Self-synthesizing transposons: unexpected key players in the evolution of viruses and defense systems

Abstract

Self-synthesizing transposons are the largest known transposable elements that encode their own DNA polymerases (DNAP). The Polinton/Maverick family of self-synthesizing transposons is widespread in eukaryotes and abundant in the genomes of some protists. In addition to the DNAP and a retrovirus-like integrase, most of the polintons encode homologs of the major and minor jelly-roll capsid proteins, DNA-packaging ATPase and capsid maturation protease. Therefore, polintons are predicted to alternate between the transposon and viral lifestyles although virion formation remains to be demonstrated. Polintons are related to a group of eukaryotic viruses known as virophages that parasitize on giant viruses of the family Mimiviridae and another recently identified putative family of polinton-like viruses (PLV) predicted to lead a similar, dual life style. Comparative genomic analysis of polintons, virophages, PLV and the other viruses with double-stranded (ds)DNA genomes infecting eukaryotes and prokaryotes suggests that the polintons evolved from bacterial tectiviruses and could have been the ancestors of a broad range of eukaryotic viruses including adenoviruses and members of the proposed order “Megavirales” as well as linear cytoplasmic plasmids. Recently, a group of predicted self-synthesizing transposons was discovered also in prokaryotes. These elements, denoted casposons, encode a DNAP and a homolog of the CRISPR-associated Cas1 endonuclease that has an integrase activity but no capsid proteins. Thus, unlike polintons, casposons appear to be limited to the transposon life style although they could have evolved from viruses. The casposons are thought to have played a pivotal role in the origin of the prokaryotic adaptive immunity, giving rise to the adaptation module of the CRISPR-Cas systems.

Bipartite Network Analysis of the Archaeal Virosphere: Evolutionary Connections between Viruses and Capsidless Mobile Elements

“…Module 5 encompasses ampullaviruses and family 1 casposons, a recently discovered class of self-synthesizing DNA transposons which employ the Cas1 endonuclease for integration (59)(60)(61). The ampullaviruses and the casposons comprise two distinct submodules within this module; the two submodules cluster together in 55% of replicas ( Fig.…”

Evolutionary Genomics of Defense Systems in Archaea and Bacteria

“…Examination of the genomic context of cas1 homologs that are not associated with CRISPR- cas loci led to the discovery of a novel superfamily of self-synthesizing transposons, the casposons, so named because the Cas1 homolog they encode was predicted to function as the transposase (integrase) (91, 92). The integrase activity of the casposon-encoded Cas1 (dubbed the casposase) subsequently has been validated experimentally (58), and similar target site specificities of casposon integration and CRISPR spacer incorporation have been demonstrated (9).…”

Polintons, virophages and transpovirons: a tangled web linking viruses, transposons and immunity

“…These elements have genomes of 15 to 20 kilobase (kb), the largest among the known transposons, flanked by long terminal inverted repeats (TIRs). In addition to the two universal genes coding for a protein-primed DNA polymerase (pDNAP) and a retrovirus-like (RVE) integrase, most of the Polintons also encode a DNA-packaging ATPase and a maturation protease that are homologous to the morphogenetic enzymes of Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) of eukaryotes [11,12]. Because of their large size (on the transposon scale) and the presence of genes for morphogenetic enzymes, Polintons have been considered ‘virus-like’ transposons since the time they were discovered, but neither actual virions nor structural proteins have been detected [7,8].…”

“…in the protist Trichomonas vaginalis [11]. These findings imply that Polintons lead a dual life style that involves both a transposon and a virus stage although the virions and the conditions of their formation remain to be characterized [11,12]. The discovery of the capsid protein genes prompted the proposal to rename the Polintons to polintoviruses [11,12] but pending the experimental validation of the prediction, we generally refer to these elements by their original name, using the term polintoviruses only when virions are specifically discussed.…”