Nucleo‐cytoplasmic Large DNA Viruses (NCLDV) of Eukaryotes

Abstract

A group of diverse viruses with large deoxyribonucleic acid (DNA) genomes that replicate in the cytoplasm and in some cases partly in the nucleus of eukaryotic cells share a set of conserved genes and probably have evolved from a common ancestral virus. Known as nucleo‐cytoplasmic large DNA viruses (NCLDV), this class of viruses encompasses seven families: Poxviridae, Asfarviridae, Iridoviridae, Ascoviridae, Phycodnaviridae, Mimiviridae, and a probable new family represented by Marseillevirus and Lausannevirus. The family Mimiviridae includes giant viruses that possess genomes of a million or more basepairs that are comparable in size and complexity with some bacterial genomes. Phylogenetic analysis of the conserved genes of the NCLDV and mapping of the resulting phylogeny of the NCLDV onto the phylogeny of their eukaryotic hosts suggest an early origin and primary radiation of the NCLDV, possibly concomitant with the primary radiation of eukaryotes.

Key Concepts:

  • Seven families of viruses with large double‐stranded DNA genomes together constitute a monophyletic class of viruses known as Nucleo‐Cytoplasmic Large DNA Viruses (NCLDV).

  • All NCLDV share several genes that encode essential proteins involved in viral genome replication and virion formation.

  • An evolutionary reconstruction using a maximum‐likelihood model assigns approximately 50 genes coding for most of the key virus functions to the common ancestor of all extant NCLDV.

  • Some of the NCLDV families infect many diverse eukaryotes whereas many groups of eukaryotes are infected by diverse NCLDV suggesting that the major radiation of the NCLDV occurred at an early stage of evolution, perhaps concomitantly with eukaryogenesis.

  • The NCLDV includes the largest known viruses: Mimiviruses which encode over 1000 genes and are comparable to bacteria in size and complexity.

Keywords: giant viruses; evolution of viruses; virus families; evolutionary reconstruction; phylogenetic analysis

Figure 1.

(a) Megavirus particle. Thin section, electron microscopy. Credits: Chantal Abergel. Image source: http://en.wikipedia.org/wiki/File:Megavirus.jpg This work is licensed under a Creative Commons Attribution‐ShareAlike 3.0 Unported License. (b) This electron micrograph depicts a number of morphologic variants found in the parapox Orf virus (Poxviridae) common to sheep and goats. Credits: Centres for Disease Control and Prevention, United States Department of Health and Human Services; Public Health Image Library (PHIL; http://phil.cdc.gov/phil/home.asp) Image ID#: 5577. (c) This transmission electron micrograph (TEM) depicts a number of smallpox virus virions. The ‘dumbbell‐shaped’ structure inside the smallpox virion is the viral core containing the viral DNA. Credits: Dr. Fred Murphy; Sylvia Whitfield, Centres for Disease Control and Prevention, United States Department of Health and Human Services; PHIL Image ID#: 1849.

Figure 2.

Schematic representation of NCLDV reproduction. (a) Nucleo‐cytoplasmic reproduction. (b) Cytoplasmic‐only reproduction. Main replication cycle events: (1) Entry; (2) early messenger ribonucleic acid (mRNA), early proteins, deoxyribonucleic acid (DNA) replication; (3) mRNA, late protein synthesis, virion assembly; (4) release of progeny virus particles.

Figure 3.

Phylogenetic tree of the DNA polymerases of the NCLDV. In addition to known viruses, the tree includes environmental sequences isolated by metagenomics that are denoted with their GenBank identifiers. For each virus family (and two subfamilies in the case of iridoviruses), a schematic image of the virion (roughly to scale) is shown; the virus membrane is shown in blue.

Figure 4.

Reconstruction of the NCLDV evolution. The phylogenetic tree of the core genes of the NCLDV is shown in a simplified schematic form; the tree topology is as in Figure . The number of genes inferred in the reconstruction is shown for each ancestral node. Reproduced from Yutin et al. () (an Open Access publication). Amsmo, Amsacta moorei entomopoxvirus; Melsa, Melanoplus sanguinipes entomopoxvirus; Helvi, Heliothis virescens ascovirus 3e; Trini, Ttrichoplusia 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.

Figure 5.

Cross‐mapping of the phylogenetic trees of the NCLDV and eukaryotes. The NCLDV tree topology is as in Figure; the chordopoxvirus and chlorovirus branches are collapsed. The eukaryotic tree is shown as a multifurcation of five supergroups. Lines connect viruses with their host organisms; solid lines show established virus‐host relationships, and broken lines show putative relationships derived from metagenomic data. Reproduced from Yutin et al. () (an Open Access publication).

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Further Reading

Boyer M, Azza S, Barrassi L et al. (2011) Mimivirus shows dramatic genome reduction after intraamoebal culture. Proceedings of the National Academy of Sciences of the USA 108: 10296–10301.

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Koonin EV (2011) The Logic of Chance: The Nature and Origin of Biological Evolution. Upper Saddle River, NJ: FT press.

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Moreira D and López‐García P (2009) Ten reasons to exclude viruses from the tree of life. Nature Reviews Microbiology 7: 306–311.

Raoult D and Boyer M (2010) Amoebae as genitors and reservoirs of giant viruses. Intervirology 53: 321–329.

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How to Cite close
Koonin, Eugene V, and Yutin, Natalya(May 2012) Nucleo‐cytoplasmic Large DNA Viruses (NCLDV) of Eukaryotes. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023268]