Nutrient and prey-sensing signaling pathways converge on the sphingolipid methyltransferase SMT1 to regulate trap formation in a predatory fungus

Abstract

The nematode trapping fungus Arthrobotrys oligospora transitions from saprophytic growth to a predatory lifestyle by forming adhesive traps in response to nutrient limitation and nematode derived cues. How nutrient availability integrates with prey sensing to control trap formation remains unclear. The presence of glucose can suppress trap formation and we found that Cre1, a conserved transcription factor that regulates the carbon catabolite repression pathway in fungi is essential for trap formation. Comparative transcriptomics and functional studies identified SMT1, which encodes a sphingolipid C9 methyltransferase, as a Cre1-dependent target that is sufficient to restore trap formation defect in the cre1 mutant. Smt1 contributes to the formation of sterol-enriched membrane domain at the tip of a growing trap hyphae and thus affects trap morphogenesis. We further discovered that the expression of SMT1 depends on both Cre1 and another transcription factor Ste12 that acts downstream of the pheromone response MAPK pathway critical for prey-sensing. These findings reveal functional crosstalk between Cre1 and Ste12 where both transcription factors are required for the expression of SMT1 and demonstrate that a predatory fungus integrates nutrient and prey-derived signals to regulate predatory lifestyle switching.