Polintons and network-like evolution of the virus world

Polintons Eukaryote genomes are populated by DNA copies of parasitic elements known as transposable elements capable of reproducing themselves in the host genome in a non-Mendelian fashion. Understanding the biology of transposable elements is important because of their impact on genome evolution. Eukaryotic transposable elements were thought to belong to only two types, called retrotransposons and DNA transposons. Retrotransposons are replicated via reverse transcription of its mRNAs, DNA transposons are transposed via transfer of its genomic copy from one site to another. In 2005, a new class of transposable element was proposed, the Polintons:

Self-synthesizing DNA transposons in eukaryotes. (2006) Proceedings of the National Academy of Sciences of the United States of America, 103(12): 4540-4545
Eukaryotes contain numerous transposable or mobile elements capable of parasite-like proliferation in the host genome. All known transposable elements in eukaryotes belong to two types: retrotransposons and DNA transposons. Here we report a previously uncharacterized class of DNA transposons called Polintons that populate genomes of protists, fungi, and animals, including entamoeba, soybean rust, hydra, sea anemone, nematodes, fruit flies, beetle, sea urchin, sea squirt, fish, lizard, frog, and chicken. Polintons from all these species are characterized by a unique set of proteins necessary for their transposition, including a protein-primed DNA polymerase B, retroviral integrase, cysteine protease, and ATPase. In addition, Polintons are characterized by 6-bp target site duplications, terminal-inverted repeats that are several hundred nucleotides long, and 5′-AG and TC-3′ termini. Analogously to known transposable elements, Polintons exist as autonomous and nonautonomous elements. Our data suggest that Polintons have evolved from a linear plasmid that acquired a retroviral integrase at least 1 billion years ago. According to the model of Polinton transposition proposed here, a Polinton DNA molecule excised from the genome serves as a template for extrachromosomal synthesis of its double-stranded DNA copy by the Polinton-encoded DNA polymerase and is inserted back into genome by its integrase.

A new review article looks at the relationship between Polintons and viruses and suggests that 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:

Polintons: a hotbed of eukaryotic virus, transposon and plasmid evolution. (2015) Nature Reviews Microbiology 13: 105–115 doi:10.1038/nrmicro3389
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.

More:

Virophages, polintons, and transpovirons: a complex evolutionary network of diverse selfish genetic elements with different reproduction strategies. (2013) Virol J, 10(158): doi: 10.1186/1743-422X-10-158
Recent 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. We 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 unknown virus. 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. The 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.

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