Tangerine: a Starship-like element in the genomes of Xanthoria lichen-forming fungi

Abstract

Lichens are symbiotic associations between filamentous fungi and photosynthetic micro-organisms, such as green algae and/or cyanobacteria, that result in a single anatomically-complex structure that can thrive in environments inhospitable to most organisms, including arctic tundra, high mountains, and deserts. Recent evidence suggests that lichens may be even more complex than previously appreciated, containing multiple microbial constituents, but how genomes of the principal fungal symbiont (which provides the majority of biomass in lichen tissue) have been shaped during evolution is largely unexplored. Recently, giant transposable elements called Starships have been found in many genomes of filamentous fungi, but to which extent they occur in lichen-forming fungi is not known. In this report, we describe a Starship element from the lichen fungus Xanthoria parietina. This element, named Tangerine, contains several genes that have signatures of horizontal gene transfer from non-lichen-forming fungi, most likely from black yeasts of the Chaetothyriales, that are often lichen-associated. Repetitive sequences carried by Tangerine, and found in other sites in Xanthoria genomes, are affected by repeat-induced point mutation (RIP), a mechanism of genome defense against transposable elements, consistent with fungal sexual reproduction which always precedes new lichen formation by Xanthoria. Tangerines "captain" belongs to a newly defined family of tyrosine recombinases specific to lichen-forming Lecanoromycetes. Several other captain clades have signatures of horizontal gene transfer between distantly related lichen-forming fungi and non-mycobiont lichen-associated fungi. We speculate that Starships may play a significant, yet hitherto unrecognized role, in lichen genome evolution and provide a roadmap for further investigation.