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

• Published in: PLoS pathogens Vol. 19; no. 5; p. e1011397
• Main Authors: Wang, Ping, Yang, Guogen, Shi, Najie, Zhao, Cheng, Hu, Fenglin, Coutts, Robert H A, Kotta-Loizou, Ioly, Huang, Bo
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 01.05.2023; Public Library of Science (PLoS)
• Subjects: Analysis; Biology and Life Sciences; Capsid protein; Computer and Information Sciences; Deoxyribonucleic acid; DNA; DNA damage; DNA repair; DNA-directed RNA polymerase; Double-stranded RNA; Entomopathogenic fungi; Fungi; Fungi, Pathogenic; Genetic aspects; Genetic transcription; Genomes; Genomics; Health aspects; Heat shock; Hydrophobicity; Identification and classification; Infections; Insects; Irradiation; Kinases; Medicine and Health Sciences; Metabolism; Metabolites; Metarhizium; Nucleotide sequence; Pathogenicity; Pathogens; Phenotypes; Phosphorus; Phosphorus compounds; Phylogenetics; Phylogeny; Physical sciences; Physiological aspects; Plant metabolites; Proteins; Ribonucleic acid; RNA; RNA viruses; RNA-directed RNA polymerase; Secondary metabolites; Triterpenoids; Ultraviolet radiation; Viral infections; Viral proteins; Virulence; Virulence (Microbiology); Viruses; China
• ISSN: 1553-7374; 1553-7366; 1553-7374
• DOI: 10.1371/journal.ppat.1011397

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.