Jessie K. Uehling

A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data

Zygomycete fungi were classified as a single phylum, Zygomycota, based on sexual reproduction by zygospores, frequent asexual reproduction by sporangia, absence of multicellular sporocarps, and production of coenocytic hyphae, all with some exceptions. Molecular phylogenies based on one or a few genes did not support the monophyly of the phylum, however, and the phylum was subsequently abandoned. Here we present phylogenetic analyses of a genome-scale data set for 46 taxa, including 25 zygomycetes and 192 proteins, and we demonstrate that zygomycetes comprise two major clades that form a paraphyletic grade. A formal phylogenetic classification is proposed herein and includes two phyla, six subphyla, four classes and 16 orders. On the basis of these results, the phyla Mucoromycota and Zoopagomycota are circumscribed. Zoopagomycota comprises Entomophtoromycotina, Kickxellomycotina and Zoopagomycotina; it constitutes the earliest diverging lineage of zygomycetes and contains species that are primarily parasites and pathogens of small animals (e.g. amoeba, insects, etc.) and other fungi, i.e. mycoparasites. Mucoromycota comprises Glomeromycotina, Mortierellomycotina, and Mucoromycotina and is sister to Dikarya. It is the more derived clade of zygomycetes and mainly consists of mycorrhizal fungi, root endophytes, and decomposers of plant material. Evolution of trophic modes, morphology, and analysis of genome-scale data are discussed.

The Ectomycorrhizal Fungal Community in a Neotropical Forest Dominated by the Endemic Dipterocarp Pakaraimaea dipterocarpacea

Ectomycorrhizal (ECM) plants and fungi can be diverse and abundant in certain tropical ecosystems. For example, the primarily paleotropical ECM plant family Dipterocarpaceae is one of the most speciose and ecologically important tree families in Southeast Asia. Pakaraimaea dipterocarpacea is one of two species of dipterocarp known from the Neotropics, and is also the only known member of the monotypic Dipterocarpaceae subfamily Pakaraimoideae. This Guiana Shield endemic is only known from the sandstone highlands of Guyana and Venezuela. Despite its unique phylogenetic position and unusual geographical distribution, the ECM fungal associations of P. dipterocarpacea are understudied throughout the tree’s range. In December 2010 we sampled ECM fungi on roots of P. dipterocarpacea and the co-occurring ECM tree Dicymbe jenmanii (Fabaceae subfamily Caesalpinioideae) in the Upper Mazaruni River Basin of Guyana. Based on ITS rDNA sequencing we documented 52 ECM species from 11 independent fungal lineages. Due to the phylogenetic distance between the two host tree species, we hypothesized that P. dipterocarpacea would harbor unique ECM fungi not found on the roots of D. jenmanii. Although statistical tests suggested that several ECM fungal species did exhibit host preferences for either P. dipterocarpacea or D. jenmanii, most of the ECM fungi were multi-host generalists. We also detected several ECM fungi that have never been found in long-term studies of nearby rainforests dominated by other Dicymbe species. One particular mushroom-forming fungus appears to be unique and may represent a new ECM lineage of Agaricales that is endemic to the Neotropics.

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.

Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens

Endosymbiosis of bacteria by eukaryotes is a defining feature of cellular evolution. In addition to well-known bacterial origins for mitochondria and chloroplasts, multiple origins of bacterial endosymbiosis are known within the cells of diverse animals, plants and fungi. Early-diverging lineages of terrestrial fungi harbor endosymbiotic bacteria belonging to the Burkholderiaceae. We sequenced the metagenome of the soil-inhabiting fungus Mortierella elongata and assembled the complete circular chromosome of its endosymbiont, Mycoavidus cysteinexigens, which we place within a lineage of endofungal symbionts that are sister clade to Burkholderia. The genome of M. elongata strain AG77 features a core set of primary metabolic pathways for degradation of simple carbohydrates and lipid biosynthesis, while the M. cysteinexigens (AG77) genome is reduced in size and function. Experiments using antibiotics to cure the endobacterium from the host demonstrate that the fungal host metabolism is highly modulated by presence/absence of M. cysteinexigens. Independent comparative phylogenomic analyses of fungal and bacterial genomes are consistent with an ancient origin for M. elongata - M. cysteinexigens symbiosis, most likely over 350 million years ago and concomitant with the terrestrialization of Earth and diversification of land fungi and plants.

New species and distribution records of Clavulina (Cantharellales, Basidiomycota) from the Guiana Shield

Two new species of Clavulina Schroet. (Clavulinaceae, Cantharellales, Basidiomycota) and new distribution records for Clavulina amazonensis Corner and Clavulina sprucei (Berk.) Corner are described from the Pakaraima Mountains of Guyana, in the central Guiana Shield region. These fungi occur in rainforests dominated by ectomycorrhizal (ECM) trees of the leguminous genus Dicymbe (Fabaceae subfam. Caesalpinioideae). Macromorphological, micromorphological and habitat data are provided for each species. Nuclear ribosomal DNA sequences of the internal transcribed spacer region and 28S subunit were obtained for new species and from representative collections of C. amazonensis and C. sprucei. The two new species, Clavulina kunmudlutsa sp. nov. and Clavulina tepurumenga sp. nov., constitute important edible fungi for the Patamona Amerindians. Our specimens of C. sprucei represent the first reports of the species since 1853 as well as a range extension of nearly 1500 km, while sequence data from basidiomata as well as ECM roots suggest that this taxon consists of a cryptic species complex.

Integrated Proteomics and Metabolomics Suggests Symbiotic Metabolism and Multimodal Regulation in a Fungal‐Endobacterial System

Many plant-associated fungi host endosymbiotic endobacteria with reduced genomes. While endobacteria play important roles in these tri-partite plant-fungal-endobacterial systems, the active physiology of fungal endobacteria has not been characterized extensively by systems biology approaches. Here, we use integrated proteomics and metabolomics to characterize the relationship between the endobacterium Mycoavidus sp. and the root-associated fungus Mortierella elongata. In nitrogen-poor media, M. elongata had decreased growth but hosted a large and growing endobacterial population. The active endobacterium likely extracted malate from the fungal host as the primary carbon substrate for energy production and biosynthesis of phospho-sugars, nucleobases, peptidoglycan and some amino acids. The endobacterium obtained nitrogen by importing a variety of nitrogen-containing compounds. Further, nitrogen limitation significantly perturbed the carbon and nitrogen flows in the fungal metabolic network. M. elongata regulated many pathways by concordant changes on enzyme abundances, post-translational modifications, reactant concentrations and allosteric effectors. Such multimodal regulations may be a general mechanism for metabolic modulation.

Lepidostroma vilgalysii, a new basidiolichen from the New World

The lichenized basidiomycete Lepidostroma vilgalysii from Mexico is described based on morphological analyses. The species is only the second representative of the family Lepidostromataceae documented from the New World, and is one of the few described lichens with an inverted morphology, with the algae in a layer at the base of the thallus. Molecular sequence data from the nuclear ribosomal LSU locus are used to confirm the placement of the holotype in Lepidostroma and to evaluate the molecular distinctiveness of the species from all other described species in the family and genus.

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.

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 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.