Virophages go nuclear in the marine alga Bigelowiella natans.

The virus world in which we live will never cease to amaze us. Historically, viruses were studied primarily from medical and economic perspectives; however, the last decades have shown that viruses play roles far more versatile than we could have imagined. Being the most abundant biological entities on the planet (there are ∼10 virus particles in every liter of seawater), viruses drive biogeochemical cycles on a global scale (1), they affect biodiversity and community structures of their hosts [for which they can even act as symbionts (2)], and perhaps most profoundly, viruses have influenced all cellular life from its very beginning and they continue to leave their footprints in cellular genomes (3, 4), including our own. One of biggest surprises in recent virological history was the discovery of Acanthamoeba polyphaga mimivirus and other giant viruses, whose particles can be seen under a light microscope and contain DNA genomes that code for more than 1,000 proteins (5). As it turns out, giant viruses are rather common in the environment, infecting freshwater amoebae as well as marine heterotrophic and photosynthetic protists (6). Another unexpected finding was that giant viruses in the family Mimiviridae were associated with a previously unknown group of smaller double-stranded DNA (dsDNA) viruses that acted as parasites of the former. Dubbed “virophages,” these icosahedrally shaped viruses with 20to 30-kilobase-pair (kbp) genomes replicate in the cytoplasmic virus factories of their giant viruses, where they exploit the transcriptional machinery of their viral host (7). To replicate, virophages must therefore infect a susceptible host cell that is coinfected with a permissive giant virus, i.e., a virus that has the capacity to support gene expression of the virophage. Virophages appear to have evolved multiple strategies to track down their viral and cellular hosts. 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. Whereas Sputnik integration into the mimivirus genome has been described (10), no provirophages (i.e., integrated virophage genomes) in a eukaryotic genome have been found so far. In PNAS, Blanc et al. (11) now report such a case. The authors searched through more than 1,000 eukaryotic genomes for signatures of virophages, and they struck gold in the unicellular alga Bigelowiella natans. B. natans belongs to a group of mixotrophic protists called chlorarachniophytes that have trodden an interesting evolutionary path. Their