Mycena genomes resolve the evolution of fungal bioluminescence

Abstract

Mushroom-forming fungi in the order Agaricales represent an independent origin of bioluminescence in the tree of life; yet the diversity, evolutionary history, and timing of the origin of fungal luciferases remain elusive. We sequenced the genomes and transcriptomes of five bonnet mushroom species (Mycena spp.), a diverse lineage comprising the majority of bioluminescent fungi. Two species with haploid genome assemblies ∼150 Mb are among the largest in Agaricales, and we found that a variety of repeats between Mycena species were differentially mediated by DNA methylation. We show that bioluminescence evolved in the last common ancestor of mycenoid and the marasmioid clade of Agaricales and was maintained through at least 160 million years of evolution. Analyses of synteny across genomes of bioluminescent species resolved how the luciferase cluster was derived by duplication and translocation, frequently rearranged and lost in most Mycena species, but conserved in the Armillaria lineage. Luciferase cluster members were coexpressed across developmental stages, with the highest expression in fruiting body caps and stipes, suggesting fruiting-related adaptive functions. Our results contribute to understanding a de novo origin of bioluminescence and the corresponding gene cluster in a diverse group of enigmatic fungal species.

Gene age predicts the transcriptional landscape of sexual morphogenesis in multicellular fungi

“…S3). For uniformity in downstream analyses, we reanalysed data from former studies (Almási et al, 2019;Gehrmann et al, 2018;Ke et al, 2020;Krizsán et al, 2019;Liu et al, 2018;Sipos et al, 2017), yielding data for eight species in the order Agaricales, which comprises a single origin of complex fruiting body morphologies (Marisol et al, 2020;Varga et al, 2019). P. ostreatus and Pt.…”

Light and Autofluorescence, Multitasking Features in Living Organisms

“…Luciferase is reported to originate in Agaricales, and it is currently detectable in Armillaria and Mycene species. 3-hydroxyhispidin, the hydroxylated hispidin, is the luciferine [251]. To note, the different effects of prolactine (PRL) and c-aminobutyric acid (GABA); respectively negative and positive common effects of amelanocyte-stimulating hormone (a-MSH) and melatonin (Mt); almost uninfluential effects of nitric oxide (NO).…”

“…Luciferase is reported to originate in Agaricales, and it is currently detectable in Armillaria and Mycene species. 3-hydroxyhispidin, the hydroxylated hispidin, is the luciferine [251].…”

Occurrence of bioluminescent and nonbioluminescent species in the littoral earthworm genus Pontodrilus

“…S2 ) 8 . The presence of both luminous and nonluminous species in a single genus is likely widespread, but only a few examples have been confirmed; for example, the genera Vibrio and Photobacterium (marine bacteria) 9 , Epigonus (deep-sea fishes) 10 , Mycena (bonnet mushrooms) 11 and Eisenia (terrestrial earthworms) 12 have been reported to contain both luminous and nonluminous species. P. litoralis and P. longissimus can easily be collected at the same beach 8 and reared in a laboratory; thus, they are suitable for studying the ecology and evolution of bioluminescence.…”