A Virophage at the Origin of Large DNA Transposons

Abstract

DNA transposons are mobile genetic elements that have shaped the genomes of eukaryotes for millions of years, yet their origins remain obscure. We discovered a virophage that, on the basis of genetic homology, likely represents an evolutionary link between double-stranded DNA viruses and Maverick/Polinton eukaryotic DNA transposons. The Mavirus virophage parasitizes the giant Cafeteria roenbergensis virus and encodes 20 predicted proteins, including a retroviral integrase and a protein-primed DNA polymerase B. On the basis of our data, we conclude that Maverick/Polinton transposons may have originated from ancient relatives of Mavirus, and thereby influenced the evolution of eukaryotic genomes, although we cannot rule out alternative evolutionary scenarios.

Virophages go nuclear in the marine alga Bigelowiella natans

“…The Sputnik virophage can adhere to long fibers on the surface of the mimivirus capsid, and it is assumed that Sputnik hitches a ride when mimivirus is phagocytosed by the amoebal host cell (8). By contrast, the mavirus virophage enters the host cell independently of its giant virus CroV, which lacks an external fiber coat (9). Another mechanism by which a virophage can stay in touch with its host cell or giant virus is to insert its genome into either host genome.…”

“…Whether this transcriptional activity is indicative of a biological mechanism that might benefit virophage or host cell remains to be tested. However, based on the protective effect that virophages like Sputnik or mavirus have on their host cell populations in the presence of giant viruses (7,9), it is tempting to speculate that the Bigelowiella provirophages could interfere with the replication of a B. natans-infecting large DNA virus. Blanc et al propose a scenario in which virophages could enter the host cell independently of a giant virus and integrate into the host genome.…”

“…1). Indeed, this scenario would describe a mutualistic relationship between a virus and a host cell (2): the host cell provides an opportunity to the virophage to persist and spread vertically within the host population, and, in return, the virophage protects the host cell from lysis by giant viruses (9,11).…”

Sputnik and Mavirus: more than just satellite viruses

“…Giant viruses such as APMV and CroV replicate in large cytoplasmic virion factories, and encode an enzymatic complexity that is unrivalled among viruses and includes a presumably complete transcription apparatus, which is packaged in the virion and used to initiate viral gene transcription at the early stage of infection [9][10][11][12] . Although yet to be confirmed experimentally, Sputnik and Mavirus appear to depend on the transcription system of their associated giant viruses, as strongly suggested by the specific promoter and polyadenylation signals that are shared between these virophages and their giant viruses 4,13,14 . Consequently, if dependence on another organism's transcription system is sufficient for classification as a subviral agent, then we must consider all but the most complex DNA viruses as satellite viruses, as the majority of them depend on the transcription machinery of the host cell.…”

“…Instead, virophages appear to be fully functional viruses, as they encode their own proteins for particle structure and DNA replication. On the one hand, the capsid proteins of Sputnik, Mavirus and Organic Lake virophage (OLV) are related to each other [3][4][5] but bear no significant sequence similarity to their giant virus counterparts, even though they are likely to adopt the double-jelly-roll fold that is typical of capsid proteins from viruses of the bacteriophage PRD1-adenovirus lineage (which includes APMV and CroV) 6 . The DNA replication systems of virophages, on the other hand, differ from one species to the next; Mavirus encodes a predicted proteinprimed B-family DNA polymerase 4 , whereas a recently described phage T7-like DNA polymerase (fused to a helicase) is found in Sputnik and OLV 5,7 .…”