A taxonomically broad metagenomic survey of 339 species spanning 57 families suggests cystobasidiomycete yeasts are not ubiquitous across all lichens

Premise Lichens are fungi that enter into obligate symbioses with photosynthesizing organisms (algae, cyanobacteria). Traditional narratives of lichens as binary symbiont pairs have given way to their recognition as dynamic metacommunities. Basidiomycete yeasts, particularly of the genus Cyphobasidium, have been inferred to be widespread and important components of lichen metacommunities. Yet, the presence of basidiomycete yeasts across a wide diversity of lichen lineages has not previously been tested. Methods We searched for lichen-associated cystobasidiomycete yeasts in newly generated metagenomic data from 413 samples of 339 lichen species spanning 57 families and 25 orders. The data set was generated as part of a large-scale project to study lichen biodiversity gradients in the southern Appalachian Mountains Biodiversity Hotspot of southeastern North America. Results Our efforts detected cystobasidiomycete yeasts in nine taxa (Bryoria nadvornikiana, Heterodermia leucomelos, Lecidea roseotincta, Opegrapha vulgata, Parmotrema hypotropum, P. subsumptum, Usnea cornuta, U. strigosa, and U. subgracilis), representing 2.7% of all species sampled. Seven of these taxa (78%) are foliose (leaf-like) or fruticose (shrubby) lichens that belong to families where basidiomycete yeasts have been previously detected. In several of the nine cases, cystobasidiomycete rDNA coverage was comparable to, or greater than, that of the primary lichen fungus single-copy nuclear genomic rDNA, suggesting sampling artifacts are unlikely to account for our results. Conclusions Studies from diverse areas of the natural sciences have led to the need to reconceptualize lichens as dynamic metacommunities. However, our failure to detect cystobasidiomycetes in 97.3% (330 species) of the sampled species suggests that basidiomycete yeasts are not ubiquitous in lichens.