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. 2007 Sep;17(9):1353-61.
doi: 10.1101/gr.6358607. Epub 2007 Jul 25.

Unique genes in giant viruses: regular substitution pattern and anomalously short size

Hiroyuki Ogata  1 , Jean-Michel Claverie
Affiliations

Unique genes in giant viruses: regular substitution pattern and anomalously short size

Hiroyuki Ogata et al. Genome Res. 2007 Sep.

Abstract

Large DNA viruses, including giant mimivirus with a 1.2-Mb genome, exhibit numerous orphan genes possessing no database homologs or genes with homologs solely in close members of the same viral family. Due to their solitary nature, the functions and evolutionary origins of those genes remain obscure. We examined sequence features and evolutionary rates of viral family-specific genes in three nucleo-cytoplasmic large DNA virus (NCLDV) lineages. First, we showed that the proportion of family-specific genes does not correlate with sequence divergence rate. Second, position-dependent nucleotide statistics were similar between family-specific genes and the remaining genes in the genome. Third, we showed that the synonymous-to-nonsynonymous substitution ratios in those viruses are at levels comparable to those estimated for vertebrate proteomes. Thus, the vast majority of family-specific genes do not exhibit an accelerated evolutionary rate, and are thus likely to specify functional polypeptides. On the other hand, these family-specific proteins exhibit several distinct properties: (1) they are shorter, (2) they include a larger fraction of predicted transmembrane proteins, and (3) they are enriched in low-complexity sequences. These results suggest that family-specific genes do not correspond to recent horizontal gene transfer. We propose that their characteristic features are the consequences of the specific evolutionary forces shaping the viral gene repertoires in the context of their parasitic lifestyles.

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Figures

Figure 1.
Figure 1.
BLAST similarity search results for the predicted proteomes of NCLDVs. Species abbreviations are as follows: LDV, Lymphocystis disease virus; ASFV, African swine fever virus; MYX, Myxoma virus; VAR, Variola virus; IIV6, Invertebrate iridescent virus 6; MsE, Melanoplus sanguinipes entomopoxvirus; AmE, Amsacta moorei entomopoxvirus; EsV1, Ectocarpus siliculosus virus 1; CPV, Canarypox virus; PBCV-1, Paramecium bursaria Chlorella virus 1; EhV-86, Emiliania huxleyi virus 86; Mimivirus, Acanthamoeba polyphaga mimivirus.
Figure 2.
Figure 2.
Lack of correlation between the proportions of family-specific genes and Ka.
Figure 3.
Figure 3.
Average G+C compositions of WORFs (filled circles), NORFs (open circles), and intergenic sequences (crosses). For WORFs and NORFs, the G+C compositions at the first and second positions (1,2) and the third positions (3) are separately computed. Bars correspond to a standard deviation. For intergenic sequences, those ≥20 nt were analyzed.
Figure 4.
Figure 4.
Proteome-scale Ka/Ks for the three NCLDV lineages and several vertebrate pairs with complete genomes. For the NCLDVs, (N) and (W) denote those for NORFs and WORFs, respectively.
Figure 5.
Figure 5.
Comparisons of Ka/Ks values between NCLDV genes and vertebrate homologs.
Figure 6.
Figure 6.
Size distributions of NORFs (white) and WORFs (black) for PBCV-1, MYX, and VAR.
Figure 7.
Figure 7.
Homology search results for the simulated amino acid sequences that mimic the size distribution and low-complexity proportions of NORFs. Bars correspond to standard deviations obtained after 10 times simulations.
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