Infection cycle and phylogeny of the Polinton-like virus Phaeocystis globosa virus virophage-14T

Abstract

Virophages are small dsDNA viruses dependent on a nucleocytoplasmic large-DNA virus infection of a cellular host for replication. Putative virophages infecting algal hosts are classified together with polinton-like viruses, transposable elements widely found in algal genomes, yet the lack of isolated strains raises questions about their existence as independent entities. In this work we isolated and characterized a virophage (PgVV-14T) co-infecting Phaeocystis globosa with the Phaeocystis globosa virus-14T (PgV-14T). PgVV-14T decreases the fitness of its PgV-14T viral host, yet it does not salvage the cellular host population. We found viral-like elements resembling PgVV-14T in Phaeocystis genomes, suggesting that these virophages are capable of integrating to the cellular host genome, bridging the gap between Polinton-like viruses and virophages. This system, with a giant virus, a virophage and endogenous viral elements preying on an algal host, presents an opportunity to gain a better understanding on the evolution of eukaryotes and their viruses.

Updated Virophage Taxonomy and Distinction from Polinton-like Viruses

“…A similar framework could likely be used for PLVs, some of them currently classified in the Polintoviricetes, which would further clarify taxonomic classification in this area of the virosphere. There is much that remains to be discovered and characterized in terms of virophage and PLV biology, including host range, interaction with giant viruses and eukaryotic hosts, or potential new defense/counterdefense systems [25,36]. Ultimately, a comprehensive genome catalog of virophages, along with a clear and updated taxonomic scheme, represents a framework that will facilitate future studies and more in-depth characterization of these fascinating viruses.…”

“…Both Sputnik and mavirus hijack the molecular machinery of their associated giant viruses and, in so doing, likely reduce the burden imposed on the protist host community by these eukaryotic viruses. A recent PLV-like element showed a similar association with both a giant virus and a eukaryotic virus and a reduction in the fitness of the giant virus, suggesting this lifestyle and infection cycle may be a common feature of virophages and PLVs [25]. However, most virophages are only known from metagenome assemblies; thus we lack information about their potential giant virus and eukaryotic hosts.…”

“…Further comparative genomic studies, including a large compendium of genomes assembled from metagenomes, indicated that these virophage (-like) sequences were diverse and part of a larger evolutionary network including other eukaryotic viruses & mobile genetic elements, most notably polinton-like viruses (PLVs) [19][20][21][22][23]. Like virophages, PLVs seem to be evolutionary related to mobile genetic elements of the Maverick/Polinton class, can co-infect eukaryotic host cells alongside a giant virus, and seemingly encode a comparable encapsidation machinery although with no detectable sequence similarity to the one of virophages [24][25][26]. Meanwhile, the integration of mavirus-like virophages into their eukaryotic host genomes and subsequent reactivation was further explored and revealed a high degree of mobility, with a potential role as a population-based defense system against their cognate giant viruses [27,28].…”