Genevieve M. Gates

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

Ascomycetes associated with ectomycorrhizas: molecular diversity and ecology with particular reference to the Helotiales

Mycorrhizosphere microbes enhance functioning of the plant-soil interface, but little is known of their ecology. This study aims to characterize the ascomycete communities associated with ectomycorrhizas in two Tasmanian wet sclerophyll forests. We hypothesize that both the phyto- and mycobiont, mantle type, soil microbiotope and geographical distance affect the diversity and occurrence of the associated ascomycetes. Using the culture-independent rDNA sequence analysis, we demonstrate a high diversity of these fungi on different hosts and habitats. Plant host has the strongest effect on the occurrence of the dominant species and community composition of ectomycorrhiza-associated fungi. Root endophytes, soil saprobes, myco-, phyto- and entomopathogens contribute to the ectomycorrhiza-associated ascomycete community. Taxonomically these Ascomycota mostly belong to the orders Helotiales, Hypocreales, Chaetothyriales and Sordariales. Members of Helotiales from both Tasmania and the Northern Hemisphere are phylogenetically closely related to root endophytes and ericoid mycorrhizal fungi, suggesting their strong ecological and evolutionary links. Ectomycorrhizal mycobionts from Australia and the Northern Hemisphere are taxonomically unrelated to each other and phylogenetically distant to other helotialean root-associated fungi, indicating independent evolution. The ubiquity and diversity of the secondary root-associated fungi should be considered in studies of mycorrhizal communities to avoid overestimating the richness of true symbionts.

Establishment of ectomycorrhizal fungal community on isolated Nothofagus cunninghamii seedlings regenerating on dead wood in Australian wet temperate forests: does fruit-body type matter?

Decaying wood provides an important habitat for animals and forms a seed bed for many shade-intolerant, small-seeded plants, particularly Nothofagus. Using morphotyping and rDNA sequence analysis, we compared the ectomycorrhizal fungal community of isolated N. cunninghamii seedlings regenerating in decayed wood against that of mature tree roots in the forest floor soil. The /cortinarius, /russula-lactarius, and /laccaria were the most species-rich and abundant lineages in forest floor soil in Australian sites at Yarra, Victoria and Warra, Tasmania. On root tips of seedlings in dead wood, a subset of the forest floor taxa were prevalent among them species of /laccaria, /tomentella-thelephora, and /descolea, but other forest floor dominants were rare. Statistical analyses suggested that the fungal community differs between forest floor soil and dead wood at the level of both species and phylogenetic lineage. The fungal species colonizing isolated seedlings on decayed wood in austral forests were taxonomically dissimilar to the species dominating in similar habitats in Europe. We conclude that formation of a resupinate fruit body type on the underside of decayed wood is not necessarily related to preferential root colonization in decayed wood. Rather, biogeographic factors as well as differential dispersal and competitive abilities of fungal taxa are likely to play a key role in structuring the ectomycorrhizal fungal community on isolated seedlings in decaying wood.

Fungal Planet description sheets: 128-153

Novel species of microfungi described in the present study include the following from Australia: Catenulostroma corymbiae from Corymbia, Devriesia stirlingiae from Stirlingia, Penidiella carpentariae from Carpentaria, Phaeococcomyces eucalypti from Eucalyptus, Phialophora livistonae from Livistona, Phyllosticta aristolochiicola from Aristolochia, Clitopilus austroprunulus on sclerophyll forest litter of Eucalyptus regnans and Toxicocladosporium posoqueriae from Posoqueria. Several species are also described from South Africa, namely: Ceramothyrium podocarpi from Podocarpus, Cercospora chrysanthemoides from Chrysanthemoides, Devriesia shakazului from Aloe, Penidiella drakensbergensis from Protea, Strelitziana cliviae from Clivia and Zasmidium syzygii from Syzygium. Other species include Bipolaris microstegii from Microstegium and Synchaetomella acerina from Acer (USA), Brunneiapiospora austropalmicola from Rhopalostylis (New Zealand), Calonectria pentaseptata from Eucalyptus and Macadamia (Vietnam), Ceramothyrium melastoma from Melastoma (Indonesia), Collembolispora aristata from stream foam (Czech Republic), Devriesia imbrexigena from glazed decorative tiles (Portugal), Microcyclospora rhoicola from Rhus (Canada), Seiridium phylicae from Phylica (Tristan de Cunha, Inaccessible Island), Passalora lobeliae-fistulosis from Lobelia (Brazil) and Zymoseptoria verkleyi from Poa (The Netherlands). Valsalnicola represents a new ascomycete genus from Alnus (Austria) and Parapenidiella a new hyphomycete genus from Eucalyptus (Australia). Morphological and culture characteristics along with ITS DNA barcodes are also provided.

The Entolomataceae of Tasmania

This book is the result of 14 years of collecting Entolomataceae in the native forests of Tasmania, Australia. Although initially involving only the Tasmanian residents Genevieve Gates and David Ratkowsky, who made twice- or thrice-weekly forays into the forests throughout the year, the project was subsequently joined by agaric specialist Machiel Noordeloos from the Netherlands and by fungi photographer Michael Pilkington from the United Kingdom. The international character of the project is further evidenced by the earlier contributions of American mycologist Tim Baroni to the Tasmanian Rhodocybe species which form the basis of the chapter on the now-expanded concept of Clitopilus , and a visit of several months in 2010 by Brazilian Ph.D. candidate Fernanda Karstedt, who helped to formulate the keys to the Entoloma species. Consequently, several thousand well-annotated collections were found during this inventory and form the basis of this monographic treatment of the Entoloma and Clitopilus of Tasmania. The resulting 90 Entoloma species and 10 Clitopilus species are well documented with standardized descriptions, line drawings of fruit bodies and diagnostic microscopic characters, and, when available, with colour photographs. Thanks to the intensive search, it was possible to illustrate most species in colour. Dichotomous keys facilitate identi fi cation of the species. The species concept used is morphologically based; in several cases, however, identi fi cation to species level is supported by molecular data. The Entolomataceae mycota of Tasmania appears to be fairly unique, as 73 out of 90 species of Entoloma and 5 out of 10 Clitopilus species are new to science, with the majority of the remaining species shared with New Zealand. Only a few taxa have characteristics that match those of European species, and might have been introduced from Europe. The large number of observations enabled the authors to use a statistical analysis of the phenological data, resulting in the recognition of fi ve distinct fruiting patterns. Some species appear preferably in winter and spring, others in the summer and autumn months, where groups can be distinguished with a rather wide fruiting spectrum, encompassing eight months, whereas others have a typical autumnal appearance in the months of April–June. The introductory part contains chapters focussed on the taxonomy, phylogeny, and biogeography of Entolomataceae in Tasmania, in which the current state of knowledge is discussed. There are chapters dedicated speci fi cally to the study of Entolomataceae, giving instructions how to collect, document, and preserve specimens for identi fi cation, and a well-illustrated chapter on characters and character states that are used in Entolomataceae identi fi cation and taxonomy. The introductory part concludes with a chapter dedicated to the ecology, distribution, and phenology of the Tasmanian Entolomataceae, based on the very many observations during this study. Full references to the cited literature are given, as well as an index of species names and synonyms.

The taxonomic foundation, species circumscription and continental endemisms of Singerocybe: evidence from morphological and molecular data

The genus Singerocybe (Tricholomataceae, Agaricales, Basidiomycota) has been the subject of controversy since its proposal in 1988. Its taxonomic foundation, species circumscription and geographical distribution have not yet been examined with molecular sequence data. In this study phylogenetic analyses on this group of fungi were conducted based on collections from Europe, eastern Asia, southern Asia, North America and Australia, with four nuclear markers, ITS, nrLSU, tef1-α and rpb2. Molecular phylogenetic analyses, together with morphological observations, strongly support Singerocybe as a monophyletic group and identify the vesicles in the pileal and stipe cuticle as a synapomorphy of this genus. Seven species are recognized in the genus, including one new species and four new combinations. Clitocybe trogioides and Clitocybe trogioides var. odorifera are synonyms of Singerocybe humilis and Singerocybe alboinfundibuliformis respectively. Most of these species are geographically restricted in their distributions. Furthermore our study expands the distribution range of Singerocybe from the North Temperate Zone to Australia (Tasmania) and tropical southern Asia.

New species and records of Rhodocybe (Entolomataceae, Agaricales) from Tasmania

Five new and two previously unrecorded species of Rhodocybe (Agaricales, fungi) are described from the Australian state of Tasmania with a key provided to species known from Australia and New Zealand. This is the first report of Rhodocybe taxa for Tasmania, and increases the known number of species of this genus for the Australia / New Zealand region from 13 to 18. The newly described species of Rhodocybe are R. pseudopiperita, R. lateritia, R. pallidogrisea, R. tasmanica and R. amara.

Multilocus phylogenetic analyses reveal unexpected abundant diversity and significant disjunct distribution pattern of the Hedgehog Mushrooms ( Hydnum L.)

Hydnum is a fungal genus proposed by Linnaeus in the early time of modern taxonomy. It contains several ectomycorrhizal species which are commonly consumed worldwide. However, Hydnum is one of the most understudied fungal genera, especially from a molecular phylogenetic view. In this study, we extensively gathered specimens of Hydnum from Asia, Europe, America and Australasia, and analyzed them by using sequences of four gene fragments (ITS, nrLSU, tef1α and rpb1). Our phylogenetic analyses recognized at least 31 phylogenetic species within Hydnum, 15 of which were reported for the first time. Most Australasian species were recognized as strongly divergent old relics, but recent migration between Australasia and the Northern Hemisphere was also detected. Within the Northern Hemisphere, frequent historical biota exchanges between the Old World and the New World via both the North Atlantic Land Bridge and the Bering Land Bridge could be elucidated. Our study also revealed that most Hydnum species found in subalpine areas of the Hengduan Mountains in southwestern China occur in northeastern/northern China and Europe, indicating that the composition of the mycobiota in the Hengduan Mountains reigion is more complicated than what we have known before.

A new Entoloma (Basidiomycetes, Agaricales) from Tasmania.

A description is given of a new Entoloma species from Eucalyptus forest with Leptospermum understorey in Tasmania, Australia, with striking yellow lamellae. Notes are given on similar species on a worldwide basis.

Death cap mushrooms from southern Australia: additions to Amanita (Amanitaceae, Agaricales) section Phalloideae Clade IX

Abstract. The following three similar Amanita spp. are described: Amanita djarilmari E.M.Davison, A. gardneri E.M.Davison from the south-west of Western Australia and A. millsii E.M.Davison & G.M.Gates (=A. sp. 10 ZLY-2014 HKAS 77322 in KUN) from Tasmania. All have a white- or pale-coloured pileus and white universal veil, but differ in the shape of the bulb, spore shape, and structure of the universal veil. All are from subgenus Lepidella section Phalloideae. Phylogenetic analysis showed that these species cannot be separated on the basis of data derived from nuclear ribosomal internal transcribed-spacer sequences. They can be separated in a multi-locus phylogeny of the 28S nuclear ribosomal large-subunit rRNA region, RNA polymerase-II region, β-tubulin region and translation elongation-factor 1-α region. Amanita djarilmari, A. gardneri, A. millsii and two other previously described species in section Phalloideae from southern Australia (A. eucalypti and A. marmorata) cluster in Clade IX. These, together with other species in this clade, segregate into two lineages, namely, Clade IX A, with a white or pale pileus, and Clade IX B, with a brown pileus. Solvent extraction, followed by liquid-chromatography tandem-mass spectrometry of A. djarilmari, A. eucalypti, A. gardneri and A. marmorata basidiomes did not detect the highly toxic amatoxins α-amanitin and β-amanitin, but did detect the phallotoxins phallacidin and phalloidin.