Pleiotropic roles of Ras GTPases in the nematode-trapping fungus Arthrobotrys oligospora identified through multi-omics analyses

Le Yang,Xuemei Li,Meihua Xie,Na Bai,Jiangliu Yang,Kexin Jiang,Ke-Qin Zhang,Jinkui Yang

doi:10.1016/j.isci.2021.102820

Abstract

SummaryThe nematode-trapping fungi are ideal agents for controlling pathogenic nematodes. Arthrobotrys oligospora is a representative species of the same, producing traps for nematode predation. Here, three orthologous Ras GTPases (Ras2, Ras3, and Rheb) were characterized in A. oligospora. Our results indicate that they play pleiotropic roles in regulating the mycelial growth, conidiation, stress resistance, and pathogenicity of A. oligospora. Furthermore, deletion of Aoras2 and Aorheb significantly affected the mitochondrial activity, reactive oxygen species levels, lipid storage, and autophagy. Transcriptome analyses of ΔAoras2 mutant revealed that many repressed genes were associated with signal transduction, energy production, and carbohydrate transport and metabolism. Moreover, metabolic profile analyses showed that AoRas2 and AoRheb affect the biosynthesis of secondary metabolites in A. oligospora. Collectively, these findings provide an in-depth insight into the essential roles of Ras GTPases in vegetative growth, development, and pathogenicity and highlight their importance in the lifestyle switch of the nematode-trapping fungi.

Highlights

Nematophagous fungi are an important group of soil microorganisms that inhibit the population of the plant and animal parasitic nematodes (Su et al, 2017)
Sequences and phylogenetic analyses of Ras GTPases (AoRas2, AoRas3, and AoRheb) Three Ras GTPases, namely, AoRas2, AoRas3, and AoRheb, were retrieved from A. oligospora using the homologous sequences of Neurospora crassa and Saccharomyces cerevisiae as queries
The phylogenetic tree of small GTPases from diverse filamentous fungi was constructed based on their amino acid sequences, and the orthologs of Ras2, Ras3, and Ras homolog enriched in brain (Rheb) were separated into three clades (Figure S1)

Summary

Introduction

Nematophagous fungi are an important group of soil microorganisms that inhibit the population of the plant and animal parasitic nematodes (Su et al, 2017). The trap formation is an important indicator for NT fungi to switch from a saprophytic to a predacious lifestyle (Yang et al, 2011; Ji et al, 2020). Dactylellina haptotyla) (Meerupati et al, 2013), Drechslerella stenobrocha (Liu et al, 2014), and Duddingtonia flagrans (Youssar et al, 2019). These studies provided a broad basis for investigating the mechanisms regulating hyphal growth and development, cell differentiation, and pathogenicity in NT fungi

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Discussion

Conclusion