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. 2010;53(5):284-92.
doi: 10.1159/000312913. Epub 2010 Jun 15.

Origin and evolution of eukaryotic large nucleo-cytoplasmic DNA viruses

Eugene V Koonin  1 , Natalya Yutin
Affiliations

Origin and evolution of eukaryotic large nucleo-cytoplasmic DNA viruses

Eugene V Koonin et al. Intervirology. 2010.

Abstract

Background/aims: The nucleo-cytoplasmic large DNA viruses (NCLDV) constitute an apparently monophyletic group that consists of 6 families of viruses infecting a broad variety of eukaryotes. A comprehensive genome comparison and maximum-likelihood reconstruction of NCLDV evolution reveal a set of approximately 50 conserved genes that can be tentatively mapped to the genome of the common ancestor of this class of eukaryotic viruses. We address the origins and evolution of NCLDV.

Results: Phylogenetic analysis indicates that some of the major clades of NCLDV infect diverse animals and protists, suggestive of early radiation of the NCLDV, possibly concomitant with eukaryogenesis. The core NCLDV genes seem to have originated from different sources including homologous genes of bacteriophages, bacteria and eukaryotes. These observations are compatible with a scenario of the origin of the NCLDV at an early stage of the evolution of eukaryotes through extensive mixing of genes from widely different genomes.

Conclusions: The common ancestor of the NCLDV probably evolved from a bacteriophage as a result of recruitment of numerous eukaryotic and some bacterial genes, and concomitant loss of the majority of phage genes except for a small core of genes coding for proteins essential for virus genome replication and virion formation.

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Figures

Fig. 1
Fig. 1
Cross-mapping of the phylogenetic trees of the NCLDV and eukaryotes, the chordopoxvirus and chlorovirus branches are collapsed. The eukaryotic tree is shown as a multifurcation of 5 supergroups. Lines connect viruses with their host organisms. Solid lines show established virus-host relationships; broken lines show putative relationships inferred from metagenomic data. The short broken line from Iridoviridae is to indicate that, according to metagenomic results, members of this family probably infect marine unicellular eukaryotes but the exact unicellular hosts are not known. Adapted from [15, 20].
Fig. 2
Fig. 2
Reconstruction of the evolution of the NCLDV gene repertoire. Numbers at internal nodes indicate the number of genes assigned to the given ancestral form with high confidence [15]. Amsmo = Amsacta moorei entomopoxvirus; Melsa = melanoplus sanguinipes entomopoxvirus; Helvi = heliothis virescens ascovirus 3e; Trini = trichoplusia ni ascovirus 2c; Spofr = spodoptera frugiperda ascovirus 1a; Afrsw = African swine fever virus; Aedta = aedes taeniorhynchus iridescent virus (Invertebrate iridescent virus 3); Invir = invertebrate iridescent virus 6; Lymdi = lymphocystis disease virus 1; Lymch = lymphocystis disease virus isolate China; Infsp = infectious spleen and kidney necrosis virus; Singr = Singapore grouper iridovirus; Frovi = frog virus 3; Ambti = ambystoma tigrinum virus; Acapo = acanthamoeba polyphaga mimivirus; Mamav = Mamavirus; Emihu = emiliania huxleyi virus 86; Felsp = Feldmannia species virus; Ectsi = ectocarpus siliculosus virus 1; Ostvi = ostreococcus virus OsV5; Marvi = Marseillevirus.
Fig. 3
Fig. 3
Breakdown of the 47 genes mapped to the ancestral NCLDV genome by likely origin. The data are from table 2.
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