Meike Piepenbring

Global diversity and geography of soil fungi

Introduction The kingdom Fungi is one of the most diverse groups of organisms on Earth, and they are integral ecosystem agents that govern soil carbon cycling, plant nutrition, and pathology. Fungi are widely distributed in all terrestrial ecosystems, but the distribution of species, phyla, and functional groups has been poorly documented. On the basis of 365 global soil samples from natural ecosystems, we determined the main drivers and biogeographic patterns of fungal diversity and community composition. Direct and indirect effects of climatic and edaphic variables on plant and fungal richness. Line thickness corresponds to the relative strength of the relationships between the variables that affect species richness. Dashed lines indicate negative relationships. MAP, mean annual precipitation; Fire, time since last fire; Dist. equator, distance from the equator; Ca, soil calcium concentration; P, soil phosphorus concentration; pH, soil pH. Rationale We identified soil-inhabiting fungi using 454 Life Sciences (Branford, CN) pyrosequencing and through comparison against taxonomically and functionally annotated sequence databases. Multiple regression models were used to disentangle the roles of climatic, spatial, edaphic, and floristic parameters on fungal diversity and community composition. Structural equation models were used to determine the direct and indirect effects of climate on fungal diversity, soil chemistry, and vegetation. We also examined whether fungal biogeographic patterns matched paradigms derived from plants and animals—namely, that species’ latitudinal ranges increase toward the poles (Rapoport’s rule) and diversity increases toward the equator. Last, we sought group-specific global biogeographic links among major biogeographic regions and biomes using a network approach and area-based clustering. Results Metabarcoding analysis of global soils revealed fungal richness estimates approaching the number of species recorded to date. Distance from equator and mean annual precipitation had the strongest effects on richness of fungi, including most fungal taxonomic and functional groups. Diversity of most fungal groups peaked in tropical ecosystems, but ectomycorrhizal fungi and several fungal classes were most diverse in temperate or boreal ecosystems, and many fungal groups exhibited distinct preferences for specific edaphic conditions (such as pH, calcium, or phosphorus). Consistent with Rapoport’s rule, the geographic range of fungal taxa increased toward the poles. Fungal endemicity was particularly strong in tropical regions, but multiple fungal taxa had cosmopolitan distribution. Conclusions Climatic factors, followed by edaphic and spatial patterning, are the best predictors of soil fungal richness and community composition at the global scale. Richness of all fungi and functional groups is causally unrelated to plant diversity, with the exception of ectomycorrhizal root symbionts, suggesting that plant-soil feedbacks do not influence the diversity of soil fungi at the global scale. The plant-to-fungi richness ratio declined exponentially toward the poles, indicating that current predictions—assuming globally constant ratios—overestimate fungal richness by 1.5- to 2.5-fold. Fungi follow similar biogeographic patterns as plants and animals, with the exception of several major taxonomic and functional groups that run counter to overall patterns. Strong biogeographic links among distant continents reflect relatively efficient long-distance dispersal compared with macro-organisms. 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 metagenomics detects hotspots of fungal diversity and macroecological patterns and indicates that plant and fungal diversity are uncoupled. [Also see Perspective by Wardle and Lindahl] Assessing fungal diversity worldwide Fungi are hyperdiverse but poorly known, despite their ecological and economic impacts. Tedersoo et al. collected nearly 15,000 topsoil samples from 365 sites worldwide and sequenced their genomes (see the Perspective by Wardle and Lindahl). Overall, they found a striking decline in fungal species richness with distance from the equator. For some specialist groups though, diversity depended more on the abundance of host plants than host diversity or geography. The findings reveal a huge gap between known and described species and the actual numbers of distinct fungi in the worlds soils. Science, this issue 10.1126/science.1256688; see also p. 1052

The generic position of Ustilago maydis, Ustilago scitaminea, and Ustilago esculenta (Ustilaginales)

Three species of smut fungi (Ustilaginales, Basidiomycota) of economic importance, Ustilago maydis on corn, U. scitaminea on sugar cane, and U. esculenta on Zizania latifolia, were investigated in order to define their systematic position using morphological characteristics of the sori, ultrastructure of teliospore walls, and molecular data of the LSU rDNA. LSU rDNA suggests that U. maydis and U. scitaminea belong to the genus Sporisorium. This has already been proposed for U. scitaminea, which develops sori with whip-shaped axes corresponding to columellae. U. maydis and U. scitaminea, like typical species of Sporisorium, present peridia and columellae in their sori. Therefore, U. scitaminea is called Sporisorium scitamineum. U. maydis, however, is not placed in the genus Sporisorium here, because ongoing investigation of molecular data from the ITS rDNA region yields contradictory results and because the name Sporisorium maydis is occupied by an imperfect fungus. U. esculenta is recognized as Yenia esculenta. This placement in a separate genus is based on molecular data and on unique teliospore ultrastructure, i.e. apically enlarged, partly confluent warts developing on a strongly folded plasmalemma, and the exosporium and endosporium forming part of the ornamentation.

Recognition of hypoxyloid and xylarioid Entonaema species and allied Xylaria species from a comparison of holomorphic morphology, HPLC profiles, and ribosomal DNA sequences

The genus Entonaema comprises Xylariaceae with hollow, gelatinous stromata that accumulate liquid. Some of its species, including the type species, appear related to Daldinia from a polyphasic approach, comprising morphological studies, comparisons of ribosomal DNA sequences, and high performance liquid chromatography (HPLC) profiles with diode array and mass spectrometric detection (HPLC-DAD-MS). This methodology was used to study Entonaema pallidum. Its major stromatal constituent was identified as xylaral, a secondary metabolite known from Xylaria polymorpha. This compound was detected in several Xylaria spp., including the tropical X. telfairii and morphologically similar taxa, whose stromata may also become hollow and filled with liquid. Cultures of E. pallidum resembled those of Xylaria, substantially differing from other Entonaema spp., in their morphology, 5.8S/ITS nrDNA sequences, and HPLC profiles. The type specimen of E. mesentericum was located in the spirit collection of the herbarium B and found to agree morphologically with the nomenclatorily younger E. pallidum. Traces of xylaral were even detected by HPLC-DAD-MS in the spirit in which the fungus had been preserved. Entonaema pallidum is thus regarded as a later synonym of E. mesentericum. Therefore, the latter name is transferred to Xylaria. A key to entonaemoid Xylariaceae is provided. Colour reactions (NH3, KOH) of the ectostroma were applied to a limited number of Xylaria spp., but metabolite profiles of cultures appear more promising as chemotaxonomic traits to segregate this genus. As xylaral was also found in Nemania and Stilbohypoxylon spp., while being apparently absent in Hypoxylon and allied genera, it may be a chemotaxonomic marker for Xylariaceae with Geniculosporium-like anamorphs.

Teliospores of smut fungi general aspects of teliospore walls and sporogenesis

SummaryThe concept and nomenclature for the elements of teliospore walls in smut fungi are presented and a survey of teliosporogenesis is given, as seen by light and transmission electron microscopy. Four developmental types are distinguished: the Ustilago, Microbotryum, Tilletia, and Entorrhiza type. In the Ustilago type, sporogenous hyphae are completely segmented into teliospore initials which are embedded in a hyaline matrix formed by gelatinised hyphal walls (found in species ofAnthracoidea, Cintractia, Heterotolyposporium, Kuntzeomyces, Macalpinomyces, Melanopsichium, Sporisorium, Testicularia, Tolyposporium junci, Trichocintractia, and species ofUstilago infecting members of the family Poaceae). In the Microbotryum type, septate sporogenous hyphae are also completely segmented into teliospore initials, however, they are not surrounded by a hyaline matrix (Microbotryum, Sphacelotheca, Ustilago spp. infecting dicotyledons). A yeast-like budding of teliosporogenic cells is observed for some species ofMicrobotryum, Sphacelotheca, andUstilago infecting dicotyledons. In the Tilletia type, teliospores differentiate locally in the sporogenous hyphae, in an apical or intercalary position, without a hyaline matrix (Conidiosporomyces, Doassinga, Entyloma, Erratomyces, Ingoldiomyces, Neovossia, Oberwinkleria, Rhamphospora, Tilletia). In all these types, the teliospore initials first develop a hyaline sheath under which the ornamentation, the exosporium, sometimes a middle layer, and the endosporium are successively deposited by the fungal cell. In the Entorrhiza type, the teliospores develop inside vital host cells with the wall of the sporogenous hypha included into the teliospore wall. The fungus develops a middle layer and an electron-transparent endosporium inside the hyphal wall while a layer forming the ornamentation is deposited onto the hyphal wall, probably by vesicles of dictyosomes of the host cell.

Teliospores of smut fungi teliospore walls and the development of ornamentation studied by electron microscopy

SummaryThe walls of mature teliospores and the development of ornamentation, as seen by transmission electron microscopy, are described for 37 genera of smut fungi, based on observations of ca. 120 species and on literature. Structural diversity of mature teliospore walls is due to differences in spore wall layers forming the spore wall (endosporium, middle layer, exosporium, ornamentation) and to different elements forming the ornamentation (exosporium, ornaments, sheath, hyphal wall, adjacent fungal cells, material of the host). During teliosporogenesis the outer layers are usually deposited first. At the beginning of the formation of the ornamentation the plasma membrane may be smooth or undulated carrying the developing ornaments on its tips or in its depressions. The ornamentation of some genera appears similar when seen by scanning electron microscopy, but can be the product of different developmental patterns (e.g., warts of species ofFarysia, Tilletia, andUstilago), however, warty and reticulate ornamentation can both be produced by similar developmental processes (shown, e.g., for species ofCintractia andTilletia). Typical structures of the mature teliospore wall and developmental patterns based on homologous similarities are described for the following groups of genera or species:Macalpinomyces, Melanopsichium, Sporisorium, andUstilago infecting members of the family Poaceae;Kuntzeomyces, Testicularia, andTrichocintractia; Anthracoidea, Cintractia, Heterotolyposporium piluliforme, andTolyposporium junci; Glomosporium, Sorosporium, andThecaphora; Conidiosporomyces, Erratomyces, Ingoldiomyces, Neovossia, Oberwinkleria, andTilletia; Entyloma, and genera of the Doassansia group;Liroa, Microbotryum, Sphacelotheca, Ustilago infecting dicotyledons, andZundeliomyces; Aurantiosporium, Fulvisporium, andUstilentyloma. Special characteristics of the teliospore wall were observed for the generaDermatosorus, Doassinga, Entorrhha, Farysia, Mycosyrinx, Rhamphospora, and some species ofTolyposporium.

Influence of phylogenetic conservatism and trait convergence on the interactions between fungal root endophytes and plants

Plants associate through their roots with fungal assemblages that impact their abundance and productivity. Non-mycorrhizal endophytes constitute an important component of such fungal diversity, but their implication in ecosystem processes is little known. Using a selection of 128 root-endophytic strains, we defined functional groups based on their traits and plant interactions with potential to predict community assembly and symbiotic association processes. In vitro tests of the strains’ interactions with Arabidopsis thaliana, Microthlaspi erraticum and Hordeum vulgare showed a net negative effect of fungal colonization on plant growth. The effects partly depended on the phylogenetic affiliation of strains, but also varied considerably depending on the plant-strain combination. The variation was partly explained by fungal traits shared by different lineages, like growth rates or melanization. The origin of strains also affected their symbioses, with endophytes isolated from Microthlaspi spp. populations being more detrimental to M. erraticum than strains from other sources. Our findings suggest that plant–endophyte associations are subject to local processes of selection, in which particular combinations of symbionts are favored across landscapes. We also show that different common endophytic taxa have differential sets of traits found to affect interactions, hinting to a functional complementarity that can explain their frequent co-existence in natural communities.

Defining species in Tulasnella by correlating morphology and nrDNA ITS-5.8S sequence data of basidiomata from a tropical Andean forest

The genus Tulasnella comprises important orchid mycobionts. Molecular phylogenetic studies on nrITS-5.8S sequences of Tulasnella species previously isolated from mycorrhizas of epiphytic orchids from a tropical Andean forest showed genomic variability among clones which was difficult to interpret as intra- or interspecific variations or to correlate with described Tulasnella species. To improve this situation, we collected basidiomata of Tulasnella in an Andean forest, studied part of the sequences of fungal ribosomal genes and correlated molecular data with the morphology of the specimens. Within five basidiomata displaying slight morphological variability, we found inter-specimen nrITS1-5.8S-ITS2 variability corresponding to proportional differences of less than 1% except for one clone with 5.1% divergence. Results indicate that the slightly variable basidiomata should be considered as one species, which is morphologically tentatively assigned to the Tulasnella pruinosa complex. However, comparison of nrITS1-5.8S-ITS2 sequences, including sequences of T. pruinosa from other origins, indicate that Tulasnella sp. is only distantly related to the T. pruinosa specimens included in the analyses. Sequences of all morphologically similar and taxonomically well-identified species are required to decide whether the basidiomata analyzed in the present study represent a new species. The new sequences are rather similar to sequences obtained previously from mycorrhizae of epiphytic orchids of the same area indicating mycorrhizal potential of this fungus.

Molecular Keys to the Janthinobacterium and Duganella spp. Interaction with the Plant Pathogen Fusarium graminearum

Janthinobacterium and Duganella are well-known for their antifungal effects. Surprisingly, almost nothing is known on molecular aspects involved in the close bacterium-fungus interaction. To better understand this interaction, we established the genomes of 11 Janthinobacterium and Duganella isolates in combination with phylogenetic and functional analyses of all publicly available genomes. Thereby, we identified a core and pan genome of 1058 and 23,628 genes. All strains encoded secondary metabolite gene clusters and chitinases, both possibly involved in fungal growth suppression. All but one strain carried a single gene cluster involved in the biosynthesis of alpha-hydroxyketone-like autoinducer molecules, designated JAI-1. Genome-wide RNA-seq studies employing the background of two isolates and the corresponding JAI-1 deficient strains identified a set of 45 QS-regulated genes in both isolates. Most regulated genes are characterized by a conserved sequence motif within the promoter region. Among the most strongly regulated genes were secondary metabolite and type VI secretion system gene clusters. Most intriguing, co-incubation studies of J. sp. HH102 or its corresponding JAI-1 synthase deletion mutant with the plant pathogen Fusarium graminearum provided first evidence of a QS-dependent interaction with this pathogen.

Lophodermium pini-mugonis sp. nov. on needles of Pinus mugo from the Alps based on morphological and molecular data.

Lophodermium pini-mugonis, collected on needles of Pinus mugo from German Alps, is described as a species new to science. It is characterized by subcuticular ascomata with a wrinkled surface and a somewhat untidy outline, a complex structure of lip cells, and ellipsoidal conidia. An analysis of the internal transcribed spaces of rDNA showed that Lophodermium pini-mugonis is, sister to Lophodermium autumnale and distantly related to other Lophodermium species on pines. The hypothesis of cospeciation of Lophodermium species with members of the Pinaceae is discussed.

ERRATOMYCES, A NEW GENUS OF TILLETIALES WITH SPECIES ON LEGUMINOSAE

AbstractIn India and in the American tropics angular black spot disease on leaves of Vigna spp. and Phaseolus vulgaris (Fabaceae) is caused by Protomycopsis patelii and Entyloma vignae, respectivel...