Prey sensing and response in a nematode-trapping fungus is governed by the MAPK pheromone response pathway

Abstract

Detection of surrounding organisms in the environment plays a major role in the evolution of interspecies interactions, such as predator–prey relationships. Nematode-trapping fungi (NTF) are predators that develop specialized trap structures to capture, kill, and consume nematodes when food sources are limited. Despite the identification of various factors that induce trap morphogenesis, the mechanisms underlying the differentiation process have remained largely unclear. Here, we demonstrate that the highly conserved pheromone-response MAPK pathway is essential for sensing ascarosides, a conserved molecular signature of nemaotdes, and is required for the predatory lifestyle switch in the NTF Arthrobotrys oligospora. Gene deletion of STE7 (MAPKK) and FUS3 (MAPK) abolished nematode-induced trap morphogenesis and conidiation and impaired the growth of hyphae. The conserved transcription factor Ste12 acting downstream of the pheromone-response pathway also plays a vital role in the predation of A. oligospora. Transcriptional profiling of a ste12 mutant identified a small subset of genes with diverse functions that are Ste12 dependent and could trigger trap differentiation. Our work has revealed that A. oligospora perceives and interprets the ascarosides produced by nematodes via the conserved pheromone signaling pathway in fungi, providing molecular insights into the mechanisms of communication between a fungal predator and its nematode prey.

AoBck1 and AoMkk1 Are Necessary to Maintain Cell Wall Integrity, Vegetative Growth, Conidiation, Stress Resistance, and Pathogenicity in the Nematode-Trapping Fungus Arthrobotrys oligospora

“…The traps are an important feature for A. oligospora and other NT fungi to capture nematodes and are essential for their survival and virulence ( Nordbring-Hertz, 2004 ). Deletion of AoBck1 and AoMkk1 in A. oligospora resulted in the complete loss of the ability to form traps and the inability to capture nematodes, which is consistent with a previous report regarding AoSlt2 ( Zhen et al, 2018 ; Chen et al, 2021 ). Similar results were also found in other fungi, such as the virulence of the Δ Bck1 , Δ Mkk1 , and Δ Slt2 mutant strains being significantly reduced in B. bassiana ( Luo et al, 2012 ; Chen et al, 2014 ) and M. robertsii ( Chen et al, 2016 ).…”

“…Arthrobotrys oligospora is a typical NT fungal species that can reproduce asexually by producing abundant conidia (Zhang et al, 2019b). In this study, the ΔAoBck1 and ΔAoMkk1 mutants completely lost their ability for conidiation, which is similar to the ΔAoSlt2 mutant (Zhen et al, 2018;Chen et al, 2021). Similar defects in conidiation were also found in other fungi, such as the significantly reduced conidial yields of the Slt2-MAPK cascade mutants in M. robertsii.…”

“…Nematodes and fungi depend on and communicate through elaborate networks of signaling. The MAPK signaling cascades are key evolutionarily conserved signal transducers in all eukaryotes, and several MAPKs have been identified in A. oligospora , including Slt2 ( Zhen et al, 2018 ; Chen et al, 2021 ), Fus3 ( Chen et al, 2021 ), Hog1 ( Kuo et al, 2020 ), and Ime2 ( Xie et al, 2020 ). In filamentous ascomycetes, the Slt2-MAPK cascade pathway is an important signaling pathway, which consists of Bck1 , Mkk1/2 , and Slt2 in S. cerevisiae ( Levin, 2005 ).…”

“…In Magnaporthe oryzae , the Δ Mps1 mutant had severe defects in aerial hyphal growth ( Xu et al, 1998 ). In A. oligospora , deletion of AoSlt2 resulted in a serious defect in mycelial growth and aerial hyphae development in A. oligospora ( Zhen et al, 2018 ; Chen et al, 2021 ). Similar to the Δ AoSlt2 mutant, the Δ AoBck1 and Δ AoMkk1 mutants also showed a significant reduction in mycelial growth and aerial hyphae, where the colonies of the Δ AoBck1 and Δ AoMkk1 mutants became irregular and hyphal branches were increased compared to the WT strain.…”

“…Specifically, the deletion of Slt2 abolished conidiation and trap formation ( Zhen et al, 2018 ). Similarly, a Slt2 deletion mutant of A. oligospora displayed severe defects in vegetative growth, conidiation, and trap morphogenesis ( Chen et al, 2021 ). However, the functions of Bck1 and Mkk1 upstream of Slt2 are poorly understood in A. oligospora and NT fungi specifically.…”