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Structure of the DP1-DP2 PolD complex bound with DNA and its implications for the evolutionary history of DNA and RNA polymerases

Abstract : PolD is an archaeal replicative DNA polymerase (DNAP) made of a proofreading exonucle-ase subunit (DP1) and a larger polymerase catalytic subunit (DP2). Recently, we reported the individual crystal structures of the DP1 and DP2 catalytic cores, thereby revealing that PolD is an atypical DNAP that has all functional properties of a replicative DNAP but with the catalytic core of an RNA polymerase (RNAP). We now report the DNA-bound cryo-electron microscopy (cryo-EM) structure of the heterodimeric DP1-DP2 PolD complex from Pyro-coccus abyssi, revealing a unique DNA-binding site. Comparison of PolD and RNAPs extends their structural similarities and brings to light the minimal catalytic core shared by all cellular transcriptases. Finally, elucidating the structure of the PolD DP1-DP2 interface, which is conserved in all eukaryotic replicative DNAPs, clarifies their evolutionary relationships with PolD and sheds light on the domain acquisition and exchange mechanism that occurred during the evolution of the eukaryotic replisome. Author summary PolD is an unusual archaeal replicative DNA polymerase (DNAP) in that it has all the functional properties of a replicative DNAP but with a catalytic core reminiscent of an RNA polymerase (RNAP). We now describe the cryo-electron microscopy (cryo-EM) structure of a DNA-bound heterodimeric DP1-DP2 PolD complex from the archaeon Pyrococcus abyssi, revealing a unique DNA-binding site. Comparison of PolD with RNAPs extends their structural similarities and highlights the minimal catalytic core PLOS Biology | https://doi.org/10.1371/journal.pbio. Citation: Raia P, Carroni M, Henry E, Pehau-Arnaudet G, Brûlé S, Béguin P, et al. (2019) Structure of the DP1-DP2 PolD complex bound with DNA and its implications for the evolutionary history of DNA and RNA polymerases. PLoS Biol 17(1): e3000122. https://doi.
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Pierre Raia, Marta Carroni, Etienne Henry, Gérard Pehau-Arnaudet, Sébastien Brûlé, et al.. Structure of the DP1-DP2 PolD complex bound with DNA and its implications for the evolutionary history of DNA and RNA polymerases. PLoS Biology, Public Library of Science, 2019, 17 (1), pp.e3000122. ⟨10.1371/journal.pbio.3000122⟩. ⟨pasteur-02057758⟩

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