Provirophages in the Bigelowiella genome bear testimony to past encounters with giant viruses

Abstract

Virophages are recently discovered double-stranded DNA virus satellites that prey on giant viruses (nucleocytoplasmic large DNA viruses; NCLDVs), which are themselves parasites of unicellular eukaryotes. This coupled parasitism can result in the indirect control of eukaryotic cell mortality by virophages. However, the details of such tripartite relationships remain largely unexplored. We have discovered ∼300 predicted genes of putative virophage origin in the nuclear genome of the unicellular alga Bigelowiella natans. Physical clustering of these genes indicates that virophage genomes are integrated into the B. natans genome. Virophage inserts show high levels of similarity and synteny between each other, indicating that they are closely related. Virophage genes are transcribed not only in the sequenced B. natans strain but also in other Bigelowiella isolates, suggesting that transcriptionally active virophage inserts are widespread in Bigelowiella populations. Evidence that B. natans is also a host to NCLDV members is provided by the identification of NCLDV inserts in its genome. These putative large DNA viruses may be infected by B. natans virophages. We also identify four repeated elements sharing structural and genetic similarities with transpovirons-a class of mobile elements first discovered in giant viruses-that were probably independently inserted in the B. natans genome. We argue that endogenized provirophages may be beneficial to both the virophage and B. natans by (i) increasing the chances for the virophage to coinfect the host cell with an NCLDV prey and (ii) defending the host cell against fatal NCLDV infections.virophage | nucleocytoplasmic large DNA virus | microbial community | endogenous virus | Maverick/polinton

The Expanding Family of Virophages

“…In 2015, virophage genomes integrated into the nuclear genome of the unicellular alga Bigelowiella natans were described, and found to be highly transcribed [46]. In the same genome, they also observed sequences from Megavirales members and repeated elements that matched with transpovirons.…”

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

“…The virophages outside the Mavirus group lack the RVE but recently many of them have been shown to encode a distinct subfamily of tyrosine recombinases that is likely to function as an integrase [13]. Indeed, integration of virophages into the genomes of giant viruses [32] and even more notably, into the genome of a cellular organism, the green alga Bigelowiella natans [33,34], has been demonstrated. Most virophages also lack the DNAP gene but recently, a new group of putative virophages has been assembled from the sheep rumen metagenome and shown to encode a DNAP related to the polinton-encoded polymerases [26].…”

Virophages go nuclear in the marine alga Bigelowiella natans

“…The largest such fragment is 165 kbp long and contains 83 genes, most of which are unknown, but some display clear phylogenetic affinities to large algal viruses. In contrast to the virophage-like elements, the large virus insert was found to be transcriptionally silent and had a G+C content similar to that of the host nuclear genome (11). This algal lineage has apparently witnessed multiple encounters with DNA viruses of various sizes.…”

“…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).…”

“…Remarkably, not only does the B. natans genome harbor virophage-like elements, it also contains pieces of putative large DNA virus genomes (11). The largest such fragment is 165 kbp long and contains 83 genes, most of which are unknown, but some display clear phylogenetic affinities to large algal viruses.…”