Cryptostroma corticale, a plant pathogen associated with a human immune respiratory syndrome displaying mixed viral infections of mycoviruses

Mycoviruses, viruses infecting fungi, have been identified in several ascomycetes as single infections or mixed infections. These interactions with plant pathogenic fungi have been associated with hyper– or hypovirulence. This report focuses on single and mixed mycovirus infection of the plant pathogenic fungus Cryptostroma corticale, the causal agent of sooty bark disease (SBD) affecting maple trees in Europe and North America. In humans, exposure of C. corticale spores causes maple bark disease (MBD), causing hypersensitive pneumonitis and allergic asthma with viral-like symptoms. In this study, we identified four species of single-stranded, positive-sense (ss+) RNA mycoviruses that are phylogenetically diverse, including one Mitovirus: Cryptostroma corticale mitovirus 1 (CcMV1) and three Narnavirus species: Cryptostroma corticale narnavirus 1, 2, and 3 (CcNV1, 2, and 3). Notably, CcMV1 shows predicted secondary structures in both 5′ and 3′ UTRs, while CcNV1 and CcNV3 exhibited strong secondary structures at the 3′ UTR. These four mycoviruses were prevalent in 45% (n = 35) of the isolates tested, and growth assays of single infection and the most complex mixed infection showed faster radial expansion compared to a virus-free isolate. These findings reveal single and mixed mycoviruses infections in C. corticale differentially affecting fungal growth, with potential implications for SBD pathogenesis and human MBD risk.