The logic of DNA replication in double-stranded DNA viruses: insights from global analysis of viral genomes - PubMed (original) (raw)

. 2016 Jun 2;44(10):4551-64.

doi: 10.1093/nar/gkw322. Epub 2016 Apr 25.

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The logic of DNA replication in double-stranded DNA viruses: insights from global analysis of viral genomes

Darius Kazlauskas et al. Nucleic Acids Res. 2016.

Abstract

Genomic DNA replication is a complex process that involves multiple proteins. Cellular DNA replication systems are broadly classified into only two types, bacterial and archaeo-eukaryotic. In contrast, double-stranded (ds) DNA viruses feature a much broader diversity of DNA replication machineries. Viruses differ greatly in both completeness and composition of their sets of DNA replication proteins. In this study, we explored whether there are common patterns underlying this extreme diversity. We identified and analyzed all major functional groups of DNA replication proteins in all available proteomes of dsDNA viruses. Our results show that some proteins are common to viruses infecting all domains of life and likely represent components of the ancestral core set. These include B-family polymerases, SF3 helicases, archaeo-eukaryotic primases, clamps and clamp loaders of the archaeo-eukaryotic type, RNase H and ATP-dependent DNA ligases. We also discovered a clear correlation between genome size and self-sufficiency of viral DNA replication, the unanticipated dominance of replicative helicases and pervasive functional associations among certain groups of DNA replication proteins. Altogether, our results provide a comprehensive view on the diversity and evolution of replication systems in the DNA virome and uncover fundamental principles underlying the orchestration of viral DNA replication.

© The Author(s) 2016. Published by Oxford University Press on behalf of Nucleic Acids Research.

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Figures

Figure 1.

Figure 1.

Quantitative distribution of DNA replication protein families and the taxonomy of virus host. The length of the bar is proportional to the number of protein family members found in the representative set of dsDNA viruses. Asterisk (*) denotes herpes processivity factors that include UL42, UL44 and BMRF1 homologs.

Figure 2.

Figure 2.

Diversity of replicative helicases domain organizations in dsDNA viruses. The number of representative sequences having specific domain organization is indicated on the left. The catalytic domain of the helicase is shown in green; primase, orange; polymerase, red; other domains, gray. αHD, α-helical domain; DUF, domain of unknown function; WH, winged-helix-turn-helix domain; ZnBD, Zn-binding domain; DBD, DNA-binding domain; Pol, DNA polymerase.

Figure 3.

Figure 3.

Replication proteins arranged by their overall observed frequencies (%) in genomes of dsDNA viruses.

Figure 4.

Figure 4.

Maximum likelihood phylogenetic analysis of family B DNA polymerases from archaea, bacteria, eukaryotes and their respective viruses. Numbers at the branch points represent non-parametric bootstrap support (1000 replicates). Branches are color-coded and the color key is provided at the bottom right corner of the figure. Alpha, Delta, Epsilon and Zeta represent subclasses of eukaryotic PolBs. ‘N’ indicates that only the catalytic N-terminal domain of the PolB-Epsilon was considered. The scale bar represents the number of substitutions per site.

Figure 5.

Figure 5.

Relationship between the observed frequencies of viral DNA replication proteins and the genome size of dsDNA viruses.

Figure 6.

Figure 6.

Associations between DNA replication proteins based on their presence/absence in dsDNA virus genomes. An arrow pointing from the protein indicates the percent of cases when this protein is encoded together with the protein at the tip of the arrow.

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References

    1. Forterre P., Prangishvili D. The major role of viruses in cellular evolution: facts and hypotheses. Curr. Opin. Virol. 2013;3:558–565. - PubMed
    1. Koonin E.V., Dolja V.V. A virocentric perspective on the evolution of life. Curr. Opin. Virol. 2013;3:546–557. - PMC - PubMed
    1. Suttle C.A. Marine viruses–major players in the global ecosystem. Nat. Rev. Microbiol. 2007;5:801–812. - PubMed
    1. Leipe D.D., Aravind L., Koonin E.V. Did DNA replication evolve twice independently? Nucleic Acids Res. 1999;27:3389–3401. - PMC - PubMed
    1. Kornberg A., Baker T.A. Dna Replication. Sausalito: University ScienceBooks; 2005.

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