Evolution of double-stranded DNA viruses of eukaryotes: from bacteriophages to transposons to giant viruses

Abstract

Diverse eukaryotes including animals and protists are hosts to a broad variety of viruses with double-stranded (ds) DNA genomes, from the largest known viruses, such as pandoraviruses and mimiviruses, to tiny polyomaviruses. Recent comparative genomic analyses have revealed many evolutionary connections between dsDNA viruses of eukaryotes, bacteriophages, transposable elements, and linear DNA plasmids. These findings provide an evolutionary scenario that derives several major groups of eukaryotic dsDNA viruses, including the proposed order "Megavirales," adenoviruses, and virophages from a group of large virus-like transposons known as Polintons (Mavericks). The Polintons have been recently shown to encode two capsid proteins, suggesting that these elements lead a dual lifestyle with both a transposon and a viral phase and should perhaps more appropriately be named polintoviruses. Here, we describe the recently identified evolutionary relationships between bacteriophages of the family Tectiviridae, polintoviruses, adenoviruses, virophages, large and giant DNA viruses of eukaryotes of the proposed order "Megavirales," and linear mitochondrial and cytoplasmic plasmids. We outline an evolutionary scenario under which the polintoviruses were the first group of eukaryotic dsDNA viruses that evolved from bacteriophages and became the ancestors of most large DNA viruses of eukaryotes and a variety of other selfish elements. Distinct lines of origin are detectable only for herpesviruses (from a different bacteriophage root) and polyoma/papillomaviruses (from single-stranded DNA viruses and ultimately from plasmids). Phylogenomic analysis of giant viruses provides compelling evidence of their independent origins from smaller members of the putative order "Megavirales," refuting the speculations on the evolution of these viruses from an extinct fourth domain of cellular life.

Keywords: Megavirales; Polintons; capsid proteins; translation; virus evolution.

Figure 1

Gene sharing between polintoviruses/Polintons and other groups of viruses, plasmids, and transposons. Homologous genes are color coded and the color key is provided at the bottom of the figure. Hatched regions in the pPolB genes indicate the position of the (predicted) terminal protein domains. Hatching is also used to indicate the gene encoding the distinct adenoviral genome packaging ATPase IVa2. P1_DY, polintovirus 1 of Drosophila yakuba; P3_TC, polintovirus 3 of Tribolium castaneum; P1_TV, polinton 1 of Trichomonas vaginalis. Modified from Ref. .

Figure 2

The polintovirus-centered scenario of evolution for eukaryotic dsDNA viruses and plasmids. INT, RVE family integrase; RNAP, DNA-dependent RNA polymerase; PRO, cysteine protease; PolB, family B DNA polymerase. Green color of the bidnavirus virion indicates that the capsid protein is unrelated to that of polintoviruses. See text for details. Modified from Ref. .

Figure 3

Origin of giant viruses. The schematic tree shows the phylogeny of the genes that are conserved across the “Megavirales,” with the three independently evolved groups of giant viruses highlighted in red. The numbers at internal branches indicated the estimated number of genes inferred to have been gained at the respective stage of evolution. The data are from Ref. .