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.

Aromatic profile of black truffle grown in Argentina: Characterization of commercial categories and alterations associated to maturation, harvesting date and orchard management practices.

Black truffle (Tuber melanosporum) is one of the most appreciated fungi in the world mainly due to its aromatic properties. In the emerging markets such as Argentina, the aroma of locally produced truffles has not been described yet. The volatile organic compounds (VOCs) from 102 black truffles from Argentina were analyzed using solid phase microextraction gas chromatography coupled with mass spectrometer detector (SPME-GC-MS). Several factors such as commercial category, maturity stage, host tree, geographical origin, and aromatic defects detected during classification were also registered and considered. As a result, 79 VOCs were detected, among which 2-methyl-propanal, 2-butanone, 2-methyl-1-propanol, butanal-3-methyl, 3-methyl-1-butanol, 2-methyl-1-butanol were present in high percentage in fresh mature truffles, whereas immature truffles were associated with 3,5-dimethoxytoluene, 2-phenyl-2-butenal, 2,3-dimethoxytoluene. The Argentine black truffles showed significant similarities in their aromatic profile when compared with their Australian and European counterparts, but with some distinctive notes.

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.

Pattern formation features might explain homoplasy: fertile surfaces in higher fungi as an example.

Fungi show a high degree of morphological convergence. Regarded for a long time as an obstacle for phylogenetic studies, homoplasy has also been proposed as a source of information about underlying morphogenetic patterning mechanisms. The "local-activation and long-range inhibition principle" (LALIP), underlying the famous reaction-diffusion model proposed by Alan Turing in 1952, appears to be one of the universal phenomena that can explain the ontogenetic origin of seriate patterns in living organisms. Reproductive structures of fungi in the class Agaricomycetes show a highly periodic structure resulting in, for example, poroid, odontoid, lamellate or labyrinthic hymenophores. In this paper, we claim that self-organized patterns might underlie the basic ontogenetic processes of these structures. Simulations based on LALIP-driven models and covering a wide range of parameters show an absolute mutual correspondence with the morphospace explored by extant agaricomycetes. This could not only explain geometric particularities but could also account for the limited possibilities displayed by hymenial configurations, thus making homoplasy a direct consequence of the limited morphospace resulting from the proposed patterning dynamics.

Community dynamics of soil-borne fungal communities along elevation gradients in neotropical and palaeotropical forests.

Because of their steep gradients in abiotic and biotic factors, mountains offer an ideal setting to illuminate the mechanisms that underlie patterns of species distributions and community assembly. We compared the composition of taxonomically and functionally diverse fungal communities in soils along five elevational gradients in mountains of the Neo- and Palaeotropics (northern Argentina, southern Brazil, Panama, Malaysian Borneo and Papua New Guinea). Both the richness and composition of soil fungal communities reflect environmental factors, particularly temperature and soil pH, with some shared patterns among neotropical and palaeotropical regions. Community dynamics are characterized by replacement of species along elevation gradients, implying a relatively narrow elevation range for most fungi, which appears to be driven by contrasting environmental preferences among both functional and taxonomic groups. For functional groups dependent on symbioses with plants (especially ectomycorrhizal fungi), the distribution of host plants drives richness and community composition, resulting in important differences in elevational patterns between neotropical and palaeotropical montane communities. The pronounced compositional and functional turnover along elevation gradients implies that tropical montane forest fungi will be sensitive to climate change, resulting in shifts in composition and functionality over time.

Thaxterogaster revisited: A phylogenetic and taxonomic overview of sequestrate Cortinarius from Patagonia.

In the Patagonian region, Cortinarius is the most diverse and abundant genus of ectomycorrhizal fungi with at least 250 species. Sequestrate forms were until recently documented within the genus Thaxterogaster, a genus now known to be polyphyletic, and many were consequently transferred to Cortinarius. Original descriptions were mostly available in German and Spanish and interpretations of morphological structures outdated. Despite recent advances in Cortinarius systematics, the current classification, diversity, and ecology of sequestrate "cortinarioid" fungi in Patagonia remain unclear. The objective of this study was to provide an update on sequestrate Cortinarius of southern South America. We documented each species with morphological descriptions, photographs, basidiospore scanning electron microscopy (SEM) images, and molecular characterization using nuc rDNA internal transcribed spacer region ITS1-5.8S-ITS2 (ITS) and nuc 28S rDNA (28S) sequence data. Original descriptions of taxa were also translated to English and revised based on fresh collections. We documented 24 species from Patagonia based on molecular data and conducted morphological and phylogenetic analysis for 18 previously described species based on type and reference specimens. In addition, we formally described two new species. Four additional taxa were provisionally determined as new but require further study. New ITS sequence data were produced from eight type specimens. We also provide a new name, Cortinarius gloiodes, nom. nov., for the taxon previously described as Thaxterogaster gliocyclus. In addition to the species treated in detail, we provided additional reference information and discussion on six described species that remained incompletely known or for which no recent collections were found. Of the 24 taxa documented from Patagonia, 15 species were assigned to 12 current sections in the genus Cortinarius. Analysis of spore ultrastructure showed that sequestrate forms of Patagonian Cortinarius lack a true perisporium.

Cortinarius section Thaumasti in South American Nothofagaceae forests.

We studied the South American species of Cortinarius section Thaumasti based on morphological and molecular data. Members of this group can easily be identified in the field because the basidiomata are small and Phlegmacium-like with a bulbous stipe and the universal veil in most species forms a distinct volva at the base of the stipe. The phylogenetic delimitation of the clade was mostly in concordance with the earlier, morphology-based grouping of the South American taxa except that C. chrysophaeus was resolved outside of the clade. Altogether nine species were recognized in the section. Four species, C. chlorophanus, C. coleopus, C. cosmoxanthus, and C. vaginatus, were previously described by other authors, whereas three species, C. chlorosplendidus, C. olivaceovaginatus, and C. subcosmoxanthus, are described here as new. We were able to identify two remaining taxa, but we do not have sufficient morphological data to allow for a formal description. All of the species in C. section Thaumasti form ectomycorrhizal associations with Nothofagaceae. They have been documented from South America and New Zealand. The Patagonian species are considered endemic to the region. A key to the described species is provided.

Systematic study of truffles in the genus Ruhlandiella, with the description of two new species from Patagonia.

Ruhlandiella is a genus of exothecial, ectomycorrhizal fungi in the order Pezizales. Ascomata of exothecial fungi typically lack a peridium and are covered with a hymenial layer instead. Ruhlandiella species have nonoperculate asci and highly ornamented ascospores. The genus was first described by Hennings in 1903 to include the single species, R. berolinensis. Since then, mycologists have uncovered Ruhlandiella species in many locations around the globe, including Australia, Spain, Italy, and the USA. Currently, there are four recognized species: R. berolinensis, R. peregrina, R. reticulata, and R. truncata. All were found near Eucalyptus or Melaleuca trees of Australasian origin. Recently, we discovered two new species of Ruhlandiella in Nothofagaceae forests in South America. They regularly form mitotic spore mats directly on soil in the forests of Patagonia. Here, we formally describe these new species and construct the phylogeny of Ruhlandiella and related genera using a multilocus phylogenetic analysis. We also revise the taxonomy of Ruhlandiella and provide an identification key to accepted species of Ruhlandiella.

Unveiling new sequestrate Cortinarius species from northern Patagonian Nothofagaceae forests based on molecular and morphological data.

Because of systematic sampling campaigns in the northern Patagonian Nothofagaceae forests of Argentina, several specimens of sequestrate fungi were collected. Some of those collections showed phylogenetic affinities and morphological similarities to members of the formerly recognized sequestrate genus Thaxterogaster, currently a synonym of Cortinarius on the basis of molecular data. Comparisons of macro- and micromorphological features and sequences of nuc rDNA internal transcribed spacer (ITS) regions have revealed that these collections belong to formerly undescribed species. The sequences of the four new taxa presented here, Cortinarius flavopurpureus, C. translucidus, C. nahuelhuapensis, and C. infrequens, were combined into a data set including additional sequences generated from herbarium collections and retrieved from public gene databases and analyzed by maximum likelihood and Bayesian inference methods. The four new species were resolved as distinct clades with strong support; at the same time, they showed unique morphological characteristics (hypogeous to subhypogeous habit, complete gasteromycetation, and spore shape and ornamentation) that separate them from previously described Cortinarius species. In addition, several undescribed and/or not previously sequenced species from these forests were detected through phylogenetic analysis of ectomycorrhizal root tip sequences. A key of characters to identify the sequestrate Cortinarius from Patagonia is provided.

New species of Cortinarius sect. Austroamericani, sect. nov., from South American Nothofagaceae forests.

In this study, we document and describe the new Cortinarius section Austroamericani. Our results reveal high species diversity within this clade, with a total of 12 recognized species. Of these, only C. rufus was previously documented. Seven species are described as new based on basidiomata collections. The four remaining species are only known from environmental sequences. All examined species form ectomycorrhizal associations with species of Nothofagaceae and are currently only known from Argentinean and Chilean Patagonia. The phylogenetic analysis based on the nuc rDNA internal transcriber spacer (ITS1-5.8S-ITS2 = ITS) and partial 28S gene (28S) sequences shows that this section is related to other taxa from the Southern Hemisphere. Species in this group do not belong to subg. Telamonia, where C. rufus was initially placed. Cortinarius rufus and the newly described C. subrufus form a basal clade within sect. Austroamericani that has a weakly supported relationship with the core clade. Because the two species are morphologically similar to species from the core clade and share their distribution and Nothofagaceae associations, we include them here as part of sect. Austroamericani sensu lato (s.l.) until more material is available to refine the delimitation.

A systematic overview of Descolea (Agaricales) in the Nothofagaceae forests of Patagonia.

The descolea clade includes species of ectomycorrhizal basidiomycetes in the genera Descolea, Setchelliogaster, Descomyces, and Timgrovea that are known primarily from the Southern Hemisphere. Taxa in this group produce basidiomes that range in morphology from typical epigeous mushrooms (Descolea) and secotioid taxa (Setchelliogaster) to fully gasteroid species (Descomyces and Timgrovea). High intraspecific morphological variation has been reported in several species within this clade, suggesting that careful morphological and molecular studies are needed to refine species concepts. Molecular analyses of fresh Patagonian collections in conjunction with taxonomic studies have confirmed high variability in key morphological features, including overall sporocarp form, spore shape and dimensions, universal veil remnants, and cuticle configuration. Based on our synthesis, we emend the genus Descolea to include sequestrate species. We describe the new sequestrate taxon Descolea inferna sp. nov. from Nothofagaceae forests in Patagonia and we propose Cortinarius squamatus as a synonym of our new combination Descolea brunnea. We also formalize the identity of Descolea pallida as a synonym of Descolea antarctica and provide new specimens of Cortinarius archeuretus, a species that has not been encountered since the original discovery during the expeditions of Roland Thaxter in 1905-1906. Here we re-describe and transfer this species to Descolea as D. archeureta. We also discuss diagnostic features that can be used to delimitate the four known South American taxa in the descolea clade.

A molecular and morphological re-examination of the generic limits of truffles in the tarzetta-geopyxis lineage - Densocarpa, Hydnocystis, and Paurocotylis.

Truffle species within the /tarzetta-geopyxis lineage share smooth, globose, hyaline spores, but differ in the amount of convolution of hymenia in ascomata. The relationships among truffle species in this lineage have historically been confused. Phylogenetic analyses of the ITS and 28S nuclear ribosomal DNA from recently collected members of the /tarzetta-geopyxis lineage from Asia, Austral Asia, North America, and South America prompted a reinvestigation of species and generic limits in the truffle genera Hydnocystis, Paurocotylis, and Stephensia. Our analyses support emendations of Hydnocystis and Paurocotylis, abandonment of Stephensia and the resurrection of the genus Densocarpa. Nomenclatural changes include the transfer of Stephensia bombycina to Hydnocystis, the transfer of Hydnocystis singeri and Stephensia bynumii to Paurocotylis, the reinstatement of Densocarpa for Stephensia shanori and transfer of Stephensia crocea to Densocarpa. This is the first detection of the genus Paurocotylis in the Americas. We describe three new species, Hydnocystis transitoria from North America, Paurocotylis patagonica from South America, and Paurocotylis watlingii from Australia. Our work highlights the unexplored diversity, morphological plasticity, and remaining taxonomic problems among truffles in the /tarzetta-geopyxis lineage.

Sequestrate fungi from Patagonian Nothofagus forests: Cystangium (Russulaceae, Basidiomycota).

Six species of Cystangium, a genus of sequestrate taxa related to Russula, were collected in Patagonia (Argentina and Chile) during autumn 2001. Two species, C. depauperatum Singer & A.H. Sm. and C. nothofagi (E. Horak) Trappe, Castellano & T. Lebel, were already known from this region, while four new species, C. domingueziae, C. gamundiae, C. grandihyphatum and C. longisterigmatum, are described, illustrated and a key to the species is provided. In addition, sequences of the ITS (rDNA) region were obtained to explore the phylogenetic relationships of our South American Cystangium species.

Greenhouse seedlings of Alnus showed low host intrageneric specificity and a strong preference for some Tomentella ectomycorrhizal associates.

Ectomycorrhizal (ECM) fungal associates of Alnus are relatively few in comparison with those associated with other tree hosts. The composition of ECM assemblages associated with Alnus seems to change very little across the Northern Hemisphere. However, Alnus-associated ECM assemblages from the Western United States, Mexico, and Argentina tend to differ from those in eastern North America and Europe, presumably due to their different biogeographic histories. Alnus glutinosa is a northern European species subjected to diverse environmental conditions. To address intrageneric host preference within two distantly related Alnus species (Alnus acuminata and A. glutinosa), we tested the ECM colonization on seedlings of both species inoculated with natural soil from A. acuminata forests. Two tomentelloid ECM fungi from A. acuminata natural soils were determined from the anatomotyping and molecular analysis. Both species colonized A. glutinosa seedlings and presented similar relative abundances. Additional soil sequence data from A. acuminata sites suggest that a variety of tomentelloid taxa occur, including several unidentified Tomentella lineages. Maximum-likelihood and Bayesian inference analyses based on internal transcribed spacer (ITS) sequences from various locations do not reflect associations of taxa based on their biogeographic origin, and clades are in general constituted by sequences from diverse regions, including South America, Mexico, USA, and Europe. Results illustrate the probable role of specific tomentelloid fungi in the early colonization of seedlings in A. acuminata forests as well as their importance in the structure of the ECM propagule community at the sites.

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.

Large-scale fungal diversity assessment in the Andean Yungas forests reveals strong community turnover among forest types along an altitudinal gradient.

The Yungas, a system of tropical and subtropical montane forests on the eastern slopes of the Andes, are extremely diverse and severely threatened by anthropogenic pressure and climate change. Previous mycological works focused on macrofungi (e.g. agarics, polypores) and mycorrhizae in Alnus acuminata forests, while fungal diversity in other parts of the Yungas has remained mostly unexplored. We carried out Ion Torrent sequencing of ITS2 rDNA from soil samples taken at 24 sites along the entire latitudinal extent of the Yungas in Argentina. The sampled sites represent the three altitudinal forest types: the piedmont (400-700 m a.s.l.), montane (700-1500 m a.s.l.) and montane cloud (1500-3000 m a.s.l.) forests. The deep sequence data presented here (i.e. 4 108 126 quality-filtered sequences) indicate that fungal community composition correlates most strongly with elevation, with many fungi showing preference for a certain altitudinal forest type. For example, ectomycorrhizal and root endophytic fungi were most diverse in the montane cloud forests, particularly at sites dominated by Alnus acuminata, while the diversity values of various saprobic groups were highest at lower elevations. Despite the strong altitudinal community turnover, fungal diversity was comparable across the different zonal forest types. Besides elevation, soil pH, N, P, and organic matter contents correlated with fungal community structure as well, although most of these variables were co-correlated with elevation. Our data provide an unprecedented insight into the high diversity and spatial distribution of fungi in the Yungas forests.

Phylogenetic analysis of the genus Modicella reveals an independent evolutionary origin of sporocarp-forming fungi in the Mortierellales.

Most studies of tissue differentiation and development have focused on animals and plants but many fungi form multi-cellular aggregations of spore-bearing tissue known as fruiting bodies or sporocarps. The ability to form sporocarps has arisen independently in several different evolutionary lineages of fungi. Evolutionary relationships of most sporocarp-forming fungi are well known, but the enigmatic zygomycete genus Modicella contains two species of sporocarp-forming fungi for which the phylogenetic affinities have not been explored based on molecular data. Species of Modicella have an uncertain trophic mode and have alternatively been considered members of the order Endogonales (which contains documented species of sporocarp-forming fungi) or the order Mortierellales (which contains no previously documented species of sporocarp-forming fungi). In this study we perform phylogenetic analyses based on ribosomal DNA of Modicella malleola from the Northern Hemisphere and Modicella reniformis from the Southern Hemisphere to determine the evolutionary affinities of the genus Modicella. Our analyses indicate that Modicella is a monophyletic genus of sporocarp-forming fungi nested within the Mortierellales, a group of microfungi with no previously documented sporocarp-forming species. Because Modicella is distantly related to all other known sporocarp-forming fungi, we infer that this lineage has independently evolved the ability form sporocarps. We conclude that the genus Modicella should be a high priority for comparative genomics studies to further elucidate the process of sporocarp formation in fungi.

Ectomycorrhizal fungal communities associated to Nothofagus species in Northern Patagonia.

Ectomycorrhizal fungi constitute an important component of soil biota in Nothofagus forests in Patagonia. However, ectomycorrhizal fungal community is poorly known in this region. Here, we assess biodiversity and community compositions of ectomycorrhizal fungal species associated with Nothofagus dombeyi, N. obliqua and N. alpina. We selected three monospecific Nothofagus forest sites for each species within the boundaries of the Lanin National Park in Northern Patagonia. Ectomycorrhizal fungal species were identified based on morphotyping and rDNA (ITS and 28S rDNA) sequence analysis using both universal and taxon-specific primers. Contrary to previous studies on congeneric host trees, our results showed no significant differences among Nothofagus forest types in terms of fungal biodiversity and community composition. However, altitude had a strong effect on the structure of the ectomycorrhizal fungal community associated with Nothofagus spp.

Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage.

Truffles have evolved from epigeous (aboveground) ancestors in nearly every major lineage of fleshy fungi. Because accelerated rates of morphological evolution accompany the transition to the truffle form, closely related epigeous ancestors remain unknown for most truffle lineages. This is the case for the quintessential truffle genus Tuber, which includes species with socio-economic importance and esteemed culinary attributes. Ecologically, Tuber spp. form obligate mycorrhizal symbioses with diverse species of plant hosts including pines, oaks, poplars, orchids, and commercially important trees such as hazelnut and pecan. Unfortunately, limited geographic sampling and inconclusive phylogenetic relationships have obscured our understanding of their origin, biogeography, and diversification. To address this problem, we present a global sampling of Tuberaceae based on DNA sequence data from four loci for phylogenetic inference and molecular dating. Our well-resolved Tuberaceae phylogeny shows high levels of regional and continental endemism. We also identify a previously unknown epigeous member of the Tuberaceae--the South American cup-fungus Nothojafnea thaxteri (E.K. Cash) Gamundí. Phylogenetic resolution was further improved through the inclusion of a previously unrecognized Southern hemisphere sister group of the Tuberaceae. This morphologically diverse assemblage of species includes truffle (e.g. Gymnohydnotrya spp.) and non-truffle forms that are endemic to Australia and South America. Southern hemisphere taxa appear to have diverged more recently than the Northern hemisphere lineages. Our analysis of the Tuberaceae suggests that Tuber evolved from an epigeous ancestor. Molecular dating estimates Tuberaceae divergence in the late Jurassic (~156 million years ago), with subsequent radiations in the Cretaceous and Paleogene. Intra-continental diversification, limited long-distance dispersal, and ecological adaptations help to explain patterns of truffle evolution and biodiversity.