Entomopathogenic fungi routinely kill their hosts before releasing infectious spores, but a few species keep insects alive while sporulating, which enhances dispersal. Transcriptomics- and metabolomics-based studies of entomopathogens with post-mortem dissemination from their parasitized hosts have unraveled infection processes and host responses. However, the mechanisms underlying active spore transmission by Entomophthoralean fungi in living insects remain elusive. Here we report the discovery, through metabolomics, of the plant-associated amphetamine, cathinone, in four Massospora cicadina-infected periodical cicada populations, and the mushroom-associated tryptamine, psilocybin, in annual cicadas infected with Massospora platypediae or Massospora levispora, which likely represent a single fungal species. The absence of some fungal enzymes necessary for cathinone and psilocybin biosynthesis along with the inability to detect intermediate metabolites or gene orthologs are consistent with possibly novel biosynthesis pathways in Massospora. The neurogenic activities of these compounds suggest the extended phenotype of Massospora that modifies cicada behavior to maximize dissemination is chemically-induced.

病原性真菌通常在释放感染性孢子之前先杀死宿主，但少数物种在形成孢子时可使昆虫存活，从而增强了传播能力。基于转录组学和代谢组学的昆虫病原体从寄生虫宿主中进行死后传播的研究揭示了感染过程和宿主反应。但是，昆虫壳虫真菌在活体昆虫中主动传播孢子的机制仍然难以捉摸。在这里，我们报告的发现，通过代谢组学，植物相关的安非他明，卡西的，四个Massospora cicadina感染的周期蝉群，以及蘑菇相关的色胺，裸盖菇碱，在感染了年度蝉Massospora platypediae或Massospora levispora，可能代表一种真菌。不存在与该不能检测中间代谢物或直系同源物的基因沿必要卡西酮和迷幻药生物合成一些真菌酶是与可能新颖生物合成途径一致Massospora。这些化合物的神经源性活性表明马尾孢的扩展表型是化学诱导的，该表型改变蝉行为以最大程度地传播。