Title: A Novel Nitrogen and Carbon Metabolism Regulatory Cascade Is Implicated in Entomopathogenicity of the Fungus Metarhizium robertsii

Yamin Meng, Xing Zhang, Dan Tang, Xiaoxuan Chen, Dan Zhang, Jun Chen, and Weiguo Fang

https://doi.org/10.1128/mSystems.00499-21

Abstract

The entomopathogenic fungus Metarhizium robertsii can switch among parasitic, saprophytic, and symbiotic lifestyles in response to changing nutritional conditions, which is attributed to its extremely versatile metabolism. Here, we found that the Fus3–mitogen-activated protein kinase (MAPK) and the transcription factor regulator of nutrient selection 1 (RNS1) constitute a novel fungal cascade that regulates the degradation of insect cuticular lipids, proteins, and chitin to obtain nutrients for hyphal growth and enter the insect hemocoel for subsequent colonization. On the insect cuticle, Fus3-MAPK physically contacts and phosphorylates RNS1, which facilitates the entry of RNS1 into nuclei. The phosphorylated RNS1 binds to the DNA motif BM2 (ACCAGAC) in its own promoter to self-induce expression, which then activates the expression of genes for degrading cuticular proteins, chitin, and lipids. We further found that the Fus3-MAPK/RNS1 cascade also activates genes for utilizing complex and less-favored nitrogen and carbon sources (casein, colloid chitin, and hydrocarbons) that were not derived from insects, which is repressed by favored organic carbon and nitrogen nutrients, including glucose and glutamine. In conclusion, we discovered a novel regulatory cascade that controls fungal nitrogen and carbon metabolism and is implicated in the entomopathogenicity of M. robertsii.

Link: https://journals.asm.org/doi/10.1128/mSystems.00499-21