Genome-level analyses resolve an ancient lineage of symbiotic ascomycetes

David Díaz-Escandón; Gulnara Tagirdzhanova; Dan Vanderpool; Carmen C G Allen; André Aptroot; Oluna Češka; David L Hawksworth; Alejandro Huereca; Kerry Knudsen; Jana Kocourková; Robert Lücking; Philipp Resl; Toby Spribille

doi:10.1016/j.cub.2022.11.014

Genome-level analyses resolve an ancient lineage of symbiotic ascomycetes

Curr Biol. 2022 Dec 5;32(23):5209-5218.e5. doi: 10.1016/j.cub.2022.11.014. Epub 2022 Nov 23.

Affiliations

¹ Department of Biological Sciences CW405, University of Alberta, Edmonton, AB T6G 2R3, Canada.
² National Genomics Center for Wildlife and Fish Conservation, Rocky Mountain Research Station, 800 E Beckwith, Missoula, MT 59812, USA.
³ Laboratório de Botânica / Liquenologia, Instituto de Biociências Universidade Federal de Mato Grosso do Sul, Avenida Costa e Silva s/n Bairro Universitário, Campo Grande, Mato Grosso do Sul CEP 79070-900, Brazil.
⁴ Victoria, BC, Canada.
⁵ Comparative Fungal Biology, Royal Botanic Gardens, Kew, Surrey TW9 3DS, UK; Department of Life Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK; Jilin Agricultural University, Changchun, Jilin Province 130118, China.
⁶ Czech University of Life Sciences, Faculty of Environmental Sciences, Department of Ecology, Kamýcká 129, Praha-Suchdol 165 00, Czech Republic.
⁷ Botanischer Garten, Freie Universität Berlin, Königin-Luise-Straße 6-8, 14195 Berlin, Germany.
⁸ Institute of Biology, University of Graz, Universitätsplatz 2, 8010 Graz, Austria.
⁹ Department of Biological Sciences CW405, University of Alberta, Edmonton, AB T6G 2R3, Canada. Electronic address: toby.spribille@ualberta.ca.

PMID: 36423639
DOI: 10.1016/j.cub.2022.11.014

Abstract

Ascomycota account for about two-thirds of named fungal species.¹ Over 98% of known Ascomycota belong to the Pezizomycotina, including many economically important species as well as diverse pathogens, decomposers, and mutualistic symbionts.² Our understanding of Pezizomycotina evolution has until now been based on sampling traditionally well-defined taxonomic classes.³^,⁴^,⁵ However, considerable diversity exists in undersampled and uncultured, putatively early-diverging lineages, and the effect of these on evolutionary models has seldom been tested. We obtained genomes from 30 putative early-diverging lineages not included in recent phylogenomic analyses and analyzed these together with 451 genomes covering all available ascomycete genera. We show that 22 of these lineages, collectively representing over 600 species, trace back to a single origin that diverged from the common ancestor of Eurotiomycetes and Lecanoromycetes over 300 million years BP. The new clade, which we recognize as a more broadly defined Lichinomycetes, includes lichen and insect symbionts, endophytes, and putative mycorrhizae and encompasses a range of morphologies so disparate that they have recently been placed in six different taxonomic classes. To test for shared hidden features within this group, we analyzed genome content and compared gene repertoires to related groups in Ascomycota. Regardless of their lifestyle, Lichinomycetes have smaller genomes than most filamentous Ascomycota, with reduced arsenals of carbohydrate-degrading enzymes and secondary metabolite gene clusters. Our expanded genome sample resolves the relationships of numerous "orphan" ascomycetes and establishes the independent evolutionary origins of multiple mutualistic lifestyles within a single, morphologically hyperdiverse clade of fungi.

Keywords: Lichinomycetes; carbohydrate-active enzymes; comparative genomics; endosymbiosis; functional annotation; fungal genomes; genome reduction; lichens; metagenomics; mycorrhizae.