Evolution of a major virion protein of the giant pandoraviruses from an inactivated bacterial glycoside hydrolase

Abstract The diverse viruses in the phylum Nucleocytoviricota (also known as NLCDVs, Nucleo-cytoplasmic Large DNA Viruses) typically possess large icosahedral virions. However, in several families of Nucleocytoviricota, the icosahedral capsid was replaced by irregular particle shapes, most notably, the amphora-like virions of pandoraviruses and pithoviruses, the largest known virus particles in the entire virosphere. Pandoraviruses appear to be the most highly derived viruses in this phylum because their evolution involved not only the change in the virion shape, but also, the actual loss of the gene encoding double-jelly roll major capsid protein (DJR MCP), the main building block of icosahedral capsids in this virus assemblage. Instead, pandoravirus virions are built of unrelated abundant proteins. Here we show that the second most abundant virion protein of pandoraviruses, major virion protein 2 (MVP2), evolved from an inactivated derivative of a bacterial glycoside hydrolase of the GH16 family. The ancestral form of MVP2 was apparently acquired early in the evolution of the Nucleocytoviricota, to become a minor virion protein. After a duplication in the common ancestor of pandoraviruses and molliviruses, one of the paralogs displaces DJR MCP in pandoraviruses, conceivably, opening the way for a major increase in the size of the virion and the genome. Exaptation of a carbohydrate-binding protein for the function of the MVP is a general trend in virus evolution and might underlie the transformation of the virion shape in other groups of the Nucleocytoviricota as well.