Plasmid-like dynamics of persistent RNA viruses in the host fungal population

Unlike the well-known acute or chronic animal and plant RNA viruses, most fungal RNA viruses (RNA mycoviruses) have a persistent life cycle. They lack an extracellular infection route and coexist with their hosts for a lifetime. RNA mycoviruses affect various biological properties of host fungi and are widespread across all major fungal groups. The frequency of fungal isolates harboring RNA mycoviruses ranges from a few percent to several tens of percent, indicating their high persistence within ecosystems. However, the dynamics of RNA mycoviruses and the maintenance mechanisms within host populations remain largely unknown. Here, we developed an experimental laboratory model system to examine the dynamics of mycoviruses within clonal host populations and to clarify the mechanisms. In our experimental system, we used two mycoviruses infecting Aspergillus fumigatus. Using this system, we discovered that viral prevalence changed according to environmental conditions (temperature or fungicide exposure). The driving forces behind these prevalence changes were viral horizontal transmission between isogenic strains through hyphal fusion, viral loss, and viral impact on host growth. Our findings indicated that the dynamics of mycoviruses are similar to those of plasmids in bacterial populations. This analogy implied an uncovered role of mycoviruses as a switching factor for fungal adaptation to changing environments.IMPORTANCEWhile RNA viruses are generally known for their ability to infect cells from the extracellular environment, a substantial diversity of RNA viruses, particularly those that persistently infect fungi, lack such infectivity. The ecological success and evolutionary maintenance of these persistent RNA viruses remain poorly understood. In this study, we experimentally demonstrate how a non-infectious RNA virus is transmitted and stably maintained within specific fungal host lineages. The revealed mechanism resembles the inheritance strategies of plasmids, highlighting a fundamentally different viral lifestyle that does not rely on extracellular horizontal transmission. These findings advance our understanding of virus-host interactions beyond the classical infection model and shed light on the evolutionary flexibility of RNA viruses.