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, 5 (1), 102-6

Genomics of Megavirus and the Elusive Fourth Domain of Life

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Genomics of Megavirus and the Elusive Fourth Domain of Life

Matthieu Legendre et al. Commun Integr Biol.

Abstract

We recently described Megavirus chilensis, a giant virus isolated off the coast of Chile, also replicating in fresh water acanthamoeba. Its 1,259,197-bp genome encodes 1,120 proteins and is the largest known viral genome. Megavirus and its closest relative Mimivirus only share 594 orthologous genes, themselves sharing only 50% of identical residues in average. Despite this divergence, comparable to the maximal divergence exhibited by bacteria within the same division (e.g., gamma proteobacteria), Megavirus retained all of the genomic features unique to Mimivirus, in particular its genes encoding key-elements of the translation apparatus, a trademark of cellular organisms. Besides homologs to the four aminoacyl-tRNA synthetases (aaRS) encoded by Mimivirus, Megavirus added three additional ones, raising the total of known virus-encoded aaRS to seven: IleRS, TrpRS, AsnRS, ArgRS, CysRS, MetRS, TyrRS. This finding strongly suggests that large DNA viruses derived from an ancestral cellular genome by reductive evolution. The nature of this cellular ancestor remains hotly debated.

Keywords: Girus; Megaviridae; Short read sequencing; Tree of Life.

Figures

Figure 1.
Figure 1.
Effect of sequence correction on read coverage. Visualization of read coverage (blue histogram) resulting from the mapping of Illumina high-throughput sequences at the same genomic locus, prior (A) and following (B) sequence correction. In this example, the deletion of an adenine in an 8-fold A-homopolymer resulted in an increase of coverage where it initially formed a steep drop, and a lengthening of the overlapping ORF (red arrows).
Figure 2.
Figure 2.
Two reliable phylogenetic reconstructions positionning the Megavirus in a partial Tree of Life. As the quality of the multiple alignment is essential to the reliability of the derived phylogeny, we only included the most similar proteins sequences of each clade in the analyses. (A) Positionning of the three closest Megavirus relatives using the largest clamp loader subunits. The multiple alignment (default options) and tree reconstruction (neighbor joining on 312 ungapped position, JTT substitution model) was performed using the on the MAFFT server (mafft.cbrc.jp/alignment/server/). The highly divergent bacterial homologs were not included, to preserve the quality of the multiple alignment. The deepest bootstrap values indicate the total lack of affinity of the Megaviridae sequences with both the archaeal and eukaryotic domains. (B) Positionning of the three closest Megavirus relatives using their largest ribonucleoside diphosphate reductase subunits. The multiple alignment (default options) and tree reconstruction (neighbor joining on 735 ungapped position, JTT substitution model) was performed as above. This time, the highly divergent archaeal homologs were not included, to preserve the quality of the multiple alignment. The deepest bootstrap values indicate a total lack of affinity of the Megaviridae with the bacterial and eukaryotic domains. In contrast, the acquisition of the vertebrate gene by the chordopoxviruses is showing very clearly, serving as an internal control that virus genes acquired by lateral transfer are indeed detectable. Amoebozoa sequences are indicated in A) and B) to emphasize that the Megavirus/Mimivirus genes do not cluster with their host’s homologs.

Comment on

  • Arslan D, Legendre M, Seltzer V, Abergel C, Claverie JM. Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proc Natl Acad Sci USA. 2011;108:17486–91. doi: 10.1073/pnas.1110889108.

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