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Review
. 2015 Feb;13(2):105-15.
doi: 10.1038/nrmicro3389. Epub 2014 Dec 22.

Polintons: a hotbed of eukaryotic virus, transposon and plasmid evolution

Mart Krupovic  1 , Eugene V Koonin  2
Affiliations
Review

Polintons: a hotbed of eukaryotic virus, transposon and plasmid evolution

Mart Krupovic et al. Nat Rev Microbiol. 2015 Feb.

Abstract

Polintons (also known as Mavericks) are large DNA transposons that are widespread in the genomes of eukaryotes. We have recently shown that Polintons encode virus capsid proteins, which suggests that these transposons might form virions, at least under some conditions. In this Opinion article, we delineate the evolutionary relationships among bacterial tectiviruses, Polintons, adenoviruses, virophages, large and giant DNA viruses of eukaryotes of the proposed order 'Megavirales', and linear mitochondrial and cytoplasmic plasmids. We hypothesize that Polintons were the first group of eukaryotic double-stranded DNA viruses to evolve from bacteriophages and that they gave rise to most large DNA viruses of eukaryotes and various other selfish genetic elements.

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Conflict of interest statement

Competing interests statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1. Evolutionary relationships between Polintons and other mobile genetic elements
a | Evolutionary network showing shared gene content between Polintons and other mobile genetic elements in archaea, bacteria and eukaryotes. Edges correspond to homologous genes. The colour key is provided in part b. Only those elements that are directly linked to Polintons are shown. b | Genome maps of various viruses, plasmids and transposons in archaea, bacteria and eukaryotes. Homologous genes are colour-coded. Hatched regions in the protein-primed type B DNA polymerase (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. VD1 and VD2 are the two genomic segments of the Bombyx mori bidensovirus 2 (BmBDV2). DJR, double jelly-roll; Ginger1-4_HM, transposon 4 of Hydra magnipapillata; MCP, major capsid protein; P1_DY, Polinton 1 of Drosophila yakuba; P1_TV, Polinton 1 of Trichomonas vaginalis; P3_TC, Polinton 3 of Tribolium castaneum; RNAP, RNA polymerase; TIR, terminal inverted repeat; Tlr1, Polinton-like transposable element from Tetrahymena thermophila.
Figure 2
Figure 2. Structural features of some viruses with double jelly-roll major capsid proteins
a | Representation of the icosahedral virion with triangulation number (T)=25; this organization is found in tectiviruses and adenoviruses. The pentagonal capsomers (shown in red) are composed of five copies of the penton protein, which has a single jelly-roll fold, whereas the hexagonal capsomers are trimers of the major capsid protein (MCP) with the double jelly-roll (DJR) topology. X-ray structures of the tectivirus PRD1 penton and MCP are shown as examples (Protein Data Bank (PDB) identifier: 1W8X). b | Structural models of the MCPs of Tlr1 (Polinton-like transposable element from Tetrahymena thermophila) and P1_DR (Polinton 1 from Danio rerio). c–e | X-ray structures of the DJR MCPs from the eukaryotic viruses PBCV1 (Paramecium bursaria Chlorella virus 1; PDB identifier: 1M4X) (c), HAdV2 (human adenovirus type 2; PDB identifier: 1P2Z) (d) and Sputnik (PDB identifier: 3J26) (e).
Figure 3
Figure 3. Phylogenetic analysis of protein-primed type B DNA polymerases from mobile elements in archaea, bacteria and eukaryotes
The maximum likelihood tree was calculated using PhyML, with the WAG (Whelan and Goldman) model of amino-acid substitution, including a gamma law (four categories) and an estimated proportion of invariable sites. Numbers at the branch points represent SH (Shimodaira–Hasegawa)-like local support values. The tree is rooted with bacterial phi29-like podoviruses. Branches with support values below 75% were collapsed. Branches are coloured according to the classification of the corresponding taxa. The branching of the major taxonomic groups is consistent with that obtained previously using different phylogenetic analysis methods and different taxonomic sampling,,,. The scale bar represents the number of substitutions per site.
Figure 4
Figure 4. A hypothetical scenario for the evolution of various eukaryotic viruses and plasmids
In this scenario, the Polintons evolved from a tectivirus-like ancestor, which entered the proto-eukaryotic host within a bacterial endosymbiont that subsequently gave rise to the mitochondria. Polintons reside in the nucleus, and the key event in the emergence of both cytoplasmic plasmids and the proposed order ‘Megavirales’ was escape from the nucleus, which was associated with the acquisition of RNA polymerase (RNAP) and the capping apparatus from the host. The essential events in the evolution of Megavirales from the cytoplasmic Polinton-like ancestor were the replacement of protein-primed type B DNA polymerase (pPolB) with the RNA/DNA-primed PolB, the acquisition of the D5-like helicase–primase and genome expansion. Polintons are also implicated in the evolution of virophages, bidnaviruses and adenoviruses. The hexagons represent icosahedral capsids; in the case of Polintons, the capsids have been predicted to exist but have not yet been observed (indicated by a question mark). Double strands represent double-stranded DNA, whereas the single-stranded DNA genome of bidnaviruses is shown as a single strand. INT, retroviral-like (RVE) family integrase; PRO, adenovirus-type cysteine protease.
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