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Two Basidiomycete Fungi in the Cortex of Wolf Lichens

2019; Elsevier BV; Volume: 29; Issue: 3 Linguagem: Inglês

10.1016/j.cub.2018.12.022

1879-0445

Veera Tuovinen, Stefan Ekman, Göran Thor, Dan Vanderpool, Toby Spribille, Hanna Johannesson,

Plant Pathogens and Fungal Diseases

Since the late 1800s, mycologists have been detecting fungi above and beyond the assumed single fungus in lichen thalli [1Zopf W. Über Nebensymbiose (Parasymbiose).Plant Biol. 1897; 15: 90-92Google Scholar, 2Hawksworth D.L. Secondary fungi in lichen symbioses: parasites, saprophytes and parasymbionts.J. Hattori Bot. Lab. 1982; 52: 357-366Google Scholar, 3Petrini O. Hake U. Dreyfuss M.M. An analysis of fungal communities isolated from fruticose lichens.Mycologia. 1990; 82: 444-451Crossref Google Scholar, 4Arnold A.E. Miadlikowska J. Higgins K.L. Sarvate S.D. Gugger P. Way A. Hofstetter V. Kauff F. Lutzoni F. A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification?.Syst. Biol. 2009; 58: 283-297Crossref PubMed Scopus (265) Google Scholar, 5Bates S.T. Berg-Lyons D. Lauber C.L. Walters W.A. Knight R. Fierer N. A preliminary survey of lichen associated eukaryotes using pyrosequencing.Lichenologist. 2012; 44: 137-146Crossref Scopus (58) Google Scholar, 6Park C.H. Kim K.M. Elvebakk A. Kim O.S. Jeong G. Hong S.G. Algal and fungal diversity in Antarctic lichens.J. Eukaryot. Microbiol. 2015; 62: 196-205Crossref PubMed Scopus (48) Google Scholar]. Over the last century, these fungi have been accorded roles ranging from commensalists to pathogens. Recently, Cyphobasidiales yeasts were shown to be ubiquitous in the cortex layer of many macrolichens [7Spribille T. Tuovinen V. Resl P. Vanderpool D. Wolinski H. Aime M.C. Schneider K. Stabentheiner E. Toome-Heller M. Thor G. et al.Basidiomycete yeasts in the cortex of ascomycete macrolichens.Science. 2016; 353: 488-492Crossref PubMed Scopus (309) Google Scholar], but for most species, little is known of their cellular distribution and constancy beyond visible fruiting structures. Here, we demonstrate the occurrence of an additional and distantly related basidiomycete, Tremella, in 95% of studied thalli in a global sample of one of the most intensively studied groups of lichens, the wolf lichens (genus Letharia). Tremella species are reported from a wide range of lichen genera [8Lawrey, J.D., and Diederich, P. (2018). Lichenicolous fungi – worldwide checklist, including isolated cultures and sequences available. http://www.lichenicolous.net.Google Scholar], but until now, their biology was deduced from fruiting bodies (basidiomata) formed on lichen thalli. Based on this, they have been thought to be uncommon to rare, to occur exclusively in a hyphal form, and to be parasitic on the dominant fungal partner [9Diederich, P. (1996). The Lichenicolous Heterobasidiomycetes (J. Cramer), pp. 1–169.Google Scholar, 10Zamora J.C. Millanes A.M. Wedin M. Rico V.J. Pérez-Ortega S. Understanding lichenicolous heterobasidiomycetes: new taxa and reproductive innovations in Tremella s.l.Mycologia. 2016; 108: 381-396Crossref PubMed Scopus (20) Google Scholar]. We show that, in wolf lichens, Tremella occurs as yeast cells also in thalli that lack basidiomata and infer that this is its dominant stage in nature. We further show that the hyphal stage, when present in Letharia, is in close contact with algal cells, challenging the assumption that lichen-associated Tremella species are uniformly mycoparasites. Our results suggest that extent of occurrence and cellular interactions of known fungi within lichens have historically been underestimated and raise new questions about their function in specific lichen symbioses.