Unintended consequences: the escape of an invasive mushroom and its impacts on animal and microbial biodiversity

Mushrooms are often moved across and between continents, but how invasive mushrooms impact the biodiversity of animals or microbes in novel ranges remains unknown. The deadly Amanita phalloides (or death cap) has invaded local forests in California and is now common throughout the western coast of North America. The fungus produces a plethora of specialized metabolites (SMs), and while SMs may play an essential role in protecting spores, what the SMs are protecting spores against remains mysterious. Building on long-standing claims, we hypothesize the toxins are a defense against potentially antagonistic invertebrates, and we further hypothesize the metabolites act against microbial competitors in soils. We believe SMs play a role in fungal invasion biology, and the Californian A. phalloides’ have an ecological advantage because they have escaped co-evolved natural enemies and their SMs are acting as a novel defense against naïve competitors lacking co-evolved resistance to the death cap’s chemistry. To test our hypotheses, we asked 1) do native and invasive death caps host unique invertebrates compared to other co-occurring Amanita? and 2) do invasive death caps host a lower diversity of invertebrates compared to native European death caps? Next, we asked 3) is there a change in microbial diversity and community composition when the death cap’s toxins leach into Californian soils? We characterized the communities of invertebrates found in A. phalloides and related Amanita mushrooms collected from invasive and native ranges using metabarcoding. Our data support our hypothesis, showing the death caps have unique invertebrate communities compared to co-occurring Amanita and Californian death caps house significantly lower invertebrate biodiversity compared to native death caps. We are now characterizing the microbial communities in soils collected from beneath invasive A. phalloides’ and testing for the presence of toxins and metabolites. Our preliminary results confirm the toxins are leaching into the native soils of California. By characterizing fungal and bacterial communities, we are describing differences in microbial diversity and composition in the presence of the death cap’s SMs. Our research lays the foundation for understanding how invasive mushrooms change local biodiversity and mechanisms behind their successful advancement.