A mycovirus enhances fitness of an insect pathogenic fungus and potentially modulates virulence through interactions between viral and host proteins

Beauveria bassiana is an entomopathogenic ascomycete widely utilized in biological pest control. However, its effectiveness is often limited by low conidiation rates, sensitivity to environmental stresses, and delayed insecticidal activity. In this study, we identify and characterize a mycovirus, Beauveria bassiana polymycovirus 4-2 (BbPmV4-2), which markedly enhances the fitness and may modulate virulence of its fungal host. BbPmV4-2 comprises eight double-stranded RNA segments, among which three are unique and have not been previously detected in related mycoviruses. Infection with BbPmV4-2 nearly doubles conidial yields and upregulates key conidiation-related genes, facilitating enhanced dispersal of both the host fungus and the mycovirus itself. Additionally, BbPmV4-2 infected strains exhibit increased tolerance to ultraviolet (UV) irradiation and elevated temperatures, and may also exhibit increased virulence against the greater wax moth, Galleria mellonella. The potentially increased virulence is attributed to increased conidial hydrophobicity, adhesion, and cuticle penetration capabilities. Functional analysis reveals that the viral open reading frame ORF5 plays a critical role in conferring hypervirulence and stress tolerance by interacting with host proteins BbGAP1, a GPI-anchored membrane protein, and BbSDU1, a deubiquitinating enzyme. These interactions elucidate a molecular mechanism by which a mycovirus that enhances environmental adaptability and potentially influences host pathogenicity. Our findings provide significant insights into mycovirus-host interactions and suggest potential strategies for optimizing biological pest control applications.