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

Tuovinen, Veera; Millanes, Ana M.; Freire-Rallo, Sandra; Rosling, Anna; Wedin, Mats

doi:10.1111/1462-2920.15455

Cited by 18 publications

(16 citation statements)

References 77 publications

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“…The origin of a lichen‐specific clade of yeasts from the basidiomycete class Cystobasidiomycetes appears broadly to coincide with the rise of parmelioid macrolichens in evolution about 100–200 million years ago (Spribille et al ., 2016; Nelsen et al ., 2020). More recently, the yeast stage of several species of lichen‐specific Tremella ( Basidiomycetes ) has been found to be a constant and abundant symbiont of the cortex and apothecial biofilm in species of Letharia (Tuovinen et al ., 2019), Alectoria (Tagirdzhanova et al ., 2021) and Lecanora (Tuovinen et al ., 2021). The predicted carbohydrate synthesis abilities of basidiomycete yeasts suggest they could modify the chemistry of the cortical biofilm, which could affect water uptake (Tagirdzhanova et al ., 2021).…”

Section: Evolution After Symbiosis Establishmentmentioning

confidence: 99%

Evolutionary biology of lichen symbioses

et al. 2022

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Lichens are the symbiotic outcomes of open, interspecies relationships, central to which are a fungus and a phototroph, typically an alga and/or cyanobacterium. The evolutionary processes that led to the global success of lichens are poorly understood. In this review, we explore the goods and services exchange between fungus and phototroph and how this propelled the success of both symbiont and symbiosis. Lichen fungal symbionts count among the only filamentous fungi that expose most of their mycelium to an aerial environment. Phototrophs export carbohydrates to the fungus, which converts them to specific polyols. Experimental evidence suggests that polyols are not only growth and respiratory substrates but also play a role in anhydrobiosis, the capacity to survive desiccation. We propose that this dual functionality is pivotal to the evolution of fungal symbionts, enabling persistence in environments otherwise hostile to fungi while simultaneously imposing costs on growth. Phototrophs, in turn, benefit from fungal protection from herbivory and light stress, while appearing to exert leverage over fungal sex and morphogenesis. Combined with the recently recognized habit of symbionts to occur in multiple symbioses, this creates the conditions for a multiplayer marketplace of rewards and penalties that could drive symbiont selection and lichen diversification.

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Section: Evolution After Symbiosis Establishmentmentioning

confidence: 99%

Evolutionary biology of lichen symbioses

et al. 2022

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“…Lichen holobionts are complex systems individualized from cyclical symbiotic associations [1], which represent one of the most paradigmatic examples of ecologically obligate mutualistic interactions between at least two organismal groups [2]: a fungus (the mycobiont) and a population of photosynthetic green or blue-green algae (the photobionts). The definition of lichens has lately been expanded to include other fungi [3,4], basidiomycete yeasts [5][6][7][8], non-photosynthetic bacteria [9][10][11][12][13] and additional populations of green microalgae [14][15][16][17][18].…”

Section: Introductionmentioning

confidence: 99%

Unravelling the Symbiotic Microalgal Diversity in Buellia zoharyi (Lichenized Ascomycota) from the Iberian Peninsula and Balearic Islands Using DNA Metabarcoding

Moya¹,

Chiva²,

Molins³

et al. 2021

Diversity

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Buellia zoharyi is a crustose placodioid lichen, usually occurring on biocrusts of semiarid ecosystems in circum-Mediterranean/Macaronesian areas. In previous work, we found that this lichenized fungus was flexible in its phycobiont choice in the Canary Islands. Here we test whether geography and habitat influence phycobiont diversity in populations of this lichen from the Iberian Peninsula and Balearic Islands using Sanger and high throughput sequencing (HTS). Additionally, three thallus section categories (central, middle and periphery) were analyzed to explore diversity of microalgal communities in each part. We found that B. zoharyi populations hosted at least three different Trebouxia spp., and this lichen can associate with distinct phycobiont strains in different habitats and geographic regions. This study also revealed that the Trebouxia composition of this lichen showed significant differences when comparing the Iberian Peninsula with the Balearics thalli. No support for differences in microalgal communities was found among thallus sections; however, several thalli showed different predominant Trebouxia spp. at each section. This result corroborate that thallus parts selected for DNA extraction in metabarcoding analyses are key to not bias the total phycobiont diversity detected. This study highlights that inclusion of HTS analysis is crucial to understand lichen symbiotic microalgal diversity.

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“…The two main groups of SFSs, members of the basidiomycete orders Cyphobasidiales and Tremellales, were both known in lichens prior to their discovery as yeasts by their fertile, hyphal forms. These are rare but easier to spot than yeasts, in the form of gall-like protrusions on lichen thalli ( Tuovinen et al 2019 , 2021 ). Their relationship to known mycoparasites has led others to suspect that they parasitize the core ascomycete symbiont ( Millanes et al 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Predicted Input of Uncultured Fungal Symbionts to a Lichen Symbiosis from Metagenome-Assembled Genomes

Tagirdzhanova

Saary

Tingley

et al. 2021

Genome Biology and Evolution

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Basidiomycete yeasts have recently been reported as stably associated secondary fungal symbionts (SFSs) of many lichens, but their role in the symbiosis remains unknown. Attempts to sequence their genomes have been hampered both by the inability to culture them and their low abundance in the lichen thallus alongside two dominant eukaryotes (an ascomycete fungus and chlorophyte alga). Using the lichen Alectoria sarmentosa, we selectively dissolved the cortex layer in which SFSs are embedded to enrich yeast cell abundance and sequenced DNA from the resulting slurries as well as bulk lichen thallus. In addition to yielding a near-complete genome of the filamentous ascomycete using both methods, metagenomes from cortex slurries yielded a 36- to 84-fold increase in coverage and near-complete genomes for two basidiomycete species, members of the classes Cystobasidiomycetes and Tremellomycetes. The ascomycete possesses the largest gene repertoire of the three. It is enriched in proteases often associated with pathogenicity and harbours the majority of predicted secondary metabolite clusters. The basidiomycete genomes possess ∼35% fewer predicted genes than the ascomycete and have reduced secretomes even compared to close relatives, while exhibiting signs of nutrient limitation and scavenging. Furthermore, both basidiomycetes are enriched in genes coding for enzymes producing secreted acidic polysaccharides, representing a potential contribution to the shared extracellular matrix. All three fungi retain genes involved in dimorphic switching, despite the ascomycete not being known to possess a yeast stage. The basidiomycete genomes are an important new resource for exploration of lifestyle and function in fungal-fungal interactions in lichen symbioses.

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

Cited by 18 publications

References 77 publications

Evolutionary biology of lichen symbioses

Evolutionary biology of lichen symbioses

Unravelling the Symbiotic Microalgal Diversity in Buellia zoharyi (Lichenized Ascomycota) from the Iberian Peninsula and Balearic Islands Using DNA Metabarcoding

Predicted Input of Uncultured Fungal Symbionts to a Lichen Symbiosis from Metagenome-Assembled Genomes

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