembly processes were most important in completely debarked trees, a pattern consistent for fungi and bacteria. Our findings suggest that human disturbances in forests shift the dominant assembly mechanism from stochastic to deterministic processes and thus alter the diversity of wood-inhabiting microorganisms.

Radar vision in the mapping of forest biodiversity from space.

Recent progress in remote sensing provides much-needed, large-scale spatio-temporal information on habitat structures important for biodiversity conservation. Here we examine the potential of a newly launched satellite-borne radar system (Sentinel-1) to map the biodiversity of twelve taxa across five temperate forest regions in central Europe. We show that the sensitivity of radar to habitat structure is similar to that of airborne laser scanning (ALS), the current gold standard in the measurement of forest structure. Our models of different facets of biodiversity reveal that radar performs as well as ALS; median R² over twelve taxa by ALS and radar are 0.51 and 0.57 respectively for the first non-metric multidimensional scaling axes representing assemblage composition. We further demonstrate the promising predictive ability of radar-derived data with external validation based on the species composition of birds and saproxylic beetles. Establishing new area-wide biodiversity monitoring by remote sensing will require the coupling of radar data to stratified and standardized collected local species data.

European mushroom assemblages are darker in cold climates.

Thermal melanism theory states that dark-colored ectotherm organisms are at an advantage at low temperature due to increased warming. This theory is generally supported for ectotherm animals, however, the function of colors in the fungal kingdom is largely unknown. Here, we test whether the color lightness of mushroom assemblages is related to climate using a dataset of 3.2 million observations of 3,054 species across Europe. Consistent with the thermal melanism theory, mushroom assemblages are significantly darker in areas with cold climates. We further show differences in color phenotype between fungal lifestyles and a lifestyle differentiated response to seasonality. These results indicate a more complex ecological role of mushroom colors and suggest functions beyond thermal adaption. Because fungi play a crucial role in terrestrial carbon and nutrient cycles, understanding the links between the thermal environment, functional coloration and species' geographical distributions will be critical in predicting ecosystem responses to global warming.

rMyCoPortal - an R package to interface with the Mycology Collections Portal.

The understanding of the biodiversity and biogeographical distribution of fungi is still limited. The small number of online databases and the large effort required to access existing data have prevented their use in research articles. The Mycology Collections Portal was established in 2012 to help alleviate these issues and currently serves data online for over 4.3 million fungal records. However, the current process for accessing the data through the web interface is manual, therefore slow, and precludes the extensive use of the existing datasets. Here we introduce the software package rMyCoPortal, which allows users rapid, automated access to the data. rMyCoPortal makes data readily available for further computations and analyses in the open source statistical programming environment R. We will demonstrate the core functions of the package, and how rMyCoPortal can be employed to obtain fungal data that can be used to address basic research questions. rMyCoPortal is a free and open-source R package, available via GitHub.

Evolutionary dynamics of host specialization in wood-decay fungi.

BACKGROUND: The majority of wood decomposing fungi are mushroom-forming Agaricomycetes, which exhibit two main modes of plant cell wall decomposition: white rot, in which all plant cell wall components are degraded, including lignin, and brown rot, in which lignin is modified but not appreciably removed. Previous studies suggested that brown rot fungi tend to be specialists of gymnosperm hosts and that brown rot promotes gymnosperm specialization. However, these hypotheses were based on analyses of limited datasets of Agaricomycetes. Overcoming this limitation, we used a phylogeny with 1157 species integrating available sequences, assembled decay mode characters from the literature, and coded host specialization using the newly developed R package, rusda. RESULTS: We found that most brown rot fungi are generalists or gymnosperm specialists, whereas most white rot fungi are angiosperm specialists. A six-state model of the evolution of host specialization revealed high transition rates between generalism and specialization in both decay modes. However, while white rot lineages switched most frequently to angiosperm specialists, brown rot lineages switched most frequently to generalism. A time-calibrated phylogeny revealed that Agaricomycetes is older than the flowering plants but many of the large clades originated after the diversification of the angiosperms in the Cretaceous. CONCLUSIONS: Our results challenge the current view that brown rot fungi are primarily gymnosperm specialists and reveal intensive white rot specialization to angiosperm hosts. We thus suggest that brown rot associated convergent loss of lignocellulose degrading enzymes was correlated with host generalism, rather than gymnosperm specialism. A likelihood model of host specialization evolution together with a time-calibrated phylogeny further suggests that the rise of the angiosperms opened a new mega-niche for wood-decay fungi, which was exploited particularly well by white rot lineages.