Equipped for success: genomes and metabolomes of the European Amanita muscaria are conserved in its novel South African range

Plants and soils have been moved around the world for centuries, but invasive mushrooms receive scant attention. The Amanita muscaria species complex was introduced to South Africa in the context of forestry, but its origins, ecology and recent evolution are unstudied. We sequenced the genomes of 24 Northern and Southern Hemisphere A. muscaria, built phylogenies and reconstructed its South African history. We identified the biosynthetic gene clusters (BGCs) encoding specialized metabolites (SMs). We subsequently extracted mushrooms' metabolites and used mass spectrometry data to group SMs into unique molecular families (MFs). We tested metabolites for bioactivity against diverse microbes and animals. We identify Europe as the origin of South African A. muscaria. A highly conserved group of BGCs is found in nearly all European and African genomes, and only 13 of 273 MFs are unique to South Africa. Metabolites extracted from all mushrooms kill nematodes, while microbes and flies appear unaffected. The nearly global distribution of the fly agaric results from multiple introductions of a single European clade to the Southern Hemisphere. Despite its long history in South Africa, the fungus has not lost any of its BGCs, suggesting a conservation of function(s) across multiple continents.