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Abstract:
Fungal predatory behavior on nematodes has evolved independently in several lineages. Pleurotus ostreatus, the basidiomycete oyster mush- room, is a nematophagous fungus that preys on nematodes when limited nutrients are available. Our previous study showed that when Caenorhabditis elegans contacted the mycelium of P. ostreatus, the toxins could enter through cilia, causing head muscle hyper-contrac- tion and calcium influx in pharyngeal and body wall muscles, finally resulting in the necrosis process. However, the molecular identity of the nematode-paralyzing toxins produced by P. ostreatus remained unclear. To study this question, we conducted random mutagenesis forward genetic screens in P. ostreatus to isolate mutants that were unable to paralyze C. elegans. We generated ~12,000 UV and EMS-mu- tagenized clones and identified 22 P. ostreatus loss-of-toxicity (lot) mutants that lacked nematicidal activity toward C. elegans. Viewing the morphology of the lot mutants revealed that they all lack the spher- ical structures, toxocysts, on the hyphae. Toxocysts are fragile and lose nematicidal activity easily. Therefore, we hypothesized that toxins inside toxocysts are volatile. We conducted GC-MS and identified 3-oc- tanone as a promising candidate for the nematicidal compound. 3-oc- tanone treatment recapitulated the phenotypes of rapid calcium influx and neuronal cell death by targeting the cell membrane and disrupting membrane integrity in vivo and in vitro to trigger rapid cell death in C. elegans. Our work reveals that P. ostreatus develops a specific struc- ture to concentrate a volatile ketone to disrupt the membrane integrity of C. elegans, resulting in rapid organismal cell death.
