Secondary metabolites are a heterogeneous class of chemicals that often mediate interactions between species. The tryptophan‐derived secondary metabolite, psilocin, is a serotonin receptor agonist that induces altered states of consciousness. A phylogenetically disjunct group of mushroom‐forming fungi in the Agaricales produce the psilocin prodrug, psilocybin. Spotty phylogenetic distributions of fungal compounds are sometimes explained by horizontal transfer of metabolic gene clusters among unrelated fungi with overlapping niches. We report the discovery of a psilocybin gene cluster in three hallucinogenic mushroom genomes, and evidence for its horizontal transfer between fungal lineages. Patterns of gene distribution and transmission suggest that synthesis of psilocybin may have provided a fitness advantage in the dung and late wood‐decay fungal niches, which may serve as reservoirs of fungal indole‐based metabolites that alter behavior of mycophagous and wood‐eating invertebrates. These hallucinogenic mushroom genomes will serve as models in neurochemical ecology, advancing the (bio)prospecting and synthetic biology of novel neuropharmaceuticals.
Abstract:1 Secondary metabolites are heterogeneous natural products that often mediate 2 interactions between species. The tryptophan--derived secondary metabolite, 3 psilocin, is a serotonin receptor agonist that induces altered states of consciousness. 4A phylogenetically disjunct group of mushroom--forming fungi in the Agaricales 5 produce the psilocin prodrug, psilocybin. Spotty phylogenetic distributions of fungal 6 compounds are sometimes explained by horizontal transfer of metabolic gene 7 clusters among unrelated fungi with overlapping niches. We report the discovery of 8 a psilocybin gene cluster in three hallucinogenic mushroom genomes, and evidence 9 for its horizontal transfer between fungal lineages. Patterns of gene distribution and 10 transmission suggest that psilocybin provides a fitness advantage in the dung and 11 late wood--decay niches, which may be reservoirs of fungal indole--based metabolites 12 that alter behavior of mycophagous and wood--eating invertebrates. These 13 hallucinogenic mushroom genomes will serve as models in neurochemical ecology, 14 advancing the prospecting and synthetic biology of novel neuropharmaceuticals. 15 16 peer-reviewed)
agarics or mushroom-forming fungi that typically occur on or with bryophytes-particularly mosses or liverworts-or that occur on soil (Redhead et al., 2002) (Fig. 1). These non-lignicolous fungi, particularly the bryophilous agarics (Racovitza, 1959;Davey and Currah, 2006), were previously treated as Agaricales Underw. due to similarities in basidiome morphology (Redhead et al., 2002) but were recovered in the Hymenochaetales by molecular phylogenetic analyses (Moncalvo et al., 2000(Moncalvo et al., , 2002Redhead et al., 2002). Later, the group was referred to as the Rickenella clade (Larsson et al., 2006) and classified in the family Rickenellaceae Vizzini (Vizzini, 2010;Nakasone and Burdsall, 2012), the name of which, unfortunately, is illegitimate due to inclusion of the type of the earlier described family Repetobasidiaceae Jülich (Jülich, 1981). In addition, the diversity of its constituents is unsettled, the monophyly of the group has been questioned (
Mosses harbor fungi whose interactions within their hosts remain largely unexplored. Trophic ranges of fungal endophytes from the moss Dicranum scoparium were hypothesized to encompass saprotrophism. This moss is an ideal host to study fungal trophic lability because of its natural senescence gradient, and because it can be grown axenically.Dicranum scoparium was co-cultured with each of eight endophytic fungi isolated from naturally occurring D. scoparium. Moss growth rates, and gene expression levels (RNA sequencing) of fungi and D. scoparium, were compared between axenic and co-culture treatments. Functional lability of two fungal endophytes was tested by comparing their RNA expression levels when colonizing living vs dead gametophytes.Growth rates of D. scoparium were unchanged, or increased, when in co-culture. One fungal isolate (Hyaloscyphaceae sp.) that promoted moss growth was associated with differential expression of auxin-related genes. When grown with living vs dead gametophytes, Coniochaeta sp. switched from having upregulated carbohydrate transporter activity to upregulated oxidation-based degradation, suggesting an endophytism to saprotrophism transition. However, no such transition was detected for Hyaloscyphaceae sp.Individually, fungal endophytes did not negatively impact growth rates of D. scoparium. Our results support the long-standing hypothesis that some fungal endophytes can switch to saprotrophism.
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