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.

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.

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.