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

Basidiomycete yeasts have recently been reported as stably associated secondary fungal symbionts 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...

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Autores principales: Tagirdzhanova, Gulnara, Saary, Paul, Tingley, Jeffrey P, Díaz-Escandón, David, Abbott, D Wade, Finn, Robert D, Spribille, Toby
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8355462/
https://www.ncbi.nlm.nih.gov/pubmed/33693712
http://dx.doi.org/10.1093/gbe/evab047
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author Tagirdzhanova, Gulnara
Saary, Paul
Tingley, Jeffrey P
Díaz-Escandón, David
Abbott, D Wade
Finn, Robert D
Spribille, Toby
author_facet Tagirdzhanova, Gulnara
Saary, Paul
Tingley, Jeffrey P
Díaz-Escandón, David
Abbott, D Wade
Finn, Robert D
Spribille, Toby
author_sort Tagirdzhanova, Gulnara
collection PubMed
description Basidiomycete yeasts have recently been reported as stably associated secondary fungal symbionts 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 secondary fungal symbionts 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 harbors the majority of predicted secondary metabolite clusters. The basidiomycete genomes possess ∼35% fewer predicted genes than the ascomycete and have reduced secretomes even compared with 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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spelling pubmed-83554622021-08-11 Predicted Input of Uncultured Fungal Symbionts to a Lichen Symbiosis from Metagenome-Assembled Genomes Tagirdzhanova, Gulnara Saary, Paul Tingley, Jeffrey P Díaz-Escandón, David Abbott, D Wade Finn, Robert D Spribille, Toby Genome Biol Evol Research Article Basidiomycete yeasts have recently been reported as stably associated secondary fungal symbionts 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 secondary fungal symbionts 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 harbors the majority of predicted secondary metabolite clusters. The basidiomycete genomes possess ∼35% fewer predicted genes than the ascomycete and have reduced secretomes even compared with 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. Oxford University Press 2021-03-09 /pmc/articles/PMC8355462/ /pubmed/33693712 http://dx.doi.org/10.1093/gbe/evab047 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Tagirdzhanova, Gulnara
Saary, Paul
Tingley, Jeffrey P
Díaz-Escandón, David
Abbott, D Wade
Finn, Robert D
Spribille, Toby
Predicted Input of Uncultured Fungal Symbionts to a Lichen Symbiosis from Metagenome-Assembled Genomes
title Predicted Input of Uncultured Fungal Symbionts to a Lichen Symbiosis from Metagenome-Assembled Genomes
title_full Predicted Input of Uncultured Fungal Symbionts to a Lichen Symbiosis from Metagenome-Assembled Genomes
title_fullStr Predicted Input of Uncultured Fungal Symbionts to a Lichen Symbiosis from Metagenome-Assembled Genomes
title_full_unstemmed Predicted Input of Uncultured Fungal Symbionts to a Lichen Symbiosis from Metagenome-Assembled Genomes
title_short Predicted Input of Uncultured Fungal Symbionts to a Lichen Symbiosis from Metagenome-Assembled Genomes
title_sort predicted input of uncultured fungal symbionts to a lichen symbiosis from metagenome-assembled genomes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8355462/
https://www.ncbi.nlm.nih.gov/pubmed/33693712
http://dx.doi.org/10.1093/gbe/evab047
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