The Diversity of Mycoviruses in Early-Diverging Fungi,and Their Evolutionary Implications

Abstract

Even microbes can, themselves, be host to microorganisms. Bacterial-fungal interactions have increasingly received attention, empowered by the identification of widespread endobiotic bacteria in some early-diverging fungal lineages. But, rarely are fungi thought of as hosts to viruses. In this dissertation research, I explore methods for fungal virus (mycovirus) discovery, identify many new viruses, and use these newly obtained viral sequences to address outstanding questions in the field. Specifically, I ask “Which fungi are infected with viruses?”, “What kinds of viruses?”, and “Where did fungal viruses come from?”. I speculate on the implications of viral infection to fungal evolution, fungal ecology, and ecosystems.

One major limitation in mycovirus research, and the focal point of this dissertation, is the lack of diverse fungal sampling. In Chapter 2, through a survey of both cultures and transcriptomes, I find higher viral prevalences in the basal lineages than have previously been reported. I identify at least 85 previously unknown viruses that span RNA virus taxonomy, and demonstrate that mycoviruses are present in research cultures around the world, the implications of which are far-reaching.

These newly identified mycovirus sequences from basal fungi enable a previously impossible examination of the evolutionary relationships between mycoviruses and fungi. In Chapter 3, I test the hypothesis of cospeciation of mycoviruses and their fungal hosts through statistical tests of phylogenetic congruence. I find evidence of cospeciation in all four viral families tested, despite this mode of speciation being quite rare. When evidence of cospeciation does exist, it is most often between hosts and their vertically-transmitted mutualists. There is evidence that host-switching is the dominant mode of speciation among RNA viruses, and so my findings suggest that mycovirus life history is unique, and of ecological importance.

Known mycoviruses are almost exclusively composed of RNA genomes. In Chapter 4, the number of known mycoviruses with DNA genomes is more than quadrupled with the identification, for the first time in Fungi, of nucleocytoplasmic large DNA viruses (NCLDV). This exciting finding has unknown but important implications to global nutrient cycling as NCLDVs notoriously reprogram their host’s metabolism. Importantly, these large viruses likely only occur in some of the most basal, zoosporic, lineages.

As they did for bacterial-fungal interactions, the early-diverging fungi have transformed what we think we know about fungal viruses, demonstrating, once again, that representation shapes knowledge. This work has addressed some of the outstanding questions in the field, and, in the process, raised many more.