Tom W. May

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

Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages

The ectomycorrhizal (EcM) symbiosis involves a large number of plant and fungal taxa worldwide. During studies on EcM diversity, numerous misidentifications, and contradictory reports on EcM status have been published. This review aims to: (1) critically assess the current knowledge of the fungi involved in the EcM by integrating data from axenic synthesis trials, anatomical, molecular, and isotope studies; (2) group these taxa into monophyletic lineages based on molecular sequence data and published phylogenies; (3) investigate the trophic status of sister taxa to EcM lineages; (4) highlight other potentially EcM taxa that lack both information on EcM status and DNA sequence data; (5) recover the main distribution patterns of the EcM fungal lineages in the world. Based on critically examining original reports, EcM lifestyle is proven in 162 fungal genera that are supplemented by two genera based on isotopic evidence and 52 genera based on phylogenetic data. Additionally, 33 genera are highlighted as potentially EcM based on habitat, although their EcM records and DNA sequence data are lacking. Molecular phylogenetic and identification studies suggest that EcM symbiosis has arisen independently and persisted at least 66 times in fungi, in the Basidiomycota, Ascomycota, and Zygomycota. The orders Pezizales, Agaricales, Helotiales, Boletales, and Cantharellales include the largest number of EcM fungal lineages. Regular updates of the EcM lineages and genera therein can be found at the UNITE homepage http://unite.ut.ee/EcM_lineages. The vast majority of EcM fungi evolved from humus and wood saprotrophic ancestors without any obvious reversals. Herbarium records from 11 major biogeographic regions revealed three main patterns in distribution of EcM lineages: (1) Austral; (2) Panglobal; (3) Holarctic (with or without some reports from the Austral or tropical realms). The holarctic regions host the largest number of EcM lineages; none are restricted to a tropical distribution with Dipterocarpaceae and Caesalpiniaceae hosts. We caution that EcM-dominated habitats and hosts in South America, Southeast Asia, Africa, and Australia remain undersampled relative to the north temperate regions. In conclusion, EcM fungi are phylogenetically highly diverse, and molecular surveys particularly in tropical and south temperate habitats are likely to supplement to the present figures. Due to great risk of contamination, future reports on EcM status of previously unstudied taxa should integrate molecular identification tools with axenic synthesis experiments, detailed morphological descriptions, and/or stable isotope investigations. We believe that the introduced lineage concept facilitates design of biogeographical studies and improves our understanding about phylogenetic structure of EcM fungal communities.

Global diversity and distribution of macrofungi

Data on macrofungal diversity and distribution patterns were compiled for major geographical regions of the world. Macrofungi are defined here to include ascomycetes and basidiomycetes with large, easily observed spore-bearing structures that form above or below ground. Each coauthor either provided data on a particular taxonomic group of macrofungi or information on the macrofungi of a specific geographic area. We then employed a meta-analysis to investigate species overlaps between areas, levels of endemism, centers of diversity, and estimated percent of species known for each taxonomic group for each geographic area and for the combined macrofungal data set. Thus, the study provides both a meta-analysis of current data and a gap assessment to help identify research needs. In all, 21,679 names of macrofungi were compiled. The percentage of unique names for each region ranged from 37% for temperate Asia to 72% for Australasia. Approximately 35,000 macrofungal species were estimated to be “unknown” by the contributing authors. This would give an estimated total of 56,679 macrofungi. Our compiled species list does not include data from most of S.E. Europe, Africa, western Asia, or tropical eastern Asia. Even so, combining our list of names with the estimates from contributing authors is in line with our calculated estimate of between 53,000 and 110,000 macrofungal species derived using plant/macrofungal species ratio data. The estimates developed in this study are consistent with a hypothesis of high overall fungal species diversity.

Phylogeography and biogeography of fungi.

The rigorous study of processes shaping geographic distributions of lineages is a relatively new and emerging field in mycology. While it was previously generally believed that most fungi have wide distributions and largely unstructured populations, recent studies have shown that this is not the case. The study of distributions in tandem with molecular approaches to phylogeny has recently made substantial advances to our understanding of the diversity and biogeography of fungi. Comprehensive species inventories have provided a better picture of the actual distribution of these organisms, while robust phylogenies based on molecular characters have provided both data that allow interpretation of current distributions and testable hypotheses regarding the processes responsible for distribution patterns. This commentary provides an introduction to five papers in this issue of Mycological Research that focus on fungal phylogeography. These papers are based on oral contributions given at two symposia at the International Mycological Congress (IMC8) held in Cairns (Australia) in August 2006.

Mushroom lectins: specificity, structure and bioactivity relevant to human disease.

Lectins are non-immunoglobulin proteins that bind diverse sugar structures with a high degree of selectivity. Lectins play crucial role in various biological processes such as cellular signaling, scavenging of glycoproteins from the circulatory system, cell–cell interactions in the immune system, differentiation and protein targeting to cellular compartments, as well as in host defence mechanisms, inflammation, and cancer. Among all the sources of lectins, plants have been most extensively studied. However, more recently fungal lectins have attracted considerable attention due to their antitumor, antiproliferative and immunomodulatory activities. Given that only 10% of mushroom species are known and have been taxonomically classified, mushrooms represent an enormous unexplored source of potentially useful and novel lectins. In this review we provide an up-to-date summary on the biochemical, molecular and structural properties of mushroom lectins, as well as their versatile applications specifically focusing on mushroom lectin bioactivity.

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.

Fungi and fire in Australian ecosystems: a review of current knowledge, management implications and future directions

Fungi are essential components of all ecosystems in roles including symbiotic partners, decomposers and nutrient cyclers and as a source of food for vertebrates and invertebrates. Fire changes the environment in which fungi live by affecting soil structure, nutrient availability, organic and inorganic substrates and other biotic components with which fungi interact, particularly mycophagous animals. We review the literature on fire and fungi in Australia, collating studies that include sites with different time since fire or different fire regimes. The studies used a variety of methods for survey and identification of fungi and focussed on different groups of fungi, with an emphasis on fruit-bodies of epigeal macrofungi and a lack of studies on microfungi in soil or plant tissues. There was a lack of replication of fire treatment effects in some studies. Nevertheless, most studies reported some consequence of fire on the fungal community. Studies on fire and fungi were concentrated in eucalypt forest in south-west and south-eastern Australia, and were lacking for ecosystems such as grasslands and tropical savannahs. The effects of fire on fungi are highly variable and depend on factors such as soil and vegetation type and variation in fire intensity and history, including the length of time between fires. There is a post-fire flush of fruit-bodies of pyrophilous macrofungi, but there are also fungi that prefer long unburnt vegetation. The few studies that tested the effect of fire regimes in relation to the intervals between burns did not yield consistent results. The functional roles of fungi in ecosystems and the interactions of fire with these functions are explained and discussed. Responses of fungi to fire are reviewed for each fungal trophic group, and also in relation to interactions between fungi and vertebrates and invertebrates. Recommendations are made to include monitoring of fungi in large-scale fire management research programs and to integrate the use of morphological and molecular methods of identification. Preliminary results suggest that fire mosaics promote heterogeneity in the fungal community. Management of substrates could assist in preserving fungal diversity in the absence of specific information on fungi.

Antibacterial metabolites from Australian macrofungi from the genus Cortinarius

In this study, ethyl acetate and aqueous fractions from 117 collections of Australian macrofungi belonging to the mushroom genus Cortinarius were screened for antimicrobial activity against Staphylococcus aureus and Pseudomonas aeruginosa. Overall, the lipophilic fractions were more active than the aqueous fractions. The ethyl acetate fractions of most or all collections of 13 species, namely Cortinarius ardesiacus, C. archeri, C. austrosaginus, C. austrovenetus, C. austroviolaceus, C. coelopus, C. [Dermocybe canaria](2), C. clelandii, C. [D. kula], C. memoria-annae, C. persplendidus, C. sinapicolor, C. vinosipes and forty seven collections of un-described Cortinarius species exhibited IC(50) values of 0.09 mg/mL against S. aureus. In contrast, most or all collections of only four species, namely C. abnormis, C. austroalbidus, C. [D. kula], C. persplendidus, and eleven un-described Cortinarius collections exhibited similar effects against P. aeruginosa (IC(50) <or= 0.09 mg/mL). Anthraquinonoid pigments isolated from C. basirubescens together with emodin physcion and erythrogluacin were assessed for their antimicrobial activity. The fungal octaketides austrocortilutein, austrocortirubin, torosachrysone, physcion and emodin were found to strongly inhibit the growth of S. aureus (IC(50) 0.7-12 microg/mL) whereas only physcion and emodin exhibited potency against P. aeruginosa (IC(50) 1.5 and 2.0 microg/mL, respectively).

Taxonomic and functional characterisation of fungi from the Sebacina vermifera complex from common and rare orchids in the genus Caladenia

The terrestrial orchid genus Caladenia contains many species which are threatened with extinction. They have highly specific associations with Sebacina vermifera and closely related fungi, and conservation of these terrestrial orchids, in part, relies on symbiotic propagation to produce plants for reintroduction and ex situ conservation collections. However, little is known of the diversity of mycorrhizal fungi associating with natural populations. Here, restriction fragment polymorphism analysis, internal transcribed spacer and nuclear large subunit sequencing and symbiotic seed germination were used to investigate the taxonomic and functional diversity of fungal isolates from single populations of six endangered Caladenia species and one common species across the same biogeographic range. Fifty-nine fungal isolates were collected for investigation including ten isolates from the six endangered species Caladenia audasii, Caladenia amoena, Caladenia sp. aff. fragrantissima (Central Victoria), Caladenia sp. aff. patersonii, Caladenia rosella and Caladenia orientalis and 49 isolates from six populations of the common species Caladenia tentaculata. While the common species associated with three distinct S. vermifera-like taxa, the six endangered species were restricted to one of these fungal taxa. No direct relationship between the taxonomic identity of the fungi and their ability to stimulate seed germination was observed; however, the majority of the fungi isolated from the Caladenia species were capable of germinating seed in vitro, indicating their mycorrhizal status and potential for symbiotic propagation in conservation programmes.

Multigene sequence data reveal morphologically cryptic phylogenetic species within the genus Laccaria in southern Australia.

Laccaria (Hydnangiaceae, Agaricales, Basidiomycota) is one of the more intensively studied ectomycorrhizal genera; however, species boundaries within Laccaria and the closely related Hydnangium and Podohydnangium in Australia have not yet been examined with molecular sequence data. Based on morphological characters, eight native species of Laccaria are currently recognized in Australia, as well as three Hydnangium species and the monotypic Podohydnangium australe. Sequences of the internal transcribed spacer region of nuclear rDNA (ITS), RNA polymerase beta subunit II (rpb2) and translation elongation factor 1 alpha (tef-1α) were generated from 77 collections of Laccaria, Hydnangium and Podohydnangium from Australia. Ten phylogenetic species and a further 11 potential species (represented by singletons) of Laccaria in Australia are delimited from sequence analyses. Most of the morphological species contained cryptic phylogenetic species, but these species were always nested entirely within a given morphological species, although not always as sister taxa. The rpb2 locus performed best as a species barcode with pairwise and patristic distance measures. The ITS sequence region returned the least resolved gene tree of the three regions examined and was the least useful as a barcode region. Based on the phylogenetic topology, there appears to have been multiple gains and/or losses of the ectomycorrhizal association of some species with the myrtle beech, Nothofagus cunninghamii as well as of sequestrate basidiocarps and two-spored basidia.