ABSTRACT
Fungi are among the most diverse and ecologically important kingdoms in life. However, the distributional ranges of fungi remain largely unknown as do the ecological mechanisms that shape their distributions1,2. To provide an integrated view of the spatial and seasonal dynamics of fungi, we implemented a globally distributed standardized aerial sampling of fungal spores3. The vast majority of operational taxonomic units were detected within only one climatic zone, and the spatiotemporal patterns of species richness and community composition were mostly explained by annual mean air temperature. Tropical regions hosted the highest fungal diversity except for lichenized, ericoid mycorrhizal and ectomycorrhizal fungi, which reached their peak diversity in temperate regions. The sensitivity in climatic responses was associated with phylogenetic relatedness, suggesting that large-scale distributions of some fungal groups are partially constrained by their ancestral niche. There was a strong phylogenetic signal in seasonal sensitivity, suggesting that some groups of fungi have retained their ancestral trait of sporulating for only a short period. Overall, our results show that the hyperdiverse kingdom of fungi follows globally highly predictable spatial and temporal dynamics, with seasonality in both species richness and community composition increasing with latitude. Our study reports patterns resembling those described for other major groups of organisms, thus making a major contribution to the long-standing debate on whether organisms with a microbial lifestyle follow the global biodiversity paradigms known for macroorganisms4,5.
Subject(s)
Air Microbiology , Biodiversity , DNA, Fungal , Fungi , Seasons , Spatio-Temporal Analysis , DNA, Fungal/analysis , DNA, Fungal/genetics , Fungi/genetics , Fungi/classification , Fungi/isolation & purification , Mycorrhizae/genetics , Mycorrhizae/classification , Mycorrhizae/isolation & purification , Phylogeny , Spores, Fungal/classification , Spores, Fungal/isolation & purification , Temperature , Tropical Climate , Geographic MappingABSTRACT
Unravelling how species communities change along environmental gradients requires a dual understanding: the direct responses of the species to their abiotic surroundings and the indirect variation of these responses through biotic interactions. Here, we focus on the interactive relationships between plants and their symbiotic root-associated fungi (RAF) along stressful abiotic gradients. We investigate whether variations in RAF community composition along altitudinal gradients influence plant growth at high altitudes, where both plants and fungi face harsher abiotic conditions. We established a translocation experiment between pairs of Bistorta vivipara populations across altitudinal gradients. To separate the impact of shifting fungal communities from the overall influence of changing abiotic conditions, we used a root barrier to prevent new colonization by RAF following translocation. To characterize the RAF communities, we applied DNA barcoding to the root samples. Through the utilization of joint species distribution modelling, we assessed the relationship between changes in plant functional traits resulting from experimental treatments and the corresponding changes in the RAF communities. Our findings indicate that RAF communities influence plant responses to stressful abiotic conditions. Plants translocated from low to high altitudes grew more when they were able to associate with the resident high-altitude RAF compared to those plants that were not allowed to associate with the resident RAF. We conclude that interactions with RAF impact how plants respond to stressful abiotic conditions. Our results provide experimental support that interactions with RAF improve plant stress tolerance to altitudinal stressors such as colder temperatures and less nutrient availability.
Subject(s)
Altitude , Plant Roots , Symbiosis , Plant Roots/microbiology , Plant Roots/growth & development , Symbiosis/genetics , Fungi/genetics , Plant Development/genetics , DNA Barcoding, Taxonomic , Mycorrhizae/genetics , Mycorrhizae/physiologyABSTRACT
Novel methods for sampling and characterizing biodiversity hold great promise for re-evaluating patterns of life across the planet. The sampling of airborne spores with a cyclone sampler, and the sequencing of their DNA, have been suggested as an efficient and well-calibrated tool for surveying fungal diversity across various environments. Here we present data originating from the Global Spore Sampling Project, comprising 2,768 samples collected during two years at 47 outdoor locations across the world. Each sample represents fungal DNA extracted from 24 m3 of air. We applied a conservative bioinformatics pipeline that filtered out sequences that did not show strong evidence of representing a fungal species. The pipeline yielded 27,954 species-level operational taxonomic units (OTUs). Each OTU is accompanied by a probabilistic taxonomic classification, validated through comparison with expert evaluations. To examine the potential of the data for ecological analyses, we partitioned the variation in species distributions into spatial and seasonal components, showing a strong effect of the annual mean temperature on community composition.
Subject(s)
Air Microbiology , DNA, Fungal , Spores, Fungal , DNA, Fungal/analysis , Fungi/genetics , Fungi/classification , BiodiversityABSTRACT
How the multiple facets of soil fungal diversity vary worldwide remains virtually unknown, hindering the management of this essential species-rich group. By sequencing high-resolution DNA markers in over 4000 topsoil samples from natural and human-altered ecosystems across all continents, we illustrate the distributions and drivers of different levels of taxonomic and phylogenetic diversity of fungi and their ecological groups. We show the impact of precipitation and temperature interactions on local fungal species richness (alpha diversity) across different climates. Our findings reveal how temperature drives fungal compositional turnover (beta diversity) and phylogenetic diversity, linking them with regional species richness (gamma diversity). We integrate fungi into the principles of global biodiversity distribution and present detailed maps for biodiversity conservation and modeling of global ecological processes.
Subject(s)
Ecosystem , Soil , Humans , Fungi/genetics , Phylogeny , Soil Microbiology , BiodiversityABSTRACT
Fungi are highly diverse organisms, which provide multiple ecosystem services. However, compared with charismatic animals and plants, the distribution patterns and conservation needs of fungi have been little explored. Here, we examined endemicity patterns, global change vulnerability and conservation priority areas for functional groups of soil fungi based on six global surveys using a high-resolution, long-read metabarcoding approach. We found that the endemicity of all fungi and most functional groups peaks in tropical habitats, including Amazonia, Yucatan, West-Central Africa, Sri Lanka, and New Caledonia, with a negligible island effect compared with plants and animals. We also found that fungi are predominantly vulnerable to drought, heat and land-cover change, particularly in dry tropical regions with high human population density. Fungal conservation areas of highest priority include herbaceous wetlands, tropical forests, and woodlands. We stress that more attention should be focused on the conservation of fungi, especially root symbiotic arbuscular mycorrhizal and ectomycorrhizal fungi in tropical regions as well as unicellular early-diverging groups and macrofungi in general. Given the low overlap between the endemicity of fungi and macroorganisms, but high conservation needs in both groups, detailed analyses on distribution and conservation requirements are warranted for other microorganisms and soil organisms.
Subject(s)
Mycorrhizae , Soil , Animals , Biodiversity , Ecosystem , Forests , Fungi , Humans , Plants , Soil MicrobiologyABSTRACT
Long amplicon metabarcoding has opened the door for phylogenetic analysis of the largely unknown communities of microeukaryotes in soil. Here, we amplified and sequenced the ITS and LSU regions of the rDNA operon (around 1500 bp) from grassland soils using PacBio SMRT sequencing. We tested how three different methods for generation of operational taxonomic units (OTUs) effected estimated richness and identified taxa, and how well large-scale ecological patterns associated with shifting environmental conditions were recovered in data from the three methods. The field site at Kungsängen Nature Reserve has drawn frequent visitors since Linnaeus's time, and its species rich vegetation includes the largest population of Fritillaria meleagris in Sweden. To test the effect of different OTU generation methods, we sampled soils across an abrupt moisture transition that divides the meadow community into a Carex acuta dominated plant community with low species richness in the wetter part, which is visually distinct from the mesic-dry part that has a species rich grass-dominated plant community including a high frequency of F. meleagris. We used the moisture and plant community transition as a framework to investigate how detected belowground microeukaryotic community composition was influenced by OTU generation methods. Soil communities in both moisture regimes were dominated by protists, a large fraction of which were taxonomically assigned to Ciliophora (Alveolata) while 30%-40% of all reads were assigned to kingdom Fungi. Ecological patterns were consistently recovered irrespective of OTU generation method used. However, different methods strongly affect richness estimates and the taxonomic and phylogenetic resolution of the characterized community with implications for how well members of the microeukaryotic communities can be recognized in the data.
ABSTRACT
Mushroom-forming fungi are important sources of food and medicine in many regions of the world, and their development and health are known to depend on various microbes. Recent studies have examined the structure of mushroom-inhabiting bacterial (MIB) communities and their association with local environmental variables, but global-scale diversity and determinants of these communities remain poorly understood. Here we examined the MIB global diversity and community composition in relation to climate, soil and host factors. We found a core global mushroom microbiome, accounting for 30% of sequence reads, while comprising a few bacterial genera such as Halomonas, Serratia, Bacillus, Cutibacterium, Bradyrhizobium and Burkholderia. Our analysis further revealed an important role of host phylogeny in shaping the communities of MIB, whereas the effects of climate and soil factors remained negligible. The results suggest that the communities of MIB and free-living bacteria are structured by contrasting community assembly processes and that fungal-bacterial interactions are an important determinant of MIB community structure.
Subject(s)
Agaricales , Microbiota , Agaricales/genetics , Bacteria/genetics , Fungi/genetics , Phylogeny , Soil MicrobiologyABSTRACT
Forests and woodlands in the West African Guineo-Sudanian transition zone contain many tree species that form symbiotic interactions with ectomycorrhizal (ECM) fungi. These fungi facilitate plant growth by increasing nutrient and water uptake and include many fruiting body-forming fungi, including some edible mushrooms. Despite their importance for ecosystem functioning and anthropogenic use, diversity and distribution of ECM fungi is severely under-documented in West Africa. We conducted a broad regional sampling across five West African countries using soil eDNA to characterize the ECM as well as the total soil fungal community in gallery forests and savanna woodlands dominated by ECM host tree species. We subsequently sequenced the entire ITS region and much of the LSU region to infer a phylogeny for all detected soil fungal species. Utilizing a long read sequencing approach allows for higher taxonomic resolution by using the full ITS region, while the highly conserved LSU gene allows for a more accurate higher-level assignment of species hypotheses, including species without ITS-based taxonomy assignments. We detect no overall difference in species richness between gallery forests and woodlands. However, additional gallery forest plots and more samples per plot would have been needed to firmly conclude this pattern. Based on both abundance and richness, species from the families Russulaceae and Inocybaceae dominate the ECM fungal soil communities across both vegetation types. The community structure of both total soil fungi and ECM fungi was significantly influenced by vegetation types and showed strong correlation within plots. However, we found no significant difference in fungal community structure between samples collected adjacent to different host tree species within each plot. We conclude that within plots, the fungal community is structured more by the overall ECM host plant community than by the species of the individual host tree that each sample was collected from.
ABSTRACT
Fungi form diverse communities and play essential roles in many terrestrial ecosystems, yet there are methodological challenges in taxonomic and phylogenetic placement of fungi from environmental sequences. To address such challenges, we investigated spatiotemporal structure of a fungal community using soil metabarcoding with four different sequencing strategies: short-amplicon sequencing of the ITS2 region (300-400 bp) with Illumina MiSeq, Ion Torrent Ion S5 and PacBio RS II, all from the same PCR library, as well as long-amplicon sequencing of the full ITS and partial LSU regions (1200-1600 bp) with PacBio RS II. Resulting community structure and diversity depended more on statistical method than sequencing technology. The use of long-amplicon sequencing enables construction of a phylogenetic tree from metabarcoding reads, which facilitates taxonomic identification of sequences. However, long reads present issues for denoising algorithms in diverse communities. We present a solution that splits the reads into shorter homologous regions prior to denoising, and then reconstructs the full denoised reads. In the choice between short and long amplicons, we suggest a hybrid approach using short amplicons for sampling breadth and depth, and long amplicons to characterize the local species pool for improved identification and phylogenetic analyses.
Subject(s)
DNA Barcoding, Taxonomic , Fungi , Mycobiome , Phylogeny , DNA, Fungal/genetics , DNA, Ribosomal Spacer/genetics , Ecosystem , Fungi/classification , Fungi/genetics , High-Throughput Nucleotide Sequencing , Spatio-Temporal AnalysisABSTRACT
Despite increasing knowledge on host-associated microbiomes, little is known about mechanisms underlying fungus-microbiome interactions. This study aimed to examine the relative importance of host genetic, geographic and environmental variations in structuring fungus-associated microbiomes. We analyzed the taxonomic composition and function of microbiomes inhabiting fungal fruiting-bodies in relation to host genetic variation, soil pH and geographic distance between samples. For this, we sequenced the metagenomes of 40 fruiting-bodies collected from six fairy rings (i.e., genets) of a saprotrophic fungus Marasmius oreades. Our analyses revealed that fine genetic variations between host fungi could strongly affect their associated microbiome, explaining, respectively, 25% and 37% of the variation in microbiome structure and function, whereas geographic distance and soil pH remained of secondary importance. These results, together with the smaller genome size of fungi compared to other eukaryotes, suggest that fruiting-bodies are suitable for further genome-centric studies on host-microbiome interactions.
Subject(s)
Ascomycota/genetics , Ascomycota/physiology , Fruiting Bodies, Fungal/physiology , Genetic Variation , Microbiota , Soil MicrobiologyABSTRACT
Mycorrhizal associations are widespread in high-latitude ecosystems and are potentially of great importance for global carbon dynamics. Although large herbivores play a key part in shaping subarctic plant communities, their impact on mycorrhizal dynamics is largely unknown. We measured extramatrical mycelial (EMM) biomass during one growing season in 16-year-old herbivore exclosures and unenclosed control plots (ambient), at three mountain birch forests and two shrub heath sites, in the Scandes forest-tundra ecotone. We also used high-throughput amplicon sequencing for taxonomic identification to investigate differences in fungal species composition. At the birch forest sites, EMM biomass was significantly higher in exclosures (1.36 ± 0.43 g C/m2) than in ambient conditions (0.66 ± 0.17 g C/m2) and was positively influenced by soil thawing degree-days. At the shrub heath sites, there was no significant effect on EMM biomass (exclosures: 0.72 ± 0.09 g C/m2; ambient plots: 1.43 ± 0.94). However, EMM biomass was negatively related to Betula nana abundance, which was greater in exclosures, suggesting that grazing affected EMM biomass positively. We found no significant treatment effects on fungal diversity but the most abundant ectomycorrhizal lineage/cortinarius, showed a near-significant positive effect of herbivore exclusion (p = .08), indicating that herbivory also affects fungal community composition. These results suggest that herbivory can influence fungal biomass in highly context-dependent ways in subarctic ecosystems. Considering the importance of root-associated fungi for ecosystem carbon balance, these findings could have far-reaching implications.