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Genome of Phaeocystis globosa virus PgV-16T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes - PubMed

  • ️Tue Jan 01 2013

Genome of Phaeocystis globosa virus PgV-16T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes

Sebastien Santini et al. Proc Natl Acad Sci U S A. 2013.

Abstract

Large dsDNA viruses are involved in the population control of many globally distributed species of eukaryotic phytoplankton and have a prominent role in bloom termination. The genus Phaeocystis (Haptophyta, Prymnesiophyceae) includes several high-biomass-forming phytoplankton species, such as Phaeocystis globosa, the blooms of which occur mostly in the coastal zone of the North Atlantic and the North Sea. Here, we report the 459,984-bp-long genome sequence of P. globosa virus strain PgV-16T, encoding 434 proteins and eight tRNAs and, thus, the largest fully sequenced genome to date among viruses infecting algae. Surprisingly, PgV-16T exhibits no phylogenetic affinity with other viruses infecting microalgae (e.g., phycodnaviruses), including those infecting Emiliania huxleyi, another ubiquitous bloom-forming haptophyte. Rather, PgV-16T belongs to an emerging clade (the Megaviridae) clustering the viruses endowed with the largest known genomes, including Megavirus, Mimivirus (both infecting acanthamoeba), and a virus infecting the marine microflagellate grazer Cafeteria roenbergensis. Seventy-five percent of the best matches of PgV-16T-predicted proteins correspond to two viruses [Organic Lake phycodnavirus (OLPV)1 and OLPV2] from a hypersaline lake in Antarctica (Organic Lake), the hosts of which are unknown. As for OLPVs and other Megaviridae, the PgV-16T sequence data revealed the presence of a virophage-like genome. However, no virophage particle was detected in infected P. globosa cultures. The presence of many genes found only in Megaviridae in its genome and the presence of an associated virophage strongly suggest that PgV-16T shares a common ancestry with the largest known dsDNA viruses, the host range of which already encompasses the earliest diverging branches of domain Eukarya.

Keywords: core gene; gene duplication; giant virus; horizontal gene transfer; mobile element.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.

Global database similarity of the PgV-16T predicted proteome. (A) Close to 50% of PgV predicted proteins do not exhibit a significant match (E < 10−5) in the NCBI NR protein database, as is typical for viruses belonging to a newly explored lineage with no other sequenced representatives (2, 6). (B) Surprisingly, for 77% of the PgV predicted proteins exhibiting a viral protein as their best match, this homolog is found in the partially sequenced OLPV1 or -2. This finding indicates strong global phylogenetic affinities between PgV (infecting a haptophyte) and the OLPVs infecting an unknown host.

Fig. 2.
Fig. 2.

Map of the PgV-16T–associated virophage-like genome. Predicted ORFs are indicated by boxes colored according to their annotation status: with a predicted function (green), with a significant (E < 10–5) match in the NR database (yellow), and no match (white). The flanking arrows represent two 1-kb-long, nearly identical sequences complementary to each other.

Fig. 3.
Fig. 3.

Fraction of protein-coding genes shared by the largest known viral genomes at increasing evolutionary distance. (A and B) Venn diagrams indicating the global proximity in gene content of the four large genomes of Mimivirus, Megavirus, CroV, and PgV. (C and D) Venn diagrams indicating that EhV and PgV exhibit a markedly different gene content (they only share “core” genes conserved in most large eukaryotic dsDNA virus, irrespective of family;

Table S1

), even though they both infect a haptophyte.

Fig. 4.
Fig. 4.

Phylogenetic position of PgV-16T among dsDNA viruses. Neighbor-joining (midpoint-rooted) tree computed from a multiple alignment of 49 viral DNA polymerase B sequences (405 ungapped sites) using the default options of the MAFFT server (30) and drawn using Mega (31). The tree was collapsed for bootstrap values of <50. The tree clearly suggests that the viruses with the largest known genome form a well-supported cluster, irrespective of their hosts: phagotrophic protozoans (in red) or photosynthetic unicellular algae (in green). Viruses presently classified as “phycodnaviruses” (e.g., “algal viruses”) (green and blue) do not form a monophyletic lineages.

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