Biogeographic history of a large clade of ectomycorrhizal fungi, the Russulaceae, in the Neotropics and adjacent regions.

The biogeography of neotropical fungi remains poorly understood. Here, we reconstruct the origins and diversification of neotropical lineages in one of the largest clades of ectomycorrhizal fungi in the globally widespread family Russulaceae. We inferred a supertree of 3285 operational taxonomic units, representing worldwide internal transcribed spacer sequences. We reconstructed biogeographic history and diversification and identified lineages in the Neotropics and adjacent Patagonia. The ectomycorrhizal Russulaceae have a tropical African origin. The oldest lineages in tropical South America, most with African sister groups, date to the mid-Eocene, possibly coinciding with a boreotropical migration corridor. There were several transatlantic dispersal events from Africa more recently. Andean and Central American lineages mostly have north-temperate origins and are associated with North Andean uplift and the general north-south biotic interchange across the Panama isthmus, respectively. Patagonian lineages have Australasian affinities. Diversification rates in tropical South America and other tropical areas are lower than in temperate areas. Neotropical Russulaceae have multiple biogeographic origins since the mid-Eocene involving dispersal and co-migration. Discontinuous distributions of host plants may explain low diversification rates of tropical lowland ectomycorrhizal fungi. Deeply diverging neotropical fungal lineages need to be better documented.

Ectomycorrhizal associations in the tropics - biogeography, diversity patterns and ecosystem roles.

Contents Summary 1076 I. Introduction 1076 II. Historical overview 1077 III. Identities and distributions of tropical ectomycorrhizal plants 1077 IV. Dominance of tropical forests by ECM trees 1078 V. Biogeography of tropical ECM fungi 1081 VI. Beta diversity patterns in tropical ECM fungal communities 1082 VII. Conclusions and future research 1086 Acknowledgements 1087 References 1087 SUMMARY: Ectomycorrhizal (ECM) associations were historically considered rare or absent from tropical ecosystems. Although most tropical forests are dominated by arbuscular mycorrhizal (AM) trees, ECM associations are widespread and found in all tropical regions. Here, we highlight emerging patterns of ECM biogeography, diversity and ecosystem functions, identify knowledge gaps, and offer direction for future research. At the continental and regional scales, tropical ECM systems are highly diverse and vary widely in ECM plant and fungal abundance, diversity, composition and phylogenetic affinities. We found strong regional differences among the dominant host plant families, suggesting that biogeographical factors strongly influence tropical ECM symbioses. Both ECM plants and fungi also exhibit strong turnover along altitudinal and soil fertility gradients, suggesting niche differentiation among taxa. Ectomycorrhizal fungi are often more abundant and diverse in sites with nutrient-poor soils, suggesting that ECM associations can optimize plant nutrition and may contribute to the maintenance of tropical monodominant forests. More research is needed to elucidate the diversity patterns of ECM fungi and plants in the tropics and to clarify the role of this symbiosis in nutrient and carbon cycling.

Resolved phylogeny and biogeography of the root pathogen Armillaria and its gasteroid relative, Guyanagaster.

BACKGROUND: Armillaria is a globally distributed mushroom-forming genus composed primarily of plant pathogens. Species in this genus are prolific producers of rhizomorphs, or vegetative structures, which, when found, are often associated with infection. Because of their importance as plant pathogens, understanding the evolutionary origins of this genus and how it gained a worldwide distribution is of interest. The first gasteroid fungus with close affinities to Armillaria-Guyanagaster necrorhizus-was described from the Neotropical rainforests of Guyana. In this study, we conducted phylogenetic analyses to fully resolve the relationship of G. necrorhizus with Armillaria. Data sets containing Guyanagaster from two collecting localities, along with a global sampling of 21 Armillaria species-including newly collected specimens from Guyana and Africa-at six loci (28S, EF1α, RPB2, TUB, actin-1 and gpd) were used. Three loci-28S, EF1α and RPB2-were analyzed in a partitioned nucleotide data set to infer divergence dates and ancestral range estimations for well-supported, monophyletic lineages. RESULTS: The six-locus phylogenetic analysis resolves Guyanagaster as the earliest diverging lineage in the armillarioid clade. The next lineage to diverge is that composed of species in Armillaria subgenus Desarmillaria. This subgenus is elevated to genus level to accommodate the exannulate mushroom-forming armillarioid species. The final lineage to diverge is that composed of annulate mushroom-forming armillarioid species, in what is now Armillaria sensu stricto. The molecular clock analysis and ancestral range estimation suggest the most recent common ancestor to the armillarioid lineage arose 51 million years ago in Eurasia. A new species, Guyanagaster lucianii sp. nov. from Guyana, is described. CONCLUSIONS: The armillarioid lineage evolved in Eurasia during the height of tropical rainforest expansion about 51 million years ago, a time marked by a warm and wet global climate. Species of Guyanagaster and Desarmillaria represent extant taxa of these early diverging lineages. Desarmillaria represents an armillarioid lineage that was likely much more widespread in the past. Guyanagaster likely evolved from a gilled mushroom ancestor and could represent a highly specialized endemic in the Guiana Shield. Armillaria species represent those that evolved after the shift in climate from warm and tropical to cool and arid during the late Eocene. No species in either Desarmillaria or Guyanagaster are known to produce melanized rhizomorphs in nature, whereas almost all Armillaria species are known to produce them. The production of rhizomorphs is an adaptation to harsh environments, and could be a driver of diversification in Armillaria by conferring a competitive advantage to the species that produce them.

Investigating niche partitioning of ectomycorrhizal fungi in specialized rooting zones of the monodominant leguminous tree Dicymbe corymbosa.

Temperate ectomycorrhizal (ECM) fungi show segregation whereby some species dominate in organic layers and others favor mineral soils. Weak layering in tropical soils is hypothesized to decrease niche space and therefore reduce the diversity of ectomycorrhizal fungi. The Neotropical ECM tree Dicymbe corymbosa forms monodominant stands and has a distinct physiognomy with vertical crown development, adventitious roots and massive root mounds, leading to multi-stemmed trees with spatially segregated rooting environments: aerial litter caches, aerial decayed wood, organic root mounds and mineral soil. We hypothesized that these microhabitats host distinct fungal assemblages and therefore promote diversity. To test our hypothesis, we sampled D. corymbosa ectomycorrhizal root tips from the four microhabitats and analyzed community composition based on pyrosequencing of fungal internal transcribed spacer (ITS) barcode markers. Several dominant fungi were ubiquitous but analyses nonetheless suggested that communities in mineral soil samples were statistically distinct from communities in organic microhabitats. These data indicate that distinctive rooting zones of D. corymbosa contribute to spatial segregation of the fungal community and likely enhance fungal diversity.

Sarcodon in the Neotropics II: four new species from Colombia and a key to the regional species.

This work reports on four species of the ectomycorrhizal (ECM) tooth fungus genus Sarcodon (Bankeraceae, Thelephorales, Basidiomycota) recently discovered in the Colombian Amazon. Sarcodon colombiensis sp. nov., Sarcodon rufobrunneus sp. nov., Sarcodon pallidogriseus sp. nov. and Sarcodon bairdii sp. nov. are described as new to science. These fungi occur in forests dominated by ECM trees in the genera Pseudomonotes (Dipterocarpaceae), Dicymbe (Fabaceae subfam. Caesalpinioideae) and Aldina (Fabaceae subfam. Papilionoideae). These records bring the number of Sarcodon species known from the Neotropics to 10. Each of the new species possesses the accepted diagnostic characters for the genus: pileate-stipitate stature, a dentate hymenophore, determinate basidiomata development, fleshy, non-zonate context, and brown, tuberculate basidiospores. Molecular phylogenetic analysis corroborated the generic placement of the species, and, in combination with morphological characters, confirmed that they are new to science. Macromorphological, micromorphological, habitat and DNA sequence data from the nuc rDNA internal transcribed spacer region (ITS) are provided for each of the new species. A key is provided that allows identification of all known Neotropical Sarcodon species and similar extralimital taxa.

New Boletaceae taxa from Guyana: Binderoboletus segoi gen. and sp. nov., Guyanaporus albipodus gen. and sp. nov., Singerocomus rubriflavus gen. and sp. nov., and a new combination for Xerocomus inundabilis.

Binderoboletus segoi gen. and sp. nov., Guyanaporus albipodus gen. and sp. nov. and Singerocomus rubriflavus gen. and sp. nov. (Boletaceae, Boletales, Basidiomycota) are described from the Pakaraima Mountains and adjacent lowlands of Guyana. Xerocomus inundabilis, originally described from the central Brazilian Amazon and based solely on the type collection, is redescribed from numerous collections from Guyana and transferred into Singerocomus. These boletes occur in Neotropical forests dominated by ectomycorrhizal trees in the genera Dicymbe (Fabaceae subfam. Caesalpinioideae), Aldina (Fabaceae subfam. Papilionoideae) and Pakaraimaea (Dipterocarpaceae). Three of the species were repeatedly found in a multiyear sporocarp survey in Dicymbe corymbosa-monodominant forest. Macromorphological, micromorphological, habitat and multilocus DNA sequence data are provided for each species. A molecular phylogenetic analysis based on a large taxon set across the Boletaceae justifies erection of the new genera.

Long-distance dispersal and speciation of Australasian and American species of Cortinarius sect. Cortinarius.

We present a multigene phylogeny (partial nuc rDNA and RPB2) of Cortinarius sect. Cortinarius (i.e. the C. violaceus group), which reveals eight species distributed in Europe, Australasia, South America, Central America and North America. Relaxed molecular clock analyses suggested that diversification began during the Miocene, thus rejecting more ancient Gondwanan origin scenarios among the taxa currently occurring in the northern and southern hemispheres. There was strong support for an Australasian origin of the C. violaceus group with initial dispersal to the Neotropics, followed by migration into North America and Europe. A dispersal-extinction cladogenesis model that includes a parameter for founder effects was the most highly supported biogeographic model in the program BioGeoBEARS. A maximum likelihood analysis showed the most recent common ancestor of sect. Cortinarius was an angiosperm ectomycorrhizal associate. Ancestral associations at the plant family level, however, were ambiguous. Of eight recovered species-level lineages, C. violaceus is the only one that associates with Pinaceae and the only species to associate with both Pinaceae and angiosperms. This analysis showed that long-distance dispersal and founder event speciation have been important factors during evolution of the C. violaceus group.

Sarcodon in the Neotropics I: new species from Guyana, Puerto Rico and Belize.

Four species of the ectomycorrhizal (ECM) genus Sarcodon (Bankeraceae, Thelephorales, Basidiomycota) are described as new to science. Sarcodon pakaraimensis sp. nov. is described from forests dominated by the ECM trees Pakaraimaea dipterocarpacea (Dipterocarpaceae) and Dicymbe jenmanii (Fabaceae subfam. Caesalpinioideae) in the Pakaraima Mountains of Guyana. Sarcodon portoricensis sp. nov. is described from lower montane wet forest within the El Yunque National Forest of Puerto Rico. Sarcodon quercophilus sp. nov. and Sarcodon umbilicatus sp. nov. are described from Quercus (Fagaceae) cloud forests within the Maya Mountains of Belize. The discovery of these species is significant given that the majority of the approximately 87 described Sarcodon species are north temperate or boreal in distribution and frequently associate with coniferous host plants; these constitute the most recent records for Sarcodon from the greater Neotropics. Each of the new species is morphologically consistent with accepted diagnostic characters for Sarcodon: pileate-stipitate stature, a dentate hymenophore, determinate basidiomatal development, fleshy, non-zonate context and brown, tuberculate basidiospores. DNA (ITS) sequence analysis corroborated the generic placement of S. pakaraimensis, S. portoricensis, S. quercophilus and S. umbilicatus and, along with morphological differences, supported their recognition as distinct species. Macromorphological, micromorphological, habitat and DNA sequence data from the nuc rDNA internal transcribed spacer region (ITS) are provided for each of the new species. A key to Neotropical Sarcodon species and similar extralimital taxa is provided.

Cantharellaceae of Guyana II: new species of Craterellus, new South American distribution records for Cantharellus guyanensis and Craterellus excelsus, and a key to the Neotropical taxa.

Craterellus olivaceoluteus sp. nov. and Craterellus cinereofimbriatus sp. nov. are described as new to science. These fungi were collected from Guyana in association with ectomycorrhizal host trees in the genera Dicymbe (Fabaceae subfam. Caesalpinioideae) and Pakaraimaea (Dipterocarpaceae). Cantharellus guyanensis Mont., originally described from French Guiana, is redescribed from recent collections from Guyana, with additional range extensions for the species provided based on material examined from French Guiana, Venezuela, and north central, northeastern and southern Brazil, circumscribing nearly the entire Guiana Shield region and beyond. A new distribution record from French Guiana is provided for Craterellus excelsus T.W. Henkel & Aime. Macromorphological, micromorphological and habitat data are provided for the new species and C. guyanensis as well as DNA sequence data from the nuclear ribosomal regions of the internal transcribed spacer (ITS) and 28S large subunit (LSU); additional sequence data is provided for C. guyanensis and C. excelsus specimens collected outside Guyana. The relationships of these taxa within the Cantharellaceae were evaluated with phylogenetic analyses of ITS and LSU sequence data. This work brings the total number of Cantharellaceae species known from Guyana to eight. A key to the Cantharellus and Craterellus species known from the lowland Neotropics and extralimital montane Central and South America is provided.

New Cortinariaceae species associated with Dicymbe, Aldina, and Pakaraimaea in Guyana.

Species of the ectomycorrhizal (ECM) family Cortinariaceae (Agaricales, Agaricomycetes, Basidiomycota) have long been considered impoverished or absent from lowland tropical rainforests. Several decades of collecting in forests dominated by ECM trees in South America's Guiana Shield is countering this view, with discovery of numerous Cortinariaceae species. To date, ~12 morphospecies of this family have been found in the central Pakaraima Mountains of Guyana. Here, we describe three of these as new species of Cortinarius and two as new species of Phlegmacium from forests dominated by the ECM tree genera Dicymbe (Fabaceae subfam. Detarioideae), Aldina (Fabaceae subfam. Papilionoideae), and Pakaraimaea (Cistaceae). Macromorphological, micromorphological, habitat, and DNA sequence data are provided for each new species.

New species of Xerocomus (Boletales) from the Guiana Shield, with notes on their mycorrhizal status and fruiting occurrence.

Xerocomus cyaneibrunnescens, Xerocomus potaroensis, and Xerocomus parvogracilis (Boletales, Basidiomycota) are described as new species from the Pakaraima Mountains of Guyana, in the central Guiana Shield region. These boletes occur in neotropical forests dominated by ectomycorrhizal (ECM) trees in the genus Dicymbe (Fabaceae subfam. Caesalpinioideae). Each species produced basidiomata during a multi-year plot survey, and each was confirmed as an ECM symbiont with one or more leguminous host plant species in Guyana.

Russulaceae of the Pakaraima Mountains of Guyana. IV. New species forming a distinct lineage of Lactarius subg. Plinthogalus.

The Neotropics have recently emerged as an important region for studies of tropical ectomycorrhizal (ECM) fungi. Specific neotropical areas with high ECM host tree densities have ECM fungal diversities rivaling those of higher-latitude forests. Some forests of the Guiana Shield are dominated by endemic ECM trees of the Fabaceae, including species of Dicymbe (subfam. Detarioideae), Aldina (subfam. Papilionoideae), and Pakaraimaea (Cistaceae). One of the most species-rich ECM fungal families present in each of these systems is Russulaceae. Long-term sampling in forests in Guyana's Pakaraima Mountains has revealed a number of species of the Russulaceae genera Lactarius, Lactifluus, and Russula. In this study, we document a previously unknown, distinct lineage of Lactarius subg. Plinthogalus containing eight species from the Guiana Shield. Here, we describe five of these species from Guyana as new to science: Lactarius humiphilus, Lactarius mycenoides, Lactarius guyanensis, Lactarius dicymbophilus, and Lactarius aurantiolamellatus. Morphological descriptions, habit, habitat, and known distribution are provided for each new species. Sequence data for the barcode internal transcribed spacer (ITS) locus are provided for types and most other collections of the new taxa, and a molecular phylogenetic analysis based on the ITS, 28S, and RPB2 (second-largest subunit of the RNA polymerase II) loci across the genus Lactarius corroborates their morphology-based infrageneric placement. The discovery of this lineage changes our insights into the biogeography and evolutionary history of Lactarius subg. Plinthogalus.

Positive interactions between mycorrhizal fungi and bacteria are widespread and benefit plant growth.

Bacteria, ectomycorrhizal (EcM) fungi, and land plants have been coevolving for nearly 200 million years, and their interactions presumably contribute to the function of terrestrial ecosystems. The direction, stability, and strength of bacteria-EcM fungi interactions across landscapes and across a single plant host, however, remains unclear. Moreover, the genetic mechanisms that govern them have not been addressed. To these ends, we collected soil samples from Bishop pine forests across a climate-latitude gradient spanning coastal California, fractionated the soil samples based on their proximity to EcM-colonized roots, characterized the microbial communities using amplicon sequencing, and generated linear regression models showing the impact that select bacterial taxa have on EcM fungal abundance. In addition, we paired greenhouse experiments with transcriptomic analyses to determine the directionality of these relationships and identify which genes EcM-synergist bacteria express during tripartite symbioses. Our data reveal that ectomycorrhizas (i.e., EcM-colonized roots) enrich conserved bacterial taxa across climatically heterogeneous regions. We also show that phylogenetically diverse EcM synergists are positively associated with plant and fungal growth and have unique gene expression profiles compared with EcM-antagonist bacteria. In sum, we identify common mechanisms that facilitate widespread and diverse multipartite symbioses, which inform our understanding of how plants develop in complex environments.

More than 10,000 pre-Columbian earthworks are still hidden throughout Amazonia.

Indigenous societies are known to have occupied the Amazon basin for more than 12,000 years, but the scale of their influence on Amazonian forests remains uncertain. We report the discovery, using LIDAR (light detection and ranging) information from across the basin, of 24 previously undetected pre-Columbian earthworks beneath the forest canopy. Modeled distribution and abundance of large-scale archaeological sites across Amazonia suggest that between 10,272 and 23,648 sites remain to be discovered and that most will be found in the southwest. We also identified 53 domesticated tree species significantly associated with earthwork occurrence probability, likely suggesting past management practices. Closed-canopy forests across Amazonia are likely to contain thousands of undiscovered archaeological sites around which pre-Columbian societies actively modified forests, a discovery that opens opportunities for better understanding the magnitude of ancient human influence on Amazonia and its current state.

Scaling up: examining the macroecology of ectomycorrhizal fungi.

Ectomycorrhizal (ECM) fungi play major ecological roles in temperate and tropical ecosystems. Although the richness of ECM fungal communities and the factors controlling their structure have been documented at local spatial scales, how they vary at larger spatial scales remains unclear. In this issue of Molecular Ecology, Tedersoo et al. (2012) present the results of a meta-analysis of ECM fungal community structure that sheds important new light on global-scale patterns. Using data from 69 study systems and 6021 fungal species, the researchers found that ECM fungal richness does not fit the classic latitudinal diversity gradient in which species richness peaks at lower latitudes. Instead, richness of ECM fungal communities has a unimodal relationship with latitude that peaks in temperate zones. Intriguingly, this conclusion suggests the mechanisms driving ECM fungal community richness may differ from those of many other organisms, including their plant hosts. Future research will be key to determine the robustness of this pattern and to examine the processes that generate and maintain global-scale gradients of ECM fungal richness.

Towards global patterns in the diversity and community structure of ectomycorrhizal fungi.

Global species richness patterns of soil micro-organisms remain poorly understood compared to macro-organisms. We use a global analysis to disentangle the global determinants of diversity and community composition for ectomycorrhizal (EcM) fungi-microbial symbionts that play key roles in plant nutrition in most temperate and many tropical forest ecosystems. Host plant family has the strongest effect on the phylogenetic community composition of fungi, whereas temperature and precipitation mostly affect EcM fungal richness that peaks in the temperate and boreal forest biomes, contrasting with latitudinal patterns of macro-organisms. Tropical ecosystems experience rapid turnover of organic material and have weak soil stratification, suggesting that poor habitat conditions may contribute to the relatively low richness of EcM fungi, and perhaps other soil biota, in most tropical ecosystems. For EcM fungi, greater evolutionary age and larger total area of EcM host vegetation may also contribute to the higher diversity in temperate ecosystems. Our results provide useful biogeographic and ecological hypotheses for explaining the distribution of fungi that remain to be tested by involving next-generation sequencing techniques and relevant soil metadata.

Cantharellaceae of Guyana I: new species, combinations and distribution records of Craterellus and a synopsis of known taxa.

Members of the Cantharellaceae (Cantharellales, Basidiomycota) are common ectomycorrhizal associates of the leguminous genus Dicymbe in the Pakaraima Mountains of Guyana. Eight distinct species or morphospecies currently are recognized in Craterellus Pers. or Cantharellus Adans. ex Fr. from Guyanese Dicymbe-dominated forests. We evaluated the systematics of these taxa with phylogenetic analyses of DNA sequence data from the nuclear ribosomal regions of the internal transcribed spacer (ITS) and 28S large subunit (LSU). The results of these analyses along with careful assessment of morphology let us described two new species, Craterellus atratoides sp. nov. and Craterellus strigosus sp. nov., redescribe Craterellus atratus (Corner) Yomyart et al. based on new material from Guyana, and propose a new combination in Craterellus for Cantharellus pleurotoides T.W. Henkel, Aime & S.L. Mill. Macroscopic illustrations are provided for two additional cantharelloid morphospecies confirmed in Craterellus, as well as the regionally endemic Cantharellus guyanensis Mont. Macromorphological, micromorphological and habitat data are provided for C. atratoides, C. strigosus and C. atratus, and ITS and LSU sequence data are provided for each of the eight known Guyanese taxa.

New species of Clavulina (Cantharellales, Basidiomycota) with resupinate and effused basidiomata from the Guiana Shield.

Three new species of Clavulina (Cantharellales, Basidiomycota) are described from rainforests dominated by ectomycorrhizal trees of the leguminous genus Dicymbe (Fabaceae subfam. Caesalpinioideae) from the central Guiana Shield. Species of Clavulina typically form branched, coralloid basidiomata with amphigenous hymenia. However, the three species described here form resupinate or effuso-coralloid basidiomata, macromorphological forms previously unknown in Clavulina. Macromorphological, micromorphological, habitat and DNA sequence data are provided for each new species. Micromorphological features and DNA sequence data from the second largest subunit of DNA-dependant RNA polymerase II (rpb2) and internal transcribed spacer (ITS) and large subunit (28S) of the ribosomal repeat justify placement of these new species in Clavulina. Comparisons with described Clavulina species and other resupinate taxa within the Cantharellales are provided.

New Elaphomyces species (Elaphomycetaceae, Eurotiales, Ascomycota) from Guyana.

Elaphomyces compleximurus sp. nov. and E. digitatus sp. nov. are described from the Pakaraima Mountains of Guyana. Macromorphological, micromorphological, habitat and DNA sequence data are provided for each new species. This is the first report of Elaphomyces ascomata associated with ectomycorrhizal members of the Fabaceae and also for the genus from the lowland South American tropics.

Membranomyces species are common ectomycorrhizal symbionts in Northern Hemisphere forests.

Membranomyces (Clavulinaceae, Cantharellales) Jülich consists of two described species of resupinate (crust-like) basidiomycetes. Previous studies indicated that Membranomyces falls within the Clavulinaceae, but the phylogenetic position of the genus has not been fully resolved. Membranomyces species were thought to be saprotrophic until 2003 when Tedersoo et al. detected Membranomyces delectabilis on ectomycorrhizal roots of Populus and Picea. Membranomyces was previously known only from collections made in eastern Canada and Europe. We recently sequenced the ITS rDNA barcode region from Scandinavian herbarium specimens identified as M. delectabilis and Membranomyces spurius. Phylogenetic analyses of these sporocarp sequences and similar environmental sequences indicated that Membranomyces is more diverse than previously thought and forms ectomycorrhizas with hosts from a diverse range of plant families in many north temperate ecosystems.