To explore strange new worlds - The diversification in Tremella caloplacae was linked to the adaptive radiation of the Teloschistaceae.

Lichenicolous fungi are a heterogeneous group of organisms that grow exclusively on lichens, forming obligate associations with them. It has often been assumed that cospeciation has occurred between lichens and lichenicolous fungi, but this has been seldom analysed from a macroevolutionary perspective. Many lichenicolous species are rare or are rarely observed, which results in frequent and large gaps in the knowledge of the diversity of many groups. This, in turn, hampers evolutionary studies that necessarily are based on a reasonable knowledge of this diversity. Tremella caloplacae is a heterobasidiomycete growing on various hosts from the lichen-forming family Teloschistaceae, and evidence suggests that it may represent a species complex. We combine an exhaustive sampling with molecular and ecological data to study species delimitation, cophylogenetic events and temporal concordance of this association. Tremella caloplacae is here shown to include at least six distinct host-specific lineages (=putative species). Host switch is the dominant and most plausible event influencing diversification and explaining the coupled evolutionary history in this system, although cospeciation cannot be discarded. Speciation in T. caloplacae would therefore have occurred coinciding with the rapid diversification - by an adaptive radiation starting in the late Cretaceous - of their hosts. New species in T. caloplacae would have developed as a result of specialization on diversifying lichen hosts that suddenly offered abundant new ecological niches to explore or adapt to.

Tremella macrobasidiata and Tremella variae have abundant and widespread yeast stages in Lecanora lichens.

Dimorphism is a widespread feature of tremellalean fungi in general, but a little-studied aspect of the biology of lichen-associated Tremella. We show that Tremella macrobasidiata and Tremella variae have an abundant and widespread yeast stage in their life cycles that occurs in Lecanora lichens. Their sexual filamentous stage is restricted to a specific lichen: T. macrobasidiata only forms basidiomata on Lecanora chlarotera hymenia and T. variae only on Lecanora varia thalli. However, the yeast stage of T. macrobasidiata is less specific and can occur in L. varia lichens, whilst all life stages of T. variae may be specific to L. varia. Contrary to the hyphal stages, the yeasts are distributed across the thalli and hymenia of Lecanora lichens, and not limited to specimens with basidiomata. Tremella macrobasidiata was present in all studied L. chlarotera, and in 59% of L. varia specimens. Only in 8% of the L. varia thalli could none of the two Tremella species be detected. Our results indicate that lichen-associated Tremella may be much more abundant and widespread than previously assumed leading to skewed estimations about their distribution ranges and lichen specificity, and raise new questions about their biology, ecology and function in the symbiosis.

Species delimitation in the cyanolichen genus Rostania.

BACKGROUND: In this study, we investigate species limits in the cyanobacterial lichen genus Rostania (Collemataceae, Peltigerales, Lecanoromycetes). Four molecular markers (mtSSU rDNA, ß-tubulin, MCM7, RPB2) were sequenced and analysed with two coalescent-based species delimitation methods: the Generalized Mixed Yule Coalescent model (GMYC) and a Bayesian species delimitation method (BPP) using a multispecies coalescence model (MSC), the latter with or without an a priori defined guide tree. RESULTS: Species delimitation analyses indicate the presence of eight strongly supported candidate species. Conclusive correlation between morphological/ecological characters and genetic delimitation could be found for six of these. Of the two additional candidate species, one is represented by a single sterile specimen and the other currently lacks morphological or ecological supporting evidence. CONCLUSIONS: We conclude that Rostania includes a minimum of six species: R. ceranisca, R. multipunctata, R. occultata 1, R. occultata 2, R. occultata 3, and R. occultata 4,5,6. Three distinct Nostoc morphotypes occur in Rostania, and there is substantial correlation between these morphotypes and Rostania thallus morphology.

Microbiome change by symbiotic invasion in lichens.

Lichens are obligate symbioses between fungi and green algae or cyanobacteria. Most lichens resynthesize their symbiotic thalli from propagules, but some develop within the structures of already existing lichen symbioses. Diploschistes muscorum starts as a parasite infecting the lichen Cladonia symphycarpa and gradually develops an independent Diploschistes lichen thallus. Here we studied how this process influences lichen-associated microbiomes and photobionts by sampling four transitional stages, at sites in Sweden and Germany, and characterizing their microbial communities using high-throughput 16S rRNA gene and photobiont-specific ITS rDNA sequencing, and fluorescence in situ hybridization. A gradual microbiome shift occurred during the transition, but fractions of Cladonia-associated bacteria were retained during the process of symbiotic reorganization. Consistent changes observed across sites included a notable decrease in the relative abundance of Alphaproteobacteria with a concomitant increase in Betaproteobacteria. Armatimonadia, Spartobacteria and Acidobacteria also decreased during the infection of Cladonia by Diploschistes. The lichens differed in photobiont specificity. Cladonia symphycarpa was associated with the same algal species at all sites, but Diploschistes muscorum had a flexible strategy with different photobiont combinations at each site. This symbiotic invasion system suggests that partners can be reorganized and selected for maintaining potential roles rather than depending on particular species.

Understanding lichenicolous heterobasidiomycetes: new taxa and reproductive innovations in Tremella s.l.

Four new lichenicolous Tremella species are described and characterized morphologically and molecularly. Tremella celata grows on Ramalina fraxinea, inducing the formation of inconspicuous galls, and having hyphae with incomplete clamps. Tremella endosporogena develops intrahymenially in the apothecia of Lecanora carpinea, having single-celled basidia and clampless hyphae. Tremella diederichiana is the name proposed for a species micromorphologically close to T. christiansenii but inducing the formation of small, pale galls on the thallus and apothecia of Lecidea aff. erythrophaea Tremella variae grows on Lecanora varia thallus, instead of on the apothecia, as do the other known Tremella species parasitizing Lecanora s.l. Phylogenetic relationships and host specificity of these species are investigated and compared with other taxa that show morphological resemblances, phylogenetic affinities or similar hosts. The formation of mitotic conidia inside old basidia (endospores), which is a poorly known reproductive strategy in the Basidiomycota, is also a distinctive character of Tremella endosporogena A discussion on the reproductive role and systematic implications of endospores is included.

Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi.

We studied the evolutionary history of the Parmeliaceae (Lecanoromycetes, Ascomycota), one of the largest families of lichen-forming fungi with complex and variable morphologies, also including several lichenicolous fungi. We assembled a six-locus data set including nuclear, mitochondrial and low-copy protein-coding genes from 293 operational taxonomic units (OTUs). The lichenicolous lifestyle originated independently three times in lichenized ancestors within Parmeliaceae, and a new generic name is introduced for one of these fungi. In all cases, the independent origins occurred c. 24 million yr ago. Further, we show that the Paleocene, Eocene and Oligocene were key periods when diversification of major lineages within Parmeliaceae occurred, with subsequent radiations occurring primarily during the Oligocene and Miocene. Our phylogenetic hypothesis supports the independent origin of lichenicolous fungi associated with climatic shifts at the Oligocene-Miocene boundary. Moreover, diversification bursts at different times may be crucial factors driving the diversification of Parmeliaceae. Additionally, our study provides novel insight into evolutionary relationships in this large and diverse family of lichen-forming ascomycetes.

Cardinal characters on a slippery slope--a re-evaluation of phylogeny, character evolution, and evolutionary rates in the jelly lichens (Collemataceae s. str).

Recent molecular systematic studies have indicated that the traits currently used for generic delimitation in the jelly lichens (Collemataceae s. str.), may not characterize monophyletic groups. Here we reconstruct the phylogeny of Collemataceae using Bayesian and maximum likelihood analyses based on mitochondrial (mtSSU rDNA) and nuclear (nuLSU rDNA, Beta-tubulin and MCM7) markers of 70 Collemataceae species. We studied the evolution of four morphological and ecological characters traditionally used to delimit genera and infra-generic groups. Finally, we tested if differences in branch-lengths between clades are due to differences in rates of molecular evolution. Eleven strongly supported groups were recovered in the resulting well-resolved and well-supported phylogeny. The presence/absence of a eucortex, which is currently used as the cardinal character to define genera in the group, does not characterize monophyletic groups corresponding to the genera as currently circumscribed. Ancestral state reconstruction indicates that the most recent common ancestor of the jelly lichens most likely was saxicolous/terricolous, lacked a tomentum, and had transversally septate ascospores. Although the cortex state could not be reconstructed for the ancestor of the family, our observations indicate that a lack of cortex may have an evolutionary advantage in saxicolous/terricolous species in semi-arid environments, as non-corticate species tends to be larger and occur in higher frequency and abundance in such regions, compared to corticate species. A significant evidence for faster evolutionary rates was found in a lineage mainly including taxa that occur in the wet tropics and humid temperate regions, compared to other lineages. We suggest that this can explain the greater diversity of Collemataceae in tropical and humid areas.

Mazaedium evolution in the Ascomycota (Fungi) and the classification of mazaediate groups of formerly unclear relationship.

Calicioid or mazaediate fungi constitute a heterogeneous assemblage of fungi sharing the presence of a mazaedium. These fungi were once treated as an order (Caliciales) of the Ascomycota but many are now known to be nested within the Arthoniomycetes, Eurotiomycetes, Lecanoromycetes and Leotiomycetes. In this study we employ multigene phylogenetic analyses of main mazaediate groups (based on nuclear 18S, 28S, 5.8S rDNA, mitochondrial 16S, and the protein coding RPB1 and Mcm7) of 116 taxa corresponding to most major groups of the inoperculate ascomycetes ("Leotiomyceta") and a selection of Pezizomycetes, to trace the evolution of the mazaedium in the Pezizomycotina (the "Euascomycetes"). In particular, we studied the placement of three calicioid groups of uncertain position, Calycidiaceae, Coniocybaceae and Microcaliciaceae. Here, we show that the Calycidiaceae is closely related to the Sphaerophoraceae in the Lecanoromycetidae (Lecanoromycetes), as supported by overall morphology and the production of sphaerophorin. The Coniocybaceae constitute an early divergent line in the inoperculate ascomycetes and here we propose to recognize this group formally as the new class and order Coniocybomycetes, Coniocybales. The Microcaliciaceae is nested within the Ostropomycetidae (Lecanoromycetes). Both Coniocybaceae and Microcaliciaceae, although highly distinctive, lack morphological similarities to related main fungal groups. Ancestral state reconstruction suggests that the ancestor of all inoperculate ascomycetes and the ancestor of all main inoperculate ascomycete groups, with the exception of the Coniocybomycetes, was non-mazediate, and thus confirms the large amount of parallel evolution and independent gains of the mazaedium in the history of the Ascomycota.

The relationships of Odontotrema (Odontotremataceae) and the resurrected Sphaeropezia (Stictidaceae)--new combinations and three new Sphaeropezia species.

Odontotremataceae is polyphyletic and constitutes two distantly related clades, the true Odontotremataceae and a segregate group within Stictidaceae including "Odontotrema" cassiopes, "O." diffindens, lichenicolous "Odontotrema" species and "Bryodiscus" arctoalpinus. Sphaeropezia here is accepted as the name for this latter group. An updated phylogeny of the Stictidaceae based on mtSSU, nuLSU and the protein coding gene RPB2 is presented together with a taxonomic revision of Swedish taxa of Odontotrema and Sphaeropezia. Bryodiscus and Lethariicola are synonymized under Sphaeropezia, and three new Sphaeropezia species are described: the lignicolous S. capreae, the fungicolous S. lyckselensis and the lichenicolous S. mycoblasti. The new species are distinguished from other species by molecular and morphological characters, and substrate preferences. The new combinations Sphaeropezia arctoalpina, S. cassiopes, S. grimmiae, S. hepaticarum, S. melaneliae, S. ochrolechiae and S. thamnoliae are proposed. The morphology of these species was studied in detail. We further propose to combine the remaining lichenicolous Odontotrema species, exept O. stereocaulicola, in Sphaeropezia based on their close relationship to the studied lichenicolous taxa. These additional new combinations include Sphaeropezia bryoriae, S. cucularis, S. figulina, S. intermedia, S. japewiae, S. lecanorae, S. navarinoi, S. pertusariae, S. rhizocarpicola, S. santessonii, and S. sipei. A lectotype is designated for the name Odontotrema diffindens Nyl.

Diversification of the newly recognized lichen-forming fungal lineage Montanelia (Parmeliaceae, Ascomycota) and its relation to key geological and climatic events.

PREMISE OF THE STUDY: In spite of the recent advances in generic and species circumscriptions and in recognizing species diversity in lichen-forming fungi, the timing of speciation and the factors that promote diversification in lichens remain largely unexplored. We used brown parmelioids as a model to assess the timing of divergence and explore the impact of geological and climatic events on lineage divergence and diversification in lichenized fungi. Additionally, to clarify the phylogenetic position of the species currently placed in Melanelia disjuncta group, we evaluated the taxonomic status and phylogenetic relationships within Parmeliaceae. • METHODS: Phylogenetic relationships and divergence time estimates were inferred from a four-loci data set. Alternative hypotheses were tested using Shimodaira-Hasegawa and expected likelihood weights tests. • KEY RESULTS: The M. disjuncta group forms a strongly supported, monophyletic lineage independent from Melanelia s.s. The M. disjuncta clade arose ca. 23.1 million years ago (Ma). Our results suggest that most of the lineages within the clade diversified during the Miocene (17.6 to 11.2 Ma). The split of other brown parmelioids, such as Emodomelanelia-Melanelixia occurred ca. 41.70 Ma, and the radiation of Melanelixia began during the Eocene-Oligocene transition (ca. 33.75 Ma). • CONCLUSIONS: Montanelia is described here as a new genus to accommodate species of the Melanelia disjuncta group. Further, the study indicates that the current species delimitation within the newly described genus requires revision. We provide evidence of lineage divergence of Montanelia at the Oligocene-Miocene boundary. Our results indicate that the diversification during Miocene would have happened during major mountain uplifts.

The yeast lichenosphere: high diversity of basidiomycetes from the lichens Tephromela atra and Rhizoplaca melanophthalma.

Lichens are well-known examples of complex symbiotic associations between organisms from different Kingdoms. Microfungi in particular, establish diverse associations with the hosting lichen thallus, as species-specific parasites or transient co-inhabitants. The whole community of lichen-associated fungi constitute the 'lichen mycobiome' comprising both ascomycetes and basidiomycetes, including filamentous and yeast taxa. Metabarcoding results and microscopy analyses show that in some thalli, basidiomycetes are frequent lichen-associated fungi but still only a few species could be axenically isolated and morphologically characterized. Within a broad project aiming at characterizing the mycobiome diversity by culture-dependent and independent approaches in two lichen species selected as reference models - Rhizoplaca melanophthalma and Tephromela atra, we succeed in isolating and culturing 76 new strains of basidiomycetous yeasts. The lichen thalli were collected in different mountain regions worldwide and at relatively high elevation. The yeast strains were isolated on different growth media and were studied for their morphological and genetic diversity. Nuclear internal transcribed spacer (ITS) and ribosomal large subunit (LSU) sequence analyses identified them to belong to ten families within the orders Agaricostilbomycetes, Cystobasidiomycetes, Microbotryomycetes, Tremellomycetes and Ustilaginomycetes. The yeasts here detected showed patterns of host-preference in a few cases and they are potentially related to the ecological conditions.

Large differences in carbohydrate degradation and transport potential among lichen fungal symbionts.

Lichen symbioses are thought to be stabilized by the transfer of fixed carbon from a photosynthesizing symbiont to a fungus. In other fungal symbioses, carbohydrate subsidies correlate with reductions in plant cell wall-degrading enzymes, but whether this is true of lichen fungal symbionts (LFSs) is unknown. Here, we predict genes encoding carbohydrate-active enzymes (CAZymes) and sugar transporters in 46 genomes from the Lecanoromycetes, the largest extant clade of LFSs. All LFSs possess a robust CAZyme arsenal including enzymes acting on cellulose and hemicellulose, confirmed by experimental assays. However, the number of genes and predicted functions of CAZymes vary widely, with some fungal symbionts possessing arsenals on par with well-known saprotrophic fungi. These results suggest that stable fungal association with a phototroph does not in itself result in fungal CAZyme loss, and lends support to long-standing hypotheses that some lichens may augment fixed CO2 with carbon from external sources.

Phylogeny and character evolution in the jelly fungi (Tremellomycetes, Basidiomycota, Fungi).

The Tremellomycetes (Agaricomycotina, Basidiomycota, Fungi) are a nutritionally heterogeneous group comprising saprotrophs, animal parasites, and fungicolous species (fungal-inhabiting, including lichen-inhabiting). The relationships of many species, particularly those with a lichenicolous habit, have never been investigated by molecular methods. We present a phylogeny of the Tremellomycetes based on three nuclear DNA ribosomal markers (nSSU, 5.8S and nLSU), representing all main taxonomic groups and life forms, including lichenicolous taxa. The Cystofilobasidiales, Filobasidiales, Holtermanniales, and Tremellales (including the Trichosporonales) are recovered as monophyletic, but this is not the case for the Tremellomycetes. We suggest, however, that the Cystofilobasidiales tentatively continue to be included in the Tremellomycetes. As currently circumscribed, the Filobasidiaceae, Sirobasidiaceae, Syzygosporaceae and Tremellaceae are non-monophyletic. Cuniculitremaceae, Sirobasidiaceae and Tetragoniomycetaceae are nested within Tremellaceae. The lichenicolous species currently included within the Tremellomycetes belong in this group, distributed across the Filobasidiales and Tremellales. Lichen-inhabiting taxa do not form a monophyletic group; they are distributed in several clades and sometimes intermixed with taxa of other nutritional habits. Character state reconstruction indicates that two morphological traits claimed to characterize groups in the Tremellomycetes (the basidium habit and basidium septation) are highly homoplastic. Comparative phylogenetic methods suggest that the transitions between single and catenulate basidia in the Tremellales are consistent with a punctuational model of evolution whereas basidium septation is likely to have evolved under a graduational model in the clade comprising the Holtermanniales, Filobasidiales, and Tremellales.

Using target enrichment sequencing to study the higher-level phylogeny of the largest lichen-forming fungi family: Parmeliaceae (Ascomycota).

Parmeliaceae is the largest family of lichen-forming fungi with a worldwide distribution. We used a target enrichment data set and a qualitative selection method for 250 out of 350 genes to infer the phylogeny of the major clades in this family including 81 taxa, with both subfamilies and all seven major clades previously recognized in the subfamily Parmelioideae. The reduced genome-scale data set was analyzed using concatenated-based Bayesian inference and two different Maximum Likelihood analyses, and a coalescent-based species tree method. The resulting topology was strongly supported with the majority of nodes being fully supported in all three concatenated-based analyses. The two subfamilies and each of the seven major clades in Parmelioideae were strongly supported as monophyletic. In addition, most backbone relationships in the topology were recovered with high nodal support. The genus Parmotrema was found to be polyphyletic and consequently, it is suggested to accept the genus Crespoa to accommodate the species previously placed in Parmotrema subgen. Crespoa. This study demonstrates the power of reduced genome-scale data sets to resolve phylogenetic relationships with high support. Due to lower costs, target enrichment methods provide a promising avenue for phylogenetic studies including larger taxonomic/specimen sampling than whole genome data would allow.

Contrasting Environmental Drivers Determine Biodiversity Patterns in Epiphytic Lichen Communities along a European Gradient.

Assessing the ecological impacts of environmental change on biological communities requires knowledge of the factors driving the spatial patterns of the three diversity facets along extensive environmental gradients. We quantified the taxonomic (TD), functional (FD), and phylogenetic diversity (PD) of lichen epiphytic communities in 23 beech forests along Europe to examine their response to environmental variation (climate, habitat quality, spatial predictors) at a continental geographic scale. We selected six traits related to the climatic conditions in forest ecosystems, the water-use strategy and the nutrient uptake, and we built a phylogenetic tree based on four molecular markers. FD and climate determined TD and PD, with spatial variables also affecting PD. The three diversity facets were primarily shaped by distinct critical predictors, with the temperature diurnal range affecting FD and PD, and precipitation of the wettest month determining TD. Our results emphasize the value of FD for explaining part of TD and PD variation in lichen communities at a broad geographic scale, while highlighting that these diversity facets provide complementary information about the communities' response under changing environmental conditions. Furthermore, traits such as growth form, photobiont type, and reproductive strategy mediated the response of lichen communities to abiotic factors emerging as useful indicators of macroclimatic variations.

Slippery when wet: phylogeny and character evolution in the gelatinous cyanobacterial lichens (Peltigerales, Ascomycetes).

Many lichen fungi form symbioses with filamentous Nostoc cyanobacteria, which cause the lichen to swell and become extremely gelatinous when moist. Within the Lecanoromycetes, such gelatinous lichens are today mainly classified in the Collemataceae (Peltigerales, Ascomycota). We performed Bayesian MCMC, maximum likelihood, and maximum parsimony analyses of three independent markers (mtSSU rDNA, nuLSU rDNA, and RPB1), to improve our understanding of the phylogeny and classification in the Peltigerales, as well as the evolution of morphological characters that have been used for classification purposes in this group. The Collemataceae and the non-gelatinous Pannariaceae are paraphyletic but can be re-circumscribed as monophyletic if Leciophysma, Physma, Ramalodium and Staurolemma are transferred to the Pannariaceae. The gelatinous taxa transferred to the Pannariaceae deviate from other Collemataceae in having simple ascospores, and several also have a ring-shaped exciple as in other Pannariaceae, rather than the disc-shaped exciple found in the typical Collemataceae. Both Collema and Leptogium are non-monophyletic. The re-circumscribed Collemataceae shares a distinct ascus type with the sister group Placynthiaceae and the Coccocarpiaceae, whereas Pannariaceae includes a variety of structures. All Pannariaceae have one-celled ascospores, whereas all Collemataceae have two- or multi-celled spores. Reconstructions of the number of character state transformations in exciple structure, thallus gelatinosity, and ascus apex structure indicate that the number of transformations is distinctly higher than the minimum possible. Most state transformations in the exciple took place from a ring-shaped to a disc-shaped exciple. Depending on the reconstruction method, most or all transformations in thallus structure took place from a non-gelatinous to a gelatinous thallus. Gains and losses of internal structures in the ascus apex account for all or a vast majority of the number of transformations in the ascus, whereas direct transformations between asci with internal structures appear to have been rare.

Species delimitation and evolution of metal bioaccumulation in the lichenized Acarospora smaragdula (Ascomycota, Fungi) complex.

The crustose lichenized fungi in the Acarosporaceae are splendid examples of organisms managing to survive in extremely harsh environments, such as highly mineralized rocks and low-pH habitats. Some representatives of the Acarospora smaragdula complex are known to accumulate substantial amounts of potentially toxic metals including iron and copper, resulting in populations with highly divergent coloration and morphology. These populations have often been treated as distinct species by lichen taxonomists. Parsimony and parsimony jackknifing analyses of ß-tubulin, nuclear ITS rDNA, and mtSSU rDNA sequence data sets was used to investigate the evolution of iron and copper accumulation and the production of the secondary compound norstictic acid in populations within the A. smaragdula species complex in Sweden, with additional samples mainly from Norway and the UK. Phylogenetic species recognition (concordance of single-gene phylogenies) was used to investigate species delimitations. Seven species are recognized in the complex. Atypically green, copper-accumulating samples, often given species rank, do not form a distinct group but are nested within A. smaragdula s. str., indicating that this ability is widespread in this species. Rust-coloured, iron-accumulating samples form two well supported separate groups, indicating that two morphologically distinct, obligate, iron-accumulating species are present, but facultatively iron-accumulating populations occur in at least one additional species. Norstictic acid, sometimes claimed to characterize the whole A. smaragdula complex, is only present in A. smaragdula s. str. The evolutionary significance of metal accumulation in Acarospora is discussed, as is the significance of our results for the application of phylogenetic species recognition/gene tree concordance-based species recognition, and DNA barcoding. © The Willi Hennig Society 2009.

Rostania revised: testing generic delimitations in Collemataceae (Peltigerales, Lecanoromycetes).

Here, we test the current generic delimitation of Rostania (Collemataceae, Peltigerales, Ascomycota) utilizing molecular phylogeny and morphological investigations. Using DNA sequence data from the mitochondrial SSU rDNA and two nuclear protein-coding genes (MCM7 and ß-tubulin) and utilizing parsimony, maximum likelihood and Bayesian phylogenetic methods, Rostania is shown to be non-monophyletic in the current sense. A new generic delimitation of Rostania is thus proposed, in which the genus is monophyletic, and three species (Rostaniacoccophylla, R.paramensis, R.quadrifida) are excluded and transferred to other genera. Rostaniaoccultata is further non-monophyletic, and a more detailed investigation of species delimitations in Rostania s. str. is needed. The new combinations Leptogiumparamense and Scytiniumquadrifidum are proposed.

Bacterial communities in an optional lichen symbiosis are determined by substrate, not algal photobionts.

Borderline lichens are simple mutualistic symbioses between fungi and algae, where the fungi form loose mycelia interweaving algal cells, instead of forming a lichen thallus. Schizoxylon albescens shows two nutritional modes: it can either live as a borderline lichen on Populus tremula bark or as a saprotroph on Populus wood. This enables us to investigate the microbiota diversity in simple fungal-algal associations and to study the impact of lichenization on the structure of bacterial communities. We sampled three areas in Sweden covering the distribution of Schizoxylon, and using high-throughput sequencing of the 16S rRNA gene and fluorescence in situ hybridization we characterized the associated microbiota. Bacterial communities in lichenized and saprotrophic Schizoxylon were clearly distinct, but when comparing the microbiota with the respective substrates, only the fruiting bodies show clear differences in composition and abundance from the communities in the substrates. The colonization by either lichenized or saprotrophic mycelia of Schizoxylon did not significantly influence the microbiota in the substrate. This suggests that in a morphologically simple form of lichenization, as represented by the Schizoxylon-Coccomyxa system, algal-fungal interactions do not significantly influence bacterial communities, but a more complex structure of the lichen thallus is likely required for hosting specific microbiota.

Multiple, Distinct Intercontinental Lineages but Isolation of Australian Populations in a Cosmopolitan Lichen-Forming Fungal Taxon, Psora decipiens (Psoraceae, Ascomycota).

Multiple drivers shape the spatial distribution of species, including dispersal capacity, niche incumbency, climate variability, orographic barriers, and plate tectonics. However, biogeographic patterns of fungi commonly do not fit conventional expectations based on studies of animals and plants. Fungi, in general, are known to occur across exceedingly broad, intercontinental distributions, including some important components of biological soil crust communities (BSCs). However, molecular data often reveal unexpected biogeographic patterns in lichenized fungal species that are assumed to have cosmopolitan distributions. The lichen-forming fungal species Psora decipiens is found on all continents, except Antarctica and occurs in BSCs across diverse habitats, ranging from hot, arid deserts to alpine habitats. In order to better understand factors that shape population structure in cosmopolitan lichen-forming fungal species, we investigated biogeographic patterns in the cosmopolitan taxon P. decipiens, along with the closely related taxa P. crenata and P. saviczii. We generated a multi-locus sequence dataset based on a worldwide sampling of these taxa in order to reconstruct evolutionary relationships and explore phylogeographic patterns. Both P. crenata and P. decipiens were not recovered as monophyletic; and P. saviczii specimens were recovered as a monophyletic clade closely related to a number of lineages comprised of specimens representing P. decipiens. Striking phylogeographic patterns were observed for P. crenata, with populations from distinct geographic regions belonging to well-separated, monophyletic lineages. South African populations of P. crenata were further divided into well-supported sub-clades. While well-supported phylogenetic substructure was also observed for the nominal taxon P. decipiens, nearly all lineages were comprised of specimens collected from intercontinental populations. However, all Australian specimens representing P. decipiens were recovered within a single well-supported monophyletic clade consisting solely of Australian samples. Our study supports up to 10 candidate species-level lineages in P. decipiens, based on genealogical concordance and coalescent-based species delimitation analyses. Our results support the general pattern of the biogeographic isolation of lichen-forming fungal populations in Australia, even in cases where closely related congeners have documented intercontinental distributions. Our study has important implications for understanding factors influencing diversification and distributions of lichens associated with BSC.