Towards defining the chloroviruses: a genomic journey through a genus of large DNA viruses

Abstract

BackgroundGiant viruses in the genus Chlorovirus (family Phycodnaviridae) infect eukaryotic green microalgae. The prototype member of the genus, Paramecium bursaria chlorella virus 1, was sequenced more than 15 years ago, and to date there are only 6 fully sequenced chloroviruses in public databases. Presented here are the draft genome sequences of 35 additional chloroviruses (287 – 348 Kb/319 – 381 predicted protein encoding genes) collected across the globe; they infect one of three different green algal species. These new data allowed us to analyze the genomic landscape of 41 chloroviruses, which revealed some remarkable features about these viruses.ResultsGenome colinearity, nucleotide conservation and phylogenetic affinity were limited to chloroviruses infecting the same host, confirming the validity of the three previously known subgenera. Clues for the existence of a fourth new subgenus indicate that the boundaries of chlorovirus diversity are not completely determined. Comparison of the chlorovirus phylogeny with that of the algal hosts indicates that chloroviruses have changed hosts in their evolutionary history. Reconstruction of the ancestral genome suggests that the last common chlorovirus ancestor had a slightly more diverse protein repertoire than modern chloroviruses. However, more than half of the defined chlorovirus gene families have a potential recent origin (after Chlorovirus divergence), among which a portion shows compositional evidence for horizontal gene transfer. Only a few of the putative acquired proteins had close homologs in databases raising the question of the true donor organism(s). Phylogenomic analysis identified only seven proteins whose genes were potentially exchanged between the algal host and the chloroviruses.ConclusionThe present evaluation of the genomic evolution pattern suggests that chloroviruses differ from that described in the related Poxviridae and Mimiviridae. Our study shows that the fixation of algal host genes has been anecdotal in the evolutionary history of chloroviruses. We finally discuss the incongruence between compositional evidence of horizontal gene transfer and lack of close relative sequences in the databases, which suggests that the recently acquired genes originate from a still largely un-sequenced reservoir of genomes, possibly other unknown viruses that infect the same hosts.

Potassium Ion Channels: Could They Have Evolved from Viruses?

“…This conclusion is supported by a recent comprehensive bioinformatics analysis of 35 newly sequenced chloroviruses, plus six previously sequenced chloroviruses (Jeanniard et al, 2013). This analysis included 14 NC64A viruses, 13 SAG viruses, and 14 Pbi viruses.…”

“…Some chloroviruses encode functional aquaglyceroporins , K + /H + transporters (Greiner et al, 2011), and Ca ++ -transporting ATPases (Bonza et al, 2010). Relevant to this discussion, 39 of the 41 chloroviruses have genes predicted to encode K + channel proteins (Jeanniard et al, 2013). One peculiarity of the chlorovirus K + channel proteins is that their monomers are small.…”

“…Collectively, these 41 viruses encode 632 putative proteins, of which, any one virus encodes 319 to 416 proteins (Jeanniard et al, 2013). Some chloroviruses encode functional aquaglyceroporins , K + /H + transporters (Greiner et al, 2011), and Ca ++ -transporting ATPases (Bonza et al, 2010).…”

Seasonal determinations of algal virus decay rates reveal overwintering in a temperate freshwater pond

“…Moreover, other nucleic acid metabolism genes encoded by algal viruses that could aid in environmental persistence include DNA ligase, DNA polymerase δ, proliferating cell nuclear antigen, as well as genes involved in base incision repair and nucleotide incision repair (Dunigan et al, 2006;Redrejo-Rodriguez and Salas, 2014). The absence of denV homologs in some chlorovirus strains such as KS1B, and other DNA repair genes in other algal virus genomes, demonstrates that these capabilities are not universally present among algal viruses (Jeanniard et al, 2013). Furthermore, the genome of EhV-86, a coccolithovirus, contains a pyrimidine dimer-specific glycosylase, while the genome of EsV-1, a phaeovirus, does not (Dunigan et al, 2006).…”

“…Many, but not all, genomes of chloroviruses, including ATCV-1 and CVM-1, contain homologs of a UV repair gene, denV, which encodes a UV-specific DNA glycosylasepyrimidine lyase (Fitzgerald et al, 2007;Jeanniard et al, 2013) known to be functional in the strain PBCV-1 (Furuta et al, 1997). Moreover, other nucleic acid metabolism genes encoded by algal viruses that could aid in environmental persistence include DNA ligase, DNA polymerase δ, proliferating cell nuclear antigen, as well as genes involved in base incision repair and nucleotide incision repair (Dunigan et al, 2006;Redrejo-Rodriguez and Salas, 2014).…”