A mechanosensitive ion channel is required for nematode predation in nematode-trapping fungi.

UNLABELLED: Mechanosensitive ion channels of small conductance-like channels (MSL) are conserved in cell-walled organisms and enable cellular responses to mechanical stimuli. Nematode-trapping fungi (NTF) rely on nematode-derived mechanical cues to form specialized predatory structures, including adhesive network and mechanically actuated constricting ring (CR) that rapidly inflate upon nematode contact. However, the sensory mechanisms underlying these processes remain unclear. Here, using the adhesive network-forming Arthrobotrys oligospora and the CR-forming Drechslerella dactyloides as representative NTF, we identify a conserved fungal MSL channel containing a unique N-terminal intrinsically disordered region. msl expression is induced during predation, especially at the early stages for A. oligospora and late stages for D. dactyloides. Genetic depletion of MSL channels impaired sporulation, growth, and nematode-induced trap formation, specifically abolishing CR inflation in D. dactyloides. After nematode stimulation, the MSL channel translocated from the plasma membrane to the cytoplasm and activated Ca2+-dependent signaling pathways that regulate transcriptional regulation, signal transduction, cytoskeleton organization, and metabolic reprogramming. Collectively, these findings establish the MSL channel as an initial mechanosensor that transduces mechanical cues into Ca2+-dependent biochemical process to coordinate trap formation and trigger CR inflation.

IMPORTANCE: By elucidating how nematode-derived signals drive trap formation and activation, this work uncovers a new mechanotransduction pathway in nematode-trapping fungi (NTF) and expands the known roles of mechanosensitive ion channels of small conductance-like channels (MSL) beyond osmotic regulation, providing the first molecular insight into mechanosensitive channel-driven regulation of predatory behavior in filamentous fungi and offering new insights for developing biological control strategies against plant-parasitic nematodes.