Primer-Independent DNA Synthesis by a Family B DNA Polymerase from Self-Replicating Mobile Genetic Elements

Summary: Family B DNA polymerases (PolBs) play a central role during replication of viral and cellular chromosomes. Here, we report the discovery of a third major group of PolBs, which we denote primer-independent PolB (piPolB), that might be a link between the previously known protein-primed and RN...

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Main Authors: Modesto Redrejo-Rodríguez, Carlos D. Ordóñez, Mónica Berjón-Otero, Juan Moreno-González, Cristian Aparicio-Maldonado, Patrick Forterre, Margarita Salas, Mart Krupovic
Format: Article
Language:English
Published: Elsevier 2017-11-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124717314869
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spelling doaj-41f495adcdde458ab33b5a430e23ff582020-11-25T01:40:28ZengElsevierCell Reports2211-12472017-11-0121615741587Primer-Independent DNA Synthesis by a Family B DNA Polymerase from Self-Replicating Mobile Genetic ElementsModesto Redrejo-Rodríguez0Carlos D. Ordóñez1Mónica Berjón-Otero2Juan Moreno-González3Cristian Aparicio-Maldonado4Patrick Forterre5Margarita Salas6Mart Krupovic7Centro de Biología Molecular “Severo Ochoa,” Consejo Superior de Investigaciones Científicas and Universidad Autónoma de Madrid, Universidad Autónoma, Cantoblanco, 28049 Madrid, Spain; Corresponding authorCentro de Biología Molecular “Severo Ochoa,” Consejo Superior de Investigaciones Científicas and Universidad Autónoma de Madrid, Universidad Autónoma, Cantoblanco, 28049 Madrid, SpainCentro de Biología Molecular “Severo Ochoa,” Consejo Superior de Investigaciones Científicas and Universidad Autónoma de Madrid, Universidad Autónoma, Cantoblanco, 28049 Madrid, SpainCentro de Biología Molecular “Severo Ochoa,” Consejo Superior de Investigaciones Científicas and Universidad Autónoma de Madrid, Universidad Autónoma, Cantoblanco, 28049 Madrid, SpainCentro de Biología Molecular “Severo Ochoa,” Consejo Superior de Investigaciones Científicas and Universidad Autónoma de Madrid, Universidad Autónoma, Cantoblanco, 28049 Madrid, SpainInstitut Pasteur, Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Paris, FranceCentro de Biología Molecular “Severo Ochoa,” Consejo Superior de Investigaciones Científicas and Universidad Autónoma de Madrid, Universidad Autónoma, Cantoblanco, 28049 Madrid, Spain; Corresponding authorInstitut Pasteur, Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Paris, France; Corresponding authorSummary: Family B DNA polymerases (PolBs) play a central role during replication of viral and cellular chromosomes. Here, we report the discovery of a third major group of PolBs, which we denote primer-independent PolB (piPolB), that might be a link between the previously known protein-primed and RNA/DNA-primed PolBs. PiPolBs are encoded by highly diverse mobile genetic elements, pipolins, integrated in the genomes of diverse bacteria and also present as circular plasmids in mitochondria. Biochemical characterization showed that piPolB displays efficient DNA polymerization activity that can use undamaged and damaged templates and is endowed with proofreading and strand displacement capacities. Remarkably, the protein is also capable of template-dependent de novo DNA synthesis, i.e., DNA-priming activity, thereby breaking the long-standing dogma that replicative DNA polymerases require a pre-existing primer for DNA synthesis. We suggest that piPolBs are involved in self-replication of pipolins and may also contribute to bacterial DNA damage tolerance. : Redrejo-Rodríguez et al. report and characterize a DNA polymerase group (piPolB) from the B family that can perform primer-independent DNA replication. PiPolBs are encoded by Pipolins, diverse self-replicating genetic elements that are widespread among bacterial phyla and in mitochondria. Keywords: DNA replication, translesion synthesis, primer-independent DNA synthesis, de novo DNA synthesis, family B DNA polymerase, self-replicating mobile element, DNA damagehttp://www.sciencedirect.com/science/article/pii/S2211124717314869
collection DOAJ
language English
format Article
sources DOAJ
author Modesto Redrejo-Rodríguez
Carlos D. Ordóñez
Mónica Berjón-Otero
Juan Moreno-González
Cristian Aparicio-Maldonado
Patrick Forterre
Margarita Salas
Mart Krupovic
spellingShingle Modesto Redrejo-Rodríguez
Carlos D. Ordóñez
Mónica Berjón-Otero
Juan Moreno-González
Cristian Aparicio-Maldonado
Patrick Forterre
Margarita Salas
Mart Krupovic
Primer-Independent DNA Synthesis by a Family B DNA Polymerase from Self-Replicating Mobile Genetic Elements
Cell Reports
author_facet Modesto Redrejo-Rodríguez
Carlos D. Ordóñez
Mónica Berjón-Otero
Juan Moreno-González
Cristian Aparicio-Maldonado
Patrick Forterre
Margarita Salas
Mart Krupovic
author_sort Modesto Redrejo-Rodríguez
title Primer-Independent DNA Synthesis by a Family B DNA Polymerase from Self-Replicating Mobile Genetic Elements
title_short Primer-Independent DNA Synthesis by a Family B DNA Polymerase from Self-Replicating Mobile Genetic Elements
title_full Primer-Independent DNA Synthesis by a Family B DNA Polymerase from Self-Replicating Mobile Genetic Elements
title_fullStr Primer-Independent DNA Synthesis by a Family B DNA Polymerase from Self-Replicating Mobile Genetic Elements
title_full_unstemmed Primer-Independent DNA Synthesis by a Family B DNA Polymerase from Self-Replicating Mobile Genetic Elements
title_sort primer-independent dna synthesis by a family b dna polymerase from self-replicating mobile genetic elements
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2017-11-01
description Summary: Family B DNA polymerases (PolBs) play a central role during replication of viral and cellular chromosomes. Here, we report the discovery of a third major group of PolBs, which we denote primer-independent PolB (piPolB), that might be a link between the previously known protein-primed and RNA/DNA-primed PolBs. PiPolBs are encoded by highly diverse mobile genetic elements, pipolins, integrated in the genomes of diverse bacteria and also present as circular plasmids in mitochondria. Biochemical characterization showed that piPolB displays efficient DNA polymerization activity that can use undamaged and damaged templates and is endowed with proofreading and strand displacement capacities. Remarkably, the protein is also capable of template-dependent de novo DNA synthesis, i.e., DNA-priming activity, thereby breaking the long-standing dogma that replicative DNA polymerases require a pre-existing primer for DNA synthesis. We suggest that piPolBs are involved in self-replication of pipolins and may also contribute to bacterial DNA damage tolerance. : Redrejo-Rodríguez et al. report and characterize a DNA polymerase group (piPolB) from the B family that can perform primer-independent DNA replication. PiPolBs are encoded by Pipolins, diverse self-replicating genetic elements that are widespread among bacterial phyla and in mitochondria. Keywords: DNA replication, translesion synthesis, primer-independent DNA synthesis, de novo DNA synthesis, family B DNA polymerase, self-replicating mobile element, DNA damage
url http://www.sciencedirect.com/science/article/pii/S2211124717314869
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