Abstract
BackgroundPolintons are large mobile genetic elements found in the genomes of eukaryotic organisms that are considered the ancient ancestors of most eukaryotic dsDNA viruses. Originally considered as transposons, they have been found to encode virus capsid genes, suggesting they may actually be integrated viruses; however, an extracellular form has yet to be detected. Recently, circa 25 Polinton-like viruses have been discovered in environmental metagenomes and algal genomes, which shared distantly related genes to both Polintons and virophages (Lavidaviridae). These entities could be the first members of a major class of ancient eukaryotic viruses; however, owing to the lack of available genomes for analysis, information on their global diversity, evolutionary relationships, eukaryotic hosts, and status as free virus particles is limited.ResultsHere, we analysed the metaviromes of an alpine lake to show that Polinton-like virus genome sequences are abundant in the water column. We identify major capsid protein genes belonging to 82 new Polinton-like viruses and use these to interrogate publicly available metagenomic datasets, identifying 543 genomes and a further 16 integrated into eukaryotic genomes. Using an analysis of shared gene content and major capsid protein phylogeny, we define large groups of Polinton-like viruses and link them to diverse eukaryotic hosts, including a new group of viruses, which possess all the core genes of virophages and infect oomycetes and Chrysophyceae.ConclusionsOur study increased the number of known Polinton-like viruses by 25-fold, identifying five major new groups of eukaryotic viruses, which until now have been hidden in metagenomic datasets. The large enrichment (> 100-fold) of Polinton-like virus sequences in the virus-sized fraction of this alpine lake and the fact that their viral major capsid proteins are found in eukaryotic host transcriptomes support the hypothesis that Polintons in unicellular eukaryotes are viruses. In summary, our data reveals a diverse assemblage of globally distributed viruses, associated with a wide range of unicellular eukaryotic hosts. We anticipate that the methods we have developed for Polinton-like virus detection and the database of over 20,000 genes we present will allow for continued discovery and analysis of these new viral groups.4nQk6QRKxQCQHashEWMwNeVideo abstract
Highlights
Polintons are the largest transposable elements known in eukaryotic genomes
To determine the relationship between the Polinton-like virus (PLV) found in Gossenköllesee and known entities, we constructed a maximum likelihood tree of major capsid protein (MCP) genes, including those identified in known Polintons (n = 56) and PLV (n = 25) [8] along with more
Maximum likelihood phylogenetic analysis of PLV MCP genes showed that most of the Gossenköllesee MCPs formed novel groups, several of which had little homology to previously described Polinton or PLV capsid genes (Fig. 1). These included a group that we refer to as the Gossevirus group, composed of seven Gossenköllesee PLVs and homologous MCPs from Polintons/PLVs detected in oomycete genomes; the GKS2 group, which was composed of 16 Gossenköllesee MCP genes with no known integrated representatives; and the VC20 group, a novel group of five viruses from Gossenköllesee, which possessed MCP genes detected in four different species of amoeba
Summary
Polintons ( known as Mavericks) are the largest transposable elements known in eukaryotic genomes. 25 Polinton-like viruses (PLVs) in sequencing datasets and environmental metagenomes [8,9,10] has further revealed a broad assemblage of related viruses, several of which were found integrated into algal genomes or associated with (attached to or inside) NCLDV particles [9, 10]. Circa 25 Polinton-like viruses have been discovered in environmental metagenomes and algal genomes, which shared distantly related genes to both Polintons and virophages (Lavidaviridae). These entities could be the first members of a major class of ancient eukaryotic viruses; owing to the lack of available genomes for analysis, information on their global diversity, evolutionary relationships, eukaryotic hosts, and status as free virus particles is limited
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