Connecting the multiple dimensions of global soil fungal diversity.

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.

Global patterns in endemicity and vulnerability of soil fungi.

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.

Tree Species Richness and Neighborhood Effects on Ectomycorrhizal Fungal Richness and Community Structure in Boreal Forest.

Tree species identity is one of the key factors driving ectomycorrhizal (EcM) fungal richness and community composition in boreal and temperate forest ecosystems, but little is known about the influence of tree species combinations and their neighborhood effects on EcM communities. To advance our understanding of host plant effects on EcM fungi, the roots of silver birch, Scots pine, and Norway spruce were analyzed using high-throughput sequencing across mature boreal forest exploratory plots of monocultures and two- and three-species mixtures in Finland. Our analyses revealed that tree species identity was an important determinant of EcM fungal community composition, but tree species richness had no significant influence on EcM fungal richness and community composition. We found that EcM fungal community composition associated with spruce depends on neighboring tree species. Our study suggests that at a regional-scale tree species identity is the primary factor determining community composition of root-associated EcM fungi alongside with tree species composition effects on EcM fungal community of spruce in mixed stands.

Regional-Scale In-Depth Analysis of Soil Fungal Diversity Reveals Strong pH and Plant Species Effects in Northern Europe.

Soil microbiome has a pivotal role in ecosystem functioning, yet little is known about its build-up from local to regional scales. In a multi-year regional-scale survey involving 1251 plots and long-read third-generation sequencing, we found that soil pH has the strongest effect on the diversity of fungi and its multiple taxonomic and functional groups. The pH effects were typically unimodal, usually both direct and indirect through tree species, soil nutrients or mold abundance. Individual tree species, particularly Pinus sylvestris, Picea abies, and Populus x wettsteinii, and overall ectomycorrhizal plant proportion had relatively stronger effects on the diversity of biotrophic fungi than saprotrophic fungi. We found strong temporal sampling and investigator biases for the abundance of molds, but generally all spatial, temporal and microclimatic effects were weak. Richness of fungi and several functional groups was highest in woodlands and around ruins of buildings but lowest in bogs, with marked group-specific trends. In contrast to our expectations, diversity of soil fungi tended to be higher in forest island habitats potentially due to the edge effect, but fungal richness declined with island distance and in response to forest fragmentation. Virgin forests supported somewhat higher fungal diversity than old non-pristine forests, but there were no differences in richness between natural and anthropogenic habitats such as parks and coppiced gardens. Diversity of most fungal groups suffered from management of seminatural woodlands and parks and thinning of forests, but especially for forests the results depended on fungal group and time since partial harvesting. We conclude that the positive effects of tree diversity on overall fungal richness represent a combined niche effect of soil properties and intimate associations.

Temporal dynamics of ectomycorrhizal fungi and persistence of Tuber melanosporum in inoculated Quercus robur seedlings in North Europe.

Tuber melanosporum is widely cultivated outside its natural habitat in various climatic conditions. This study aims to monitor the persistence of T. melanosporum in inoculated oak seedlings and document temporal changes of native ectomycorrhizal fungi in an Estonian 5-year-old plantation. Sampling of ectomycorrhizal fungi was carried out in June-July 2011-2013 to provide DNA-based identification of the inoculated truffle species and other co-occurring ectomycorrhizal fungi. The mycorrhiza of T. melanosporum proved resistant to cold winters, and the fungus persisted well in the root systems of surviving seedlings albeit slight decline in relative colonization level over 3 years. We identified the genera Hymenogaster and Hebeloma to be the dominant ectomycorrhizal competing fungi in root systems. Good vegetative growth of mycelia and the presence of two compatible mating types suggest that cultivation of T. melanosporum is possible in the Nordic climate. Evaluation of fruit-body production will be a critical next step, because fruiting efficiency allows to determine economic feasibility and ecological sustainability of the Périgord truffle cultivation in northern climate.

Fungal biogeography. Global diversity and geography of soil fungi.

Fungi play major roles in ecosystem processes, but the determinants of fungal diversity and biogeographic patterns remain poorly understood. Using DNA metabarcoding data from hundreds of globally distributed soil samples, we demonstrate that fungal richness is decoupled from plant diversity. The plant-to-fungus richness ratio declines exponentially toward the poles. Climatic factors, followed by edaphic and spatial variables, constitute the best predictors of fungal richness and community composition at the global scale. Fungi show similar latitudinal diversity gradients to other organisms, with several notable exceptions. These findings advance our understanding of global fungal diversity patterns and permit integration of fungi into a general macroecological framework.

Global biogeography of the ectomycorrhizal /sebacina lineage (Fungi, Sebacinales) as revealed from comparative phylogenetic analyses.

Compared with plants and animals, large-scale biogeographic patterns of microbes including fungi are poorly understood. By the use of a comparative phylogenetic approach and ancestral state reconstructions, we addressed the global biogeography, rate of evolution and evolutionary origin of the widely distributed ectomycorrhizal (EcM) /sebacina lineage that forms a large proportion of the Sebacinales order. We downloaded all publicly available internal transcribed spacer (ITS) sequences and metadata and supplemented sequence information from three genes to construct dated phylogenies and test biogeographic hypotheses. The /sebacina lineage evolved 45-57 Myr ago that groups it with relatively young EcM taxa in other studies. The most parsimonious origin for /sebacina is inferred to be North American temperate coniferous forests. Among biogeographic traits, region and biome exhibited stronger phylogenetic signal than host family. Consistent with the resource availability (environmental energy) hypothesis, the ITS region is evolving at a faster rate in tropical than nontropical regions. Most biogeographic regions exhibited substantial phylogenetic clustering suggesting a strong impact of dispersal limitation over a large geographic scale. In northern Holarctic regions, however, phylogenetic distances and phylogenetic grouping of isolates indicate multiple recent dispersal events.