Selective manipulation of the host RNA-polymerase transcription fidelity increases phenotypic mutations in an insect Parvovirus

In the dynamic dance of evolution, organisms are often faced with fluctuating environments to which adaptation through selection of traditional heritable genetic mutations can be limiting. In this study, we unveil a refined mechanism of non-heritable variability in a virus with a compact DNA genome. We discovered that the genome of the Junona cnia densovirus (JcDV) experiences a 10-fold lower transcription fidelity than the rest of the hosts transcriptome, despite the shared transcription machinery. We found that the virus capsid proteins interact with the hosts RNA Polymerase II, and further show that truncating these proteins through early stop codons largely restore the transcriptional fidelity of viral genes. These observations suggest a potential mechanism for the selective manipulation of transcription accuracy. We also pinpoint specific sequence contexts that may provide other knobs to finely control the local transcription fidelity. We estimate that this lower transcriptional fidelity results in more than 7% of the viral proteome bearing at least one non-synonymous mutation. The production of non-heritable functional diversity by hijacking the transcriptional machinery might be a refined strategy to enhance short term adaptation within the complex and ever-changing host-parasite interface, and might be shared by other genetic parasites. Our findings shed light on a virus-specific transcription fidelity control mechanism, expanding our understanding of adaptive strategies in biological entities.