Extreme overall mushroom genome expansion in Mycena s.s. irrespective of plant hosts or substrate specializations

• Published in: Cell genomics Vol. 4; no. 7; p. 100586
• Main Authors: Harder, Christoffer Bugge, Miyauchi, Shingo, Virágh, Máté, Kuo, Alan, Thoen, Ella, Andreopoulos, Bill, Lu, Dabao, Skrede, Inger, Drula, Elodie, Henrissat, Bernard, Morin, Emmanuelle, Kohler, Annegret, Barry, Kerrie, LaButti, Kurt, Salamov, Asaf, Lipzen, Anna, Merényi, Zsolt, Hegedüs, Botond, Baldrian, Petr, Stursova, Martina, Weitz, Hedda, Taylor, Andy, Koriabine, Maxim, Savage, Emily, Grigoriev, Igor V., Nagy, László G., Martin, Francis, Kauserud, Håvard
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 10.07.2024; Elsevier
• Subjects: Agaricales - genetics; Arctic biology; Biologi; Biological Sciences; biotrophy–saprotrophy evolution; carbon degradation; DNA Transposable Elements - genetics; Evolution, Molecular; fungal genomics; fungal guild; Gene Transfer, Horizontal; Genetics; Genetik; genome size diversity; Genome, Fungal - genetics; Natural Sciences; Naturvetenskap; Phylogeny; plant-fungus interactions; Plants - genetics; Plants - microbiology; root-associations; saprotrophs; TE proliferation; carbon degradation; fungal guild; genome size diversity; plant-fungus interactions; fungal genomics; TE proliferation; biotrophy–saprotrophy evolution; root-associations; saprotrophs; Arctic biology
• ISSN: 2666-979X; 2666-979X
• DOI: 10.1016/j.xgen.2024.100586

Mycena s.s. is a ubiquitous mushroom genus whose members degrade multiple dead plant substrates and opportunistically invade living plant roots. Having sequenced the nuclear genomes of 24 Mycena species, we find them to defy the expected patterns for fungi based on both their traditionally perceived saprotrophic ecology and substrate specializations. Mycena displayed massive genome expansions overall affecting all gene families, driven by novel gene family emergence, gene duplications, enlarged secretomes encoding polysaccharide degradation enzymes, transposable element (TE) proliferation, and horizontal gene transfers. Mainly due to TE proliferation, Arctic Mycena species display genomes of up to 502 Mbp (2–8× the temperate Mycena), the largest among mushroom-forming Agaricomycetes, indicating a possible evolutionary convergence to genomic expansions sometimes seen in Arctic plants. Overall, Mycena show highly unusual, varied mosaic-like genomic structures adaptable to multiple lifestyles, providing genomic illustration for the growing realization that fungal niche adaptations can be far more fluid than traditionally believed. [Display omitted] •Mycena have the largest mushroom genomes hitherto found•Caused by TE proliferation, novel gene families, duplications, and enlarged secretomes•Their genome structures are fit for multiple lifestyles•Arctic Mycena strain genomes are particularly large, mimicking Arctic plant genomes Mycena genome sizes and structure do not follow the expectations from their supposed saprotrophic ecological specializations. Instead, they are overall highly expanded in size in all aspects with multiple genes enabling them for different lifestyles. Certain Arctic Mycena strains have the largest mushroom genomes hitherto found.