A novel partitivirus orchestrates conidiation, stress response, pathogenicity, and secondary metabolism of the entomopathogenic fungus Metarhizium majus

Abstract

Mycoviruses are widely present in all major groups of fungi but those in entomopathogenic Metarhizium spp. remain understudied. In this investigation, a novel double-stranded (ds) RNA virus is isolated from Metarhizium majus and named Metarhizium majus partitivirus 1 (MmPV1). The complete genome sequence of MmPV1 comprises two monocistronic dsRNA segments (dsRNA 1 and dsRNA 2), which encode an RNA-dependent RNA polymerase (RdRp) and a capsid protein (CP), respectively. MmPV1 is classified as a new member of the genus Gammapartitivirus in the family Partitiviridae based on phylogenetic analysis. As compared to an MmPV1-free strain, two isogenic MmPV1-infected single-spore isolates were compromised in terms of conidiation, and tolerance to heat shock and UV-B irradiation, while these phenotypes were accompanied by transcriptional suppression of multiple genes involved in conidiation, heat shock response and DNA damage repair. MmPV1 attenuated fungal virulence since infection resulted in reduced conidiation, hydrophobicity, adhesion, and cuticular penetration. Additionally, secondary metabolites were significantly altered by MmPV1 infection, including reduced production of triterpenoids, and metarhizins A and B, and increased production of nitrogen and phosphorus compounds. However, expression of individual MmPV1 proteins in M. majus had no impact on the host phenotype, suggesting insubstantive links between defective phenotypes and a single viral protein. These findings indicate that MmPV1 infection decreases M. majus fitness to its environment and its insect-pathogenic lifestyle and environment through the orchestration of the host conidiation, stress tolerance, pathogenicity, and secondary metabolism. Fungi can carry mycoviruses, which are viruses that infect fungi. In this study, a new mycovirus called Metarhizium majus partitivirus 1 (MmPV1) was isolated from Metarhizium majus, a fungus that is well-known to kill insects. The virus has two segments of genetic material that code for a protein that helps replicate the virus (RNA-dependent RNA polymerase) and a protein that makes up the virus’s outer shell (capsid protein). Phylogenetic analysis showed that MmPV1 belongs to the Gammapartitivirus genus of the Partitiviridae family. This report revealed that MmPV1 infection decreased the fitness of the fungus in its environment by affecting its ability to produce spores, tolerate heat and UV-B radiation, and penetrate insect cuticles. This decreased pathogenicity was accompanied by changes in the production of secondary metabolites, including reduced production of certain compounds and increased production of others. Interestingly, expressing individual MmPV1 proteins did not have an impact on the host phenotype, indicating that the combination of viral proteins is responsible for the observed effects. Overall, this study highlights the complex interactions between mycoviruses and their fungal hosts and sheds light on the role of viruses in shaping fungal ecology and evoluti.