Evidence for gene transfer between mycoviruses and their host: Curvulaviridae as a case study

Gene transfer between distinct evolutionary lineages has been recognized as a frequent event occurring between viruses and their hosts. This phenomenon has been studied to some extent in animal and plant viruses, not so much in the case of mycoviruses, for which the evolutionary origins of their proteins remain poorly understood. In this study, we have tested the hypothesis of a mosaic origin for mycoviruses genomes, with the RNA-dependent RNA-polymerase (RdRp) being of viral origin and the coat protein (CP) resulting from one or more transfer events from the host genome. Firstly, phylogenetic trees were constructed for the RdRps and the CPs from a selection of viruses to address for possible incongruent evolutionary histories. Moreover, a PSI-BLAST search using the CP sequences from the different mycovirus groups retrieved hypothetical proteins (HP) with many orthologues in fungal genomes showing significant sequence homology with the CP from the members within the Curvulaviridae family. The structures of these HPs, predicted in silico using AlphaFold, tend to show high similarity with viral CPs suggesting the occurrence of gene transfer between viruses and fungi, although no clear function has been yet attributed to these genes in the host. Phylogenetic analyses suggest that this gene transfer could have occurred in multiple independent events. Additional selection analysis supports the notion that the most parsimonious explanation is the transfer of the HP from the host to an ancestral viral genome followed by fast evolution to accommodate the newly acquired protein to function as a CP.