How to catch a nematode if you were a mushroom

Carnivores have evolved diverse strategies to capture their prey efficiently. The oyster mushroom Pleurotus ostreatus is a carnivorous fungus that attacks and paralyze their nematode prey via their sensory cilia. Through genetic screens of P. ostreatus, we discovered that a spherical structure named toxocyst that developed at intervals along the fungal hyphae is required to paralyzed the nematodes. Intriguingly, we detected a natural ketone in the toxocysts, and treatment of Caenorhabditis elegans with that compound recapitulated the phenotypes of rapid paralysis, calcium influx and neuronal cell death. We found that this natural ketone disrupts nematode cell membrane integrity in multiple tissues, enabling uncontrolled exchange between the extracellular and intracellular environments. The ion imbalance generated a calcium wave in the mitochondria of hypodermis, and gave rise to cell death that propagated throughout the entire organism. Finally, we demonstrated that structurally related compounds could also exert prominent biotoxicity in C. elegans, with the carbon number of the ketone being crucial. Our work reveals that the toxocyst in oyster mushroom is a specialized structure that evolved to enable the accumulation of a natural ketone produced by the hyphae that is required for nematode predation and established a paradigm for studying organismal death in C. elegans.