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Comparative Study
. 2011 Oct 18;108(42):17486-91.
doi: 10.1073/pnas.1110889108. Epub 2011 Oct 10.

Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae

Defne Arslan  1 , Matthieu Legendre, Virginie Seltzer, Chantal Abergel, Jean-Michel Claverie
Affiliations
Comparative Study

Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae

Defne Arslan et al. Proc Natl Acad Sci U S A. .

Abstract

Mimivirus, a DNA virus infecting acanthamoeba, was for a long time the largest known virus both in terms of particle size and gene content. Its genome encodes 979 proteins, including the first four aminoacyl tRNA synthetases (ArgRS, CysRS, MetRS, and TyrRS) ever found outside of cellular organisms. The discovery that Mimivirus encoded trademark cellular functions prompted a wealth of theoretical studies revisiting the concept of virus and associated large DNA viruses with the emergence of early eukaryotes. However, the evolutionary significance of these unique features remained impossible to assess in absence of a Mimivirus relative exhibiting a suitable evolutionary divergence. Here, we present Megavirus chilensis, a giant virus isolated off the coast of Chile, but capable of replicating in fresh water acanthamoeba. Its 1,259,197-bp genome is the largest viral genome fully sequenced so far. It encodes 1,120 putative proteins, of which 258 (23%) have no Mimivirus homologs. The 594 Megavirus/Mimivirus orthologs share an average of 50% of identical residues. Despite this divergence, Megavirus retained all of the genomic features characteristic of Mimivirus, including its cellular-like genes. Moreover, Megavirus exhibits three additional aminoacyl-tRNA synthetase genes (IleRS, TrpRS, and AsnRS) adding strong support to the previous suggestion that the Mimivirus/Megavirus lineage evolved from an ancestral cellular genome by reductive evolution. The main differences in gene content between Mimivirus and Megavirus genomes are due to (i) lineages specific gains or losses of genes, (ii) lineage specific gene family expansion or deletion, and (iii) the insertion/migration of mobile elements (intron, intein).

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Electron microscopy of Megavirus compared with Mimivirus. (A) Mimivirus (Upper) and Megavirus (Lower) particles in a same vacuole (coinfection). (A, Inset) Cowlicks (arrow) as often seen in the Megavirus fiber outer layer. (B) Megavirus stargate. (B, Inset) Transversal section of a Megavirus particle below an open stargate. Megavirus (C) and Mimivirus (D) seeds surrounded by a lipid membrane (arrows). Megavirus (E) and Mimivirus (F) early stages of the virion factories with the seeds at their centers. Megavirus (G) and Mimivirus (H) mature virion factories in full production. (Scale bars: A–F, 200 nm; G and H, 1 μm).
Fig. 2.
Fig. 2.
Comparison of Mimivirus and Megavirus genomes. (A) Colinearity of Mimivirus and Megavirus CDSs. Each dot symbolizes the best BLAST match (e value ≤ 10−5) between the CDSs of the two viruses, in the same orientation (blue) or in reverse orientation (red). (B) The distribution of homologous CDSs. Megavirus 594 CDSs with Mimivirus orthologs are shown in red. The 268 additional Megavirus CDSs with a significant (nonreciprocal) match in Mimivirus CDSs are shown in blue. CDSs specific to Megavirus are shown in yellow. Orthologs clearly cluster in the central region, whereas the two other categories of CDSs (e.g., duplicated in or specific to Megavirus) tend to cluster at the extremities.
Fig 3.
Fig 3.
Phylogenetic reconstruction of IleRS sequences. The midpoint-rooted neighbor-joining tree was generated from a 381-aa alignment of conserved positions. The tree topology and bootstrap values were very similar when using different alignment programs, reconstruction methods, and substitution models) (SI Materials and Methods and Materials and Methods). The Megavirus (star) and CroV IleRS sequences are branching off the eukaryote domain before the radiation of the cytoplasmic IleRSs.
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