Abstract
BackgroundRecent advances of genomics and metagenomics reveal remarkable diversity of viruses and other selfish genetic elements. In particular, giant viruses have been shown to possess their own mobilomes that include virophages, small viruses that parasitize on giant viruses of the Mimiviridae family, and transpovirons, distinct linear plasmids. One of the virophages known as the Mavirus, a parasite of the giant Cafeteria roenbergensis virus, shares several genes with large eukaryotic self-replicating transposon of the Polinton (Maverick) family, and it has been proposed that the polintons evolved from a Mavirus-like ancestor.ResultsWe performed a comprehensive phylogenomic analysis of the available genomes of virophages and traced the evolutionary connections between the virophages and other selfish genetic elements. The comparison of the gene composition and genome organization of the virophages reveals 6 conserved, core genes that are organized in partially conserved arrays. Phylogenetic analysis of those core virophage genes, for which a sufficient diversity of homologs outside the virophages was detected, including the maturation protease and the packaging ATPase, supports the monophyly of the virophages. The results of this analysis appear incompatible with the origin of polintons from a Mavirus-like agent but rather suggest that Mavirus evolved through recombination between a polinton and an unknownvirus. Altogether, virophages, polintons, a distinct Tetrahymena transposable element Tlr1, transpovirons, adenoviruses, and some bacteriophages form a network of evolutionary relationships that is held together by overlapping sets of shared genes and appears to represent a distinct module in the vast total network of viruses and mobile elements.ConclusionsThe results of the phylogenomic analysis of the virophages and related genetic elements are compatible with the concept of network-like evolution of the virus world and emphasize multiple evolutionary connections between bona fide viruses and other classes of capsid-less mobile elements.
Highlights
Recent advances of genomics and metagenomics reveal remarkable diversity of viruses and other selfish genetic elements
The minor capsid protein initially has not been detected in the Mavirus but direct sequence comparisons supported by gene synteny suggest that MV17 is a highly diverged homolog of the minor capsid protein of the two other virophages
It has been recently shown that the virophages of the Mimiviridae have a broad host range and can serve as vectors for gene exchanges among the three different groups of mimiviruses [31,32]
Summary
Recent advances of genomics and metagenomics reveal remarkable diversity of viruses and other selfish genetic elements. The third virophage genome was isolated from the Antarctic Organic Lake ( OLV, Organic Lake Virophage) where it apparently controls the reproduction of its virus host that originally has been classified as a distinct phycodnavirus [12] but according to a more detailed recent phylogenetic study, is more closely related to the family Mimiviridae [13]. 5 additional genomes of putative virophages have been assembled from metagenomic sequences [14] Four complete genomes, those of Yellowstone Lake Virophages (YLSV1-4), appeared to be related to OLV, whereas the fifth, nearly complete one, the Ace Lake Mavirus (ALM), appeared to be a relative of the Mavirus [14]. The rest of the genes show diverse phylogenetic affinities suggestive of chimeric origins of the virophages [8,11,12]
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