Ancient Host-Virus Gene Transfer Hints at a Diverse Pre-LECA Virosphere

The details surrounding the early evolution of eukaryotes and their viruses are largely unknown. Several key enzymes involved in DNA synthesis and transcription are shared between eukaryotes and large DNA viruses in the phylum Nucleocytoviricota, but the evolutionary relationships between these genes remain unclear. In particular, previous studies of eukaryotic DNA and RNA polymerases often show deep-branching clades of eukaryotes and viruses indicative of ancient gene exchange. Here, we performed updated phylogenetic analysis of eukaryotic and viral family B DNA polymerases, multimeric RNA polymerases, and mRNA-capping enzymes to explore their evolutionary relationships. Our results show that viral enzymes form clades that are typically adjacent to eukaryotes, suggesting that they originate prior to the emergence of the Last Eukaryotic Common Ancestor (LECA). The machinery for viral DNA replication, transcription, and mRNA capping are all key processes needed for the maintenance of virus factories, which are complex structures formed by many nucleocytoviruses during infection, indicating that viruses capable of making these structures are ancient. These findings hint at a diverse and complex pre-LECA virosphere and indicate that large DNA viruses may encode proteins that are relics of extinct proto-eukaryotic lineages.