A novel fungal sensor (Ngs1) of N-acetylglucosamine (GlcNAc) mediates the fungal response to GlcNAc in the interaction between entomopathogenic Beauveria bassiana and insect host.

As N-acetylglucosamine (GlcNAc) ubiquitously exists in both insect cuticle and fungal cell walls, the GlcNAc sensor (Ngs1) potentially plays important roles in the interactions between entomopathogenic fungi and their insect hosts. However, the roles of the Ngs1 derived from the entomopathogens in response to the host's cuticle remain completely unexplored. In this study, a putative Ngs1 homolog was identified in the entomopathogenic fungus Beauveria bassiana. Deletion of Ngs1 significantly reduced virulence towards Galleria mellonella larvae either through cuticle infection (by 23%) or by bypassing the cuticle (by 44%). To investigate the role of Ngs1 in fungal virulence, an analysis of the transcriptome induced by Locusta migratoria exoskeleton was conducted, highlighting the regulatory mechanism of Ngs1 in carbohydrate metabolic process, particularly chitin metabolism and GlcNAc metabolism. Consistent with the transcriptomic data, Ngs1-deletion mutants showed reduced activities of both secreted chitinase (17% reduction) and Pr1 protease (35% reduction). Loss of Ngs1 down-regulated the transcript levels of GlcNAc-catabolism genes, resulting in a 17% decrease in fungal growth on GlcNAc-supported media. Furthermore, Ngs1 deficiency attenuated the fungal response to GlcNAc, leading to the alteration of fungal resistance to diverse stress cues. All of these changes contribute to the reduction in virulence in Ngs1-deficient B. bassiana. These findings support that Ngs1 plays a critical role in responding to insect-derived GlcNAc, affecting the production of cuticle-degrading enzymes to penetrate insect epidermis, GlcNAc-induced changes of stress resistance, and contribute to the fungal virulence against insects.