Psychoactive plant- and mushroom-associated alkaloids from two behavior modifying cicada pathogens

Area of Science:

• Mycology and Insect Pathology
• Chemical Ecology and Neurobiology

Background:

• Entomopathogenic fungi typically kill hosts before spore release, but some species maintain hosts alive for enhanced dispersal.
• Mechanisms for active spore transmission by Entomophthoralean fungi in living insects are poorly understood.
• Previous studies focused on post-mortem dissemination, leaving active transmission pathways unexplored.

Purpose of the Study:

• To investigate the biochemical mechanisms behind active spore transmission in Massospora fungi infecting cicadas.
• To identify the compounds responsible for modifying host behavior to facilitate fungal dissemination.

Main Methods:

• Metabolomics analysis was employed to identify chemical compounds in infected cicada populations.
• Comparative analysis of fungal enzymes and gene orthologs was performed to infer biosynthesis pathways.

Main Results:

• Cathinone, a plant-associated amphetamine, was discovered in periodical cicadas infected with Massospora cicadina.
• Psilocybin, a mushroom-associated tryptamine, was found in annual cicadas infected with Massospora platypediae or Massospora levispora.
• Absence of key biosynthetic enzymes and intermediates suggests novel pathways for cathinone and psilocybin production in Massospora.

Conclusions:

• Massospora fungi produce psychoactive compounds (cathinone, psilocybin) that likely induce neurogenic effects in cicada hosts.
• These neurogenic effects constitute an 'extended phenotype,' chemically manipulating cicada behavior to maximize fungal spore dispersal.
• The findings reveal a novel strategy of chemically-induced behavioral modification for fungal propagation in insects.