Local adaptation to soil hypoxia determines the structure of an arbuscular mycorrhizal fungal community in roots from natural CO₂ springs

The processes responsible for producing and maintaining the diversity of natural arbuscular mycorrhizal (AM) fungal communities remain largely unknown. We used natural CO(2) springs (mofettes), which create hypoxic soil environments, to determine whether a long-term, directional, abiotic selection pressure could change AM fungal community structure and drive the selection of particular AM fungal phylotypes. We explored whether those phylotypes that appear exclusively in hypoxic soils are local specialists or widespread generalists able to tolerate a range of soil conditions. AM fungal community composition was characterized by cloning, restriction fragment length polymorphism typing, and the sequencing of small subunit rRNA genes from roots of four plant species growing at high (hypoxic) and low (control) geological CO(2) exposure. We found significant levels of AM fungal community turnover (β diversity) between soil types and the numerical dominance of two AM fungal phylotypes in hypoxic soils. Our results strongly suggest that direct environmental selection acting on AM fungi is a major factor regulating AM fungal communities and their phylogeographic patterns. Consequently, some AM fungi are more strongly associated with local variations in the soil environment than with their host plant's distribution.     

Extremotolerance in fungi: evolution on the edge

Our planet offers many opportunities for life on the edge: high and low temperatures, high salt concentrations, acidic and basic conditions and toxic environments, to name but a few extremes. Recent studies have revealed the diversity of fungi that can occur in stressful environments that are hostile to most eukaryotes. We review these studies here, with the additional purpose of proposing some mechanisms that would allow for the evolutionary adaptation of eukaryotic microbial life under extreme conditions. We focus, in particular, on life in ice and life at high salt concentrations, as there is a surprising similarity between the fungal populations in these two kinds of environments, both of which are characterized by low water activity. We propose steps of evolution of generalist species towards the development of specialists in extreme habitats. We argue that traits present in some fungal groups, such as asexuality, synthesis of melanin-like pigments and a flexible morphology, are preadaptations that facilitate persistence and eventual adaptation to conditions on the ecological edge, as well as biotope switches. These processes are important for understanding the evolution of extremophiles; moreover, they have implications for the emergence of novel fungal pathogens.     

Diversity and community structure of ectomycorrhizal fungi in a wooded meadow

Wooded meadows are seminatural plant communities that support high diversity of various taxa. Due to changes in land use, wooded meadows have severely declined during the last century. The dominant trees in wooded meadows acquire mineral nutrients via ectomycorrhizal fungi. Using anatomotyping and sequencing of root tips, interpolation and extrapolation methods, we studied the diversity and community structure of ectomycorrhizal fungi in two soil horizons of both managed and forested parts of a wooded meadow in Estonia. Species of Thelephoraceae, Sebacinaceae and the genus Inocybe dominated the whole ectomycorrhizal fungal community of 172 observed species. Forested and managed parts of the wooded meadow harboured different communities of ectomycorrhizal fungi, whereas soil horizon had a negligible effect on the fungal community composition. Diverse soil conditions and host trees likely support the high richness of ectomycorrhizal fungi in the wooded meadow ecosystem. Direct sequencing integrated with interpolation and extrapolation methods are promising to identify the fungi at the species level and to compare species richness between communities of ectomycorrhizal fungi.     

Biogenic Mn-Oxides in Subseafloor Basalts

The deep biosphere of the subseafloor basalts is recognized as a major scientific frontier in disciplines like biology, geology, and oceanography. Recently, the presence of fungi in these environments has involved a change of view regarding diversity and ecology. Here, we describe fossilized fungal communities in vugs in subseafloor basalts from a depth of 936.65 metres below seafloor at the Detroit Seamount, Pacific Ocean. These fungal communities are closely associated with botryoidal Mn oxides composed of todorokite. Analyses of the Mn oxides by Electron Paramagnetic Resonance spectroscopy (EPR) indicate a biogenic signature. We suggest, based on mineralogical, morphological and EPR data, a biological origin of the botryoidal Mn oxides. Our results show that fungi are involved in Mn cycling at great depths in the seafloor and we introduce EPR as a means to easily identify biogenic Mn oxides in these environments.     

Genotype identity determines productivity and CO2 efflux across a genotype-species gradient of ectomycorrhizal fungi

Ectomycorrhizal (EM) fungal communities are taxonomically diverse, and independent manipulation of both intra- and interspecific diversity has previously been shown to positively influence the productivity and activity of EM fungi. Here, we combine manipulations of intra- and interspecific richness and test the effects of a genotype-species gradient on the biomass production and respiration of EM fungi in vitro. Genotype identity had the most pronounced effect on fungal productivity, and in some cases variation within species was greater than between species. We found small negative effects of both species and genotype richness on biomass production, CO₂ efflux and the final nitrogen (N) content of the fungal communities corresponding to mixed negative selection and complementarity effects. Our study highlights the degree of variability between individual EM fungi at the genotype level, and consequently emphasises the importance of individual genotypes for playing key roles in shaping belowground community functioning.     

Evolutionary maintenance of genomic diversity within arbuscular mycorrhizal fungi

Most organisms are built from a single genome. In striking contrast, arbuscular mycorrhizal fungi appear to maintain genomic variation within an individual fungal network. Arbuscular mycorrhizal fungi dwell in the soil, form mutualistic networks with plants, and bear multiple, potentially genetically diverse nuclei within a network. We explore, from a theoretical perspective, why such genetic diversity might be maintained within individuals. We consider selection acting within and between individual fungal networks. We show that genetic diversity could provide a benefit at the level of the individual, by improving growth in variable environments, and that this can stabilize genetic diversity even in the presence of nuclear conflict. Arbuscular mycorrhizal fungi complicate our understanding of organismality, but our findings offer a way of understanding such biological anomalies.     

Fungal sporocarps house diverse and host-specific communities of fungicolous fungi

Sporocarps (fruit bodies) are the sexual reproductive stage in the life cycle of many fungi. They are highly nutritious and consequently vulnerable to grazing by birds and small mammals, and invertebrates, and can be infected by microbial and fungal parasites and pathogens. The complexity of communities thriving inside sporocarps is largely unknown. In this study, we revealed the diversity, taxonomic composition and host preference of fungicolous fungi (i.e., fungi that feed on other fungi) in sporocarps. We carried out DNA metabarcoding of the ITS2 region from 176 sporocarps of 11 wood-decay fungal host species, all collected within a forest in northeast Finland. We assessed the influence of sporocarp traits, such as lifespan, morphology and size, on the fungicolous fungal community. The level of colonisation by fungicolous fungi, measured as the proportion of non-host ITS2 reads, varied between 2.8–39.8% across the 11 host species and was largely dominated by Ascomycota. Host species was the major determinant of the community composition and diversity of fungicolous fungi, suggesting that host adaptation is important for many fungicolous fungi. Furthermore, the alpha diversity was consistently higher in short-lived and resupinate sporocarps compared to long-lived and pileate ones, perhaps due to a more hostile environment for fungal growth in the latter too. The fungicolous fungi represented numerous lineages in the fungal tree of life, among which a significant portion was poorly represented with reference sequences in databases.Subject terms: Microbial ecology, Molecular evolution     

Patterns of fungal diversity in New Zealand Nothofagus forests

The development of protocols for the conservation of fungi requires knowledge of the factors controlling their distribution, diversity, and community composition. Here we compare patterns of variation in fungal communities across New Zealand's Nothofagus forests, reportedly the most myco-diverse in New Zealand and hence potentially key to effective conservation of fungi in New Zealand. Diversity of leaf endophytic fungi, as assessed by culturing on agar plates, is assessed for three Nothofagus sp. growing in mixed stands from four sites. Host species was found to have a greater influence on fungal community assemblage than site. The leaf endophyte communities associated with Nothofagus solandri and Nothofagus fusca (both Nothofagus subgenus Fuscopora), were more similar to each other than either were to the community associated with Nothofagus menziesii (Nothofagus subgenus Lophozonia). The broad taxonomic groups isolated, identified on the basis of internal transcribed spacer (ITS) sequences, were similar to those found in similar studies from other parts of the world, and from an earlier study on the endophyte diversity in four podocarp species from New Zealand, but there were few matches at species level. Average levels of endophyte species diversity associated with single Nothofagus species and single podocarp species were similar, despite historical literature and collection data recording more than twice as many fungal species on average from the Nothofagus species. The significance of these findings to fungal conservation is discussed.     

Comparison of root-associated communities of native and non-native ectomycorrhizal hosts in an urban landscape

Non-native tree species are often used as ornamentals in urban landscapes. However, their root-associated fungal communities remain yet to be examined in detail. Here, we compared richness, diversity and community composition of ectomycorrhizosphere fungi in general and ectomycorrhizal (EcM) fungi in particular between a non-native Pinus nigra and a native Quercus macrocarpa across a growing season in urban parks using 454-pyrosequencing. Our data show that, while the ectomycorrhizosphere community richness and diversity did not differ between the two host, the EcM communities associated with the native host were often more species rich and included more exclusive members than those of the non-native hosts. In contrast, the ectomycorrhizosphere communities of the two hosts were compositionally clearly distinct in nonmetric multidimensional ordination analyses, whereas the EcM communities were only marginally so. Taken together, our data suggest EcM communities with broad host compatibilities and with a limited numbers of taxa with preference to the non-native host. Furthermore, many common fungi in the non-native Pinus were not EcM taxa, suggesting that the fungal communities of the non-native host may be enriched in non-mycorrhizal fungi at the cost of the EcM taxa. Finally, while our colonization estimates did not suggest a shortage in EcM inoculum for either host in urban parks, the differences in the fungi associated with the two hosts emphasize the importance of using native hosts in urban environments as a tool to conserve endemic fungal diversity and richness in man-made systems.     

Community composition and diversity of Neotropical root‐associated fungi in common and rare trees

Interactions between plants and root‐associated fungi can affect the assembly, diversity, and relative abundances of tropical plant species. Host–symbiont compatibility and some degree of host specificity are prerequisites for these processes to occur, and these prerequisites may vary with host abundance. However, direct assessments of whether specificity of root‐associated fungi varies with host abundance are lacking. Here, in a diverse tropical forest in Los Tuxtlas, Mexico, we couple DNA metabarcoding with a sampling design that controls for host phylogeny, host age, and habitat variation, to characterize fungal communities associated with the roots of three confamilial pairs of host species that exhibit contrasting (high and low) relative abundances. We uncovered a functionally and phylogenetically diverse fungal community composed of 1,038 OTUs (operational taxonomic units with 97% genetic similarity), only 14 of which exhibited host specificity. Host species was a significant predictor of fungal community composition only for the subset of OTUs composed of putatively pathogenic fungi. We found no significant difference in the number of specialists associating with common versus rare trees, but we found that host abundance was negatively correlated with the diversity of root fungal communities. This latter result was significant for symbiotrophs (mostly arbuscular mycorrhizal fungi) and, to a lesser extent, for pathotrophs (mostly plant pathogens). Thus, root fungal communities differ between common and rare trees, which may impact the strength of conspecific negative density dependence. Further studies from other tropical sites and host lineages are warranted, given the role of root‐associated fungi in biodiversity maintenance.     

Arbuscular mycorrhizal communities in tropical forests are affected by host tree species and environment

Arbuscular mycorrhizal (AM) fungi are mutualists with plant roots that are proposed to enhance plant community diversity. Models indicate that AM fungal communities could maintain plant diversity in forests if functionally different communities are spatially separated. In this study we assess the spatial and temporal distribution of the AM fungal community in a wet tropical rainforest in Costa Rica. We test whether distinct fungal communities correlate with variation in tree life history characteristics, with host tree species, and the relative importance of soil type, seasonality and rainfall. Host tree species differ in their associated AM fungal communities, but differences in the AM community between hosts could not be generalized over life history groupings of hosts. Changes in the relative abundance of a few common AM fungal species were the cause of differences in AM fungal communities for different host tree species instead of differences in the presence and absence of AM fungal species. Thus, AM fungal communities are spatially distinguishable in the forest, even though all species are widespread. Soil fertility ranging between 5 and 9 Mg/ha phosphorus did not affect composition of AM fungal communities, although sporulation was more abundant in lower fertility soils. Sampling soils over seasons revealed that some AM fungal species sporulate profusely in the dry season compared to the rainy season. On one host tree species sampled at two sites with vastly different rainfall, relative abundance of spores from Acaulospora was lower and that of Glomus was relatively higher at the site with lower and more seasonal rainfall.     

Specificity in Arabidopsis thaliana recruitment of root fungal communities from soil and rhizosphere

Biotic and abiotic conditions in soil pose major constraints on growth and reproductive success of plants. Fungi are important agents in plant soil interactions but the belowground mycobiota associated with plants remains poorly understood. We grew one genotype each from Sweden and Italy of the widely-studied plant model Arabidopsis thaliana. Plants were grown under controlled conditions in organic topsoil local to the Swedish genotype, and harvested after ten weeks. Total DNA was extracted from three belowground compartments: endosphere (sonicated roots), rhizosphere and bulk soil, and fungal communities were characterized from each by amplification and sequencing of the fungal barcode region ITS2. Fungal species diversity was found to decrease from bulk soil to rhizosphere to endosphere. A significant effect of plant genotype on fungal community composition was detected only in the endosphere compartment. Despite A. thaliana being a non-mycorrhizal plant, it hosts a number of known mycorrhiza fungi in its endosphere compartment, which is also colonized by endophytic, pathogenic and saprotrophic fungi. Species in the Archaeorhizomycetes were most abundant in rhizosphere samples suggesting an adaptation to environments with high nutrient turnover for some of these species. We conclude that A. thaliana endosphere fungal communities represent a selected subset of fungi recruited from soil and that plant genotype has small but significant quantitative and qualitative effects on these communities.     

Peeking through a frosty window: molecular insights into the ecology of Arctic soil fungi

Fungi are ubiquitous in Arctic soils, where they function as symbionts and decomposers and may affect the carbon balance of terrestrial ecosystems subjected to climate change, and yet little is known about soil fungi at high latitudes. Here we review data from recent molecular studies to determine broad patterns in Arctic soil fungal ecology. The data indicate comparatively high fungal diversity in Arctic soils, with currently no evidence for lower species richness at higher latitudes. The dominant fungi, and particularly ectomycorrhizal-forming fungi, appear to be cosmopolitan species. Arctic soil fungi are capable of growth at sub-zero temperatures, melanized forms are frequent, host specificity is low and there is evidence that community composition alters under experimental warming. Future challenges are to determine the drivers of fungal diversity, whether or not diversity alters at higher latitudes and how apparently cosmopolitan fungi are able to survive the extreme environments encountered in Arctic habitats.     

Plant identity strongly structures the root-associated fungal community in a diverse subtropical forest

Revealing the relationship between plants and root-associated fungi is very important in understanding diversity maintenance and community assembly in ecosystems. However, the community assembly of root-associated fungi of focal plant species along a subtropical plant species diversity gradient is less documented. Here, we examined root-associated fungal communities associated with five ectomycorrhizal (EM) plant species (Betula luminifera, Castanea henryi, Castanopsis fargesii, C. sclerophylla, and Quercus serrate) in a Chinese subtropical woody plant species diversity (1, 2, 4, 8, 16 and 24 species) experiment, using paired-end Illumina MiSeq sequencing of the ITS2 region. In total, we detected 1933 root-associated fungal operational taxonomic units (OTUs) at a 97% sequence similarity level. Plant identity had a significant effect on total and saprotrophic fungal OTU richness, but plant species diversity level had a significant effect on saprotrophic and pathogenic fungal OTU richness. The community composition of total, saprotrophic and EM fungi was structured by plant identity and plant species diversity level. However, the community composition of pathogenic fungi was only shaped by plant identity. This study highlights that plant identity has a stronger effect on the root-associated fungal community than plant species diversity level in a diverse subtropical forest ecosystem.     

Nuclear and genome dynamics in multinucleate ascomycete fungi

Genetic variation between individuals is essential to evolution and adaptation. However, intra-organismic genetic variation also shapes the life histories of many organisms, including filamentous fungi. A single fungal syncytium can harbor thousands or millions of mobile and potentially genotypically different nuclei, each having the capacity to regenerate a new organism. Because the dispersal of asexual or sexual spores propagates individual nuclei in many of these species, selection acting at the level of nuclei creates the potential for competitive and cooperative genome dynamics. Recent work in Neurospora crassa and Sclerotinia sclerotiorum has illuminated how nuclear populations are coordinated for fungal growth and other behaviors and has revealed both molecular and physical mechanisms for preventing and policing inter-genomic conflict. Recent results from population-level genomic studies in a variety of filamentous fungi suggest that nuclear exchange between mycelia and recombination between heterospecific nuclei may be of more importance to fungal evolution, diversity and the emergence of newly virulent strains than has previously been recognized.     

Elevated temperature may reduce functional but not taxonomic diversity of fungal assemblages on decomposing leaf litter in streams

Mounting evidence points to a linkage between biodiversity and ecosystem functioning (B-EF). Global drivers, such as warming and nutrient enrichment, can alter species richness and composition of aquatic fungal assemblages associated with leaf-litter decomposition, a key ecosystem process in headwater streams. However, effects of biodiversity changes on ecosystem functions might be countered by the presumed high functional redundancy of fungal species. Here, we examined how environmental variables and leaf-litter traits (based on leaf chemistry) affect taxonomic and functional α- and β-diversity of fungal decomposers. We analysed taxonomic diversity (DNA-fingerprinting profiles) and functional diversity (community-level physiological profiles) of fungal communities in four leaf-litter species from four subregions differing in stream-water characteristics and riparian vegetation. We hypothesized that increasing stream-water temperature and nutrients would alter taxonomic diversity more than functional diversity due to the functional redundancy among aquatic fungi. Contrary to our expectations, fungal taxonomic diversity varied little with stream-water characteristics across subregions, and instead taxon replacement occurred. Overall taxonomic β-diversity was fourfold higher than functional diversity, suggesting a high degree of functional redundancy among aquatic fungi. Elevated temperature appeared to boost assemblage uniqueness by increasing β-diversity while the increase in nutrient concentrations appeared to homogenize fungal assemblages. Functional richness showed a negative relationship with temperature. Nonetheless, a positive relationship between leaf-litter decomposition and functional richness suggests higher carbon use efficiency of fungal communities in cold waters.     

Cryptogam communities on decaying deciduous wood – does tree species diversity matter?

Bryophyte and fungal communities were investigated on fallen trees representing seven deciduous tree species in a mixed near natural nemoral forest. Bryophytes were represented by 41 taxa, including several very frequent species. Of the 296 fungal species, most were recorded with very low frequency and the share of high frequent species was much lower than among the bryophytes. Species turnover was bigger in the fungal communities, compared to the bryophyte communities, and related to a higher extent to measured differences in environmental conditions. Tree species diversity was found to be an important factor for fungal species composition, while only small differences in bryophyte species composition were found between the different tree species. On the other hand bryophyte species richness showed distinct relations to tree species and microclimatic variables, a tendency which was not evident for fungal diversity. It is concluded that the two organism groups to some extent differ in their conservation demands. Thus, conservation of wood-inhabiting bryophytes requires prioritising of large, coherent forest stands in which a stable humid microclimate and a reasonable supply of dead wood is secured. Successful conservation of fungi requires that substantial amounts of dead wood are left for natural decay in a variety of natural forest environments representing different tree species, so that heterogeneity in dead wood types is secured.     

Endophytic fungal community in stems and leaves of plants from desert areas in China

Endophytic fungi are known to play important ecological roles in protecting plants from various abiotic and biotic stresses. Therefore, it is valuable to investigate the endophytic fungal community associated with plants distributed in harsh environments, such as deserts. Fungal communities in the stems and leaves of ten plant samples belonging to eight species were collected from a desert area in China and tested after plant surface sterilization. The fungal compositions were different among plants. Salsola collina, Suaeda salsa, and Coriospermum declinatum possessed the highest fungal richness. The colonization rates of these samples were high, exceeding 50% in eight of the samples. However, the fungal diversity of the samples was low when measured using Shannon??s index, Fisher??s ??, and Simpson??s index. Alternaria alternata, A. franseriae, Fusarium solani, and a second Fusarium species were most frequently isolated from all samples. The diversity of isolated species was low in desert areas, although the colonization rate was relatively high. It was concluded that fungal communities associated with plants in deserts had low diversity, but a small number of species colonized various plants with a high colonization rate. The Jaccard, Sorensen, and Bray?CCurtis similarity indices for the fungal communities were low between stems and leaves. This indicated that different fungal communities colonized these two tissues. Phoma pomorum and Phoma sp. showed tissue preferences.     

Divergent phenologies may facilitate the coexistence of arbuscular mycorrhizal fungi in a North Carolina grassland

Interest in the diversity of arbuscular mycorrhizal (AM) fungal communities has been stimulated by recent data that demonstrate that fungal communities influence the competitive hierarchies, productivity, diversity, and successional patterns of plant communities. Although natural communities of AM fungi are diverse, we have a poor understanding of the mechanisms that promote and maintain that diversity. Plants may coexist by inhabiting disparate temporal niches; plants of many grasslands are either warm or cool season specialists. We hypothesized that AM fungi might be similarly seasonal. To test our hypothesis, we tracked the sporulation of individual AM fungal species growing within a North Carolina grassland. Data were collected in 1996 and 1997; in 1997, sampling focused on two common species. We found that AM fungi, especially Acaulospora colossica and Gigaspora gigantea, maintained different and contrasting seasonalities. Acaulospora colossica sporulated more frequently in the warm season, but Gi. gigantea sporulated more frequently in the cool season. Moreover, AM fungal species were spatially aggregated at a fine scale. Contrasting seasonal and spatial niches may facilitate the maintenance of a diverse community of AM fungi. Furthermore, these data may illuminate our understanding of the AM fungal influence on plant communities: various fungal species may preferentially associate with different plant species and thereby promote diversity in the plant community.     

Airborne and Grain Dust Fungal Community Compositions Are Shaped Regionally by Plant Genotypes and Farming Practices

Chronic exposure to airborne fungi has been associated with different respiratory symptoms and pathologies in occupational populations, such as grain workers. However, the homogeneity in the fungal species composition of these bioaerosols on a large geographical scale and the different drivers that shape these fungal communities remain unclear. In this study, the diversity of fungi in grain dust and in the aerosols released during harvesting was determined across 96 sites at a geographical scale of 560 km² along an elevation gradient of 500 m by tag-encoded 454 pyrosequencing of the internal transcribed spacer (ITS) sequences. Associations between the structure of fungal communities in the grain dust and different abiotic (farming system, soil characteristics, and geographic and climatic parameters) and biotic (wheat cultivar and previous crop culture) factors were explored. These analyses revealed a strong relationship between the airborne and grain dust fungal communities and showed the presence of allergenic and mycotoxigenic species in most samples, which highlights the potential contribution of these fungal species to work-related respiratory symptoms of grain workers. The farming system was the major driver of the alpha and beta phylogenetic diversity values of fungal communities. In addition, elevation and soil CaCO₃ concentrations shaped the alpha diversity, whereas wheat cultivar, cropping history, and the number of freezing days per year shaped the taxonomic beta diversity of these communities.