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.

Architecture et Fonction des Macromolécules Biologiques CNRS Aix Marseille Université 163 avenue de Luminy 13288 Marseille France

Architecture et Fonction des Macromolécules Biologiques CNRS Aix Marseille Université 163 avenue de Luminy 13288 Marseille France; INRAE UMR 1163 Biodiversité et Biotechnologie Fongiques 13009 Marseille France

Department of Biosciences University of Oslo Box 1066 Blindern 0316 Oslo Norway

Department of Biosciences University of Oslo Box 1066 Blindern 0316 Oslo Norway; Department of Biology Microbial Ecology Group Biology Department Lund University Lund Sweden; University of Copenhagen Department of Biology Section of Terrestrial Ecology 2100 Copenhagen Ø Denmark

Institute of Microbiology of the Czech Academy of Sciences Videnska 1083 14220 Prague 4 Czech Republic

Okinawa Institute of Science and Technology Graduate University Onna Okinawa 904 0495 Japan; Université de Lorraine INRAE UMR Interactions Arbres Microorganismes Centre INRAE Grand Est Nancy 54280 Champenoux France

School of Biological Sciences University of Aberdeen Aberdeen UK

School of Biological Sciences University of Aberdeen Aberdeen UK; The James Hutton Institute Aberdeen UK

Synthetic and Systems Biology Unit Institute of Biochemistry Biological Research Centre HUN REN Szeged 6726 Szeged Hungary

U S Department of Energy Joint Genome Institute Lawrence Berkeley National Laboratory Berkeley CA 94720 USA

U S Department of Energy Joint Genome Institute Lawrence Berkeley National Laboratory Berkeley CA 94720 USA; Department of Plant and Microbial Biology University of California Berkeley Berkeley CA 94720 USA

Université de Lorraine INRAE UMR Interactions Arbres Microorganismes Centre INRAE Grand Est Nancy 54280 Champenoux France

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