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Evolution of Eukaryotic DNA Polymerases via Interaction Between Cells and Large DNA Viruses

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Abstract

B-family DNA-directed DNA polymerases are DNA replication enzymes found in Eukaryota, Archaea, large DNA viruses, and in some, but not all, bacteria. Several polymerase domains are conserved among the B-family DNA polymerases from these organisms, suggesting that the B-family DNA polymerases evolved from a common ancestor. Eukaryotes retain at least three replicative B-family DNA polymerases, DNA polymerase α, δ, and ε, and one translesion B-family DNA polymerase, DNA polymerase ζ. Here, we present molecular evolutionary evidence that suggests DNA polymerase genes evolved through horizontal gene transfer between the viral and archaeal–eukaryotic lineages. Molecular phylogenetic analyses of the B-family DNA polymerases from nucleo-cytoplasmic large DNA viruses (NCLDVs), eukaryotes, and archaea suggest that different NCLDV lineages such as Poxviridae and Mimiviridae were involved in the evolution of different DNA polymerases (pol-α-, δ-, ε-, and ζ-like genes) in archaeal–eukaryotic cell lineages, putatively through horizontal gene transfer. These results support existing theories that link the evolution of NCLDVs and the origin of the eukaryotic nucleus.

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References

  • Bell PJL (2001) Viral eukaryogenesis: was the ancestor of the nucleus a complex DNA virus? J Mol Evol 53:251–256

    Article  CAS  PubMed  Google Scholar 

  • Bell PJL (2009) The viral eukaryogenesis hypothesis. Annu N Y Acad Sci 1178:91–105

    Article  CAS  Google Scholar 

  • Burgers PMJ (2009) Polymerase dynamics at the eukaryotic DNA replication fork. J Biol Chem 284:4041–4045

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cavalier-Smith T (2010) Origin of the cell nucleus, mitosis and sex: roles of intracellular coevolution. Biol Direct 5:7

    Article  PubMed Central  PubMed  Google Scholar 

  • Claverie JM (2006) Viruses take center stage in cellular evolution. Genome Biol 7:110

    Article  PubMed Central  PubMed  Google Scholar 

  • Claverie JM, Abergel C (2013) Open questions about giant viruses. Adv Virus Res 85:25–56

    Article  CAS  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Edgell DR, Malik S-B, Doolittle WF (1998) Evidence of independent gene duplications during the evolution of archaeal and eukaryotic family B DNA polymerases. Mol Biol Evol 15:1207–1217

    Article  CAS  PubMed  Google Scholar 

  • Filée J, Forterre P, Sen-Lin T, Laurent J (2002) Evolution of DNA polymerase families: evidence for multiple gene exchange between cellular and viral proteins. J Mol Evol 54:763–773

    Article  PubMed  Google Scholar 

  • Fuerst JA, Sagulenko E (2012) Keys to eukaryality: planctomycetes and ancestral evolution of cellular complexity. Front Microbiol 3:167

    Article  PubMed Central  PubMed  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  PubMed  Google Scholar 

  • Hübscher U, Maga G, Spadari S (2002) Eukaryotic DNA polymerases. Annu Rev Biochem 71:133–163

    Article  PubMed  Google Scholar 

  • Iyer LM, Aravind L, Koonin EV (2001) Common origin of four diverse families of large eukaryotic DNA viruses. J Virol 75:11720–11734

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Iyer LM, Balaji S, Koonin EV, Aravind L (2006) Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res 117:156–184

    Article  CAS  PubMed  Google Scholar 

  • Kuznetsov YG, Klose T, Rossmann M, McPherson A (2013) Morphogenesis of mimivirus and its viral factories: an atomic force microscopy study of infected cells. J Virol 87:11200–11213

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lartillot N, Philippe H (2004) A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol 21:1095–1109

    Article  CAS  PubMed  Google Scholar 

  • Lundin D, Poole AM, Sjöberg BM, Högbom M (2012) Use of structural phylogenetic networks for classification of the ferritin-like super family. J Biol Chem 287:20565–20575

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martin W (2005) Archaebacteria (Archaea) and the origin of the eukaryotic nucleus. Curr Opin Microbiol 8:630–637

    Article  CAS  PubMed  Google Scholar 

  • Monier A, Claverie JM, Ogata H (2008) Taxonomic distribution of large DNA viruses in the sea. Genome Biol 9:R106

    Article  PubMed Central  PubMed  Google Scholar 

  • Ogata H, Claverie JM (2007) Unique genes in giant viruses: regular substitution pattern and anomalously short size. Genome Res 17:1353–1361

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ogata H, Raoult D, Claverie JM (2005) A new example of viral intein in Mimivirus. Virol J 2:8

    Article  PubMed Central  PubMed  Google Scholar 

  • Philippe N et al (2013) Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341:281–286

    Article  CAS  PubMed  Google Scholar 

  • Raoult D et al (2004) The 1.2-megabase genome sequence of mimivirus. Science 306:1344–1350

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed Central  PubMed  Google Scholar 

  • Schramm B, Locker JK (2005) Cytoplasmic organization of POXvirus DNA replication. Traffic 6:839–846

    Article  CAS  PubMed  Google Scholar 

  • Tahirov TH, Makarova KS, Rogozin IB, Pavlov YI, Koonin EV (2009) Evolution of DNA polymerases: an inactivated polymerase-exonuclease module in Pol ε and a chimeric origin of eukaryotic polymerases from two classes of archaeal ancestors. Biol Direct 4:11

    Article  PubMed Central  PubMed  Google Scholar 

  • Takemura M (2001) Poxviruses and the origin of the eukaryotic nucleus. J Mol Evol 52:419–425

    CAS  PubMed  Google Scholar 

  • Takemura M (2002) Evolution and degeneration of eukaryotic DNA replication system. BioSystems 65:139–145

    Article  CAS  PubMed  Google Scholar 

  • Takemura M (2005) Evolutionary history of the retinoblastoma gene from archaea to eukarya. BioSystems 82:266–272

    Article  CAS  PubMed  Google Scholar 

  • Takemura M (2011) Function of DNA polymerase α in a replication fork and its putative roles in genomic stability and eukaryotic evolution. In: Kušić-Tišma (ed) Fundamental aspects of DNA replication, InTech-Open Access Publisher, p 187–204

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tolonen N et al (2001) Vaccinia virus DNA replication occurs in endoplasmic reticulum-enclosed cytoplasmic mini-nuclei. Mol Biol Cell 12:2031–2046

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Villarreal LP, DeFilippis VR (2000) A hypothesis for DNA viruses as the origin of eukaryotic replication proteins. J Virol 74:7079–7084

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang TSF (1991) Eukaryotic DNA polymerases. Annu Rev Biochem 60:513–552

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson M, McInerney JO, Hirt RP, Foster PG, Embley TM (2007) Of clades and clans: terms for phylogenetic relationships in unrooted trees. Trends Eco Evol 22:114–115

    Article  Google Scholar 

  • Williams TA, Foster PG, Cox CJ, Embley TM (2013) An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504:231–236

    Article  CAS  PubMed  Google Scholar 

  • Yamada T (2011) Giant viruses in the environment: their origins and evolution. Curr Opin Virol 1:58–62

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Akihiko Yamagishi of Tokyo University of Pharmacy and Life Sciences for his useful comments, and Yutaro Sato and Hiroki Kikuchi for their technical assistance. This work was supported by a Grant-in-Aid (KAKENHI) for Scientific Research (B) (Grant 25285251) from the Japan Society for the Promotion of Science (JSPS). Some of the computation time was provided by the SuperComputer System, Institute for Chemical Research, Kyoto University, and supported by JSPS KAKENHI (Grant 26430184).

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Correspondence to Masaharu Takemura.

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Takemura, M., Yokobori, Si. & Ogata, H. Evolution of Eukaryotic DNA Polymerases via Interaction Between Cells and Large DNA Viruses. J Mol Evol 81, 24–33 (2015). https://doi.org/10.1007/s00239-015-9690-z

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  • DOI: https://doi.org/10.1007/s00239-015-9690-z

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