Evolution of replicative DNA polymerases in archaea and their contributions to the eukaryotic replication machinery

The elaborate eukaryotic DNA replication machinery evolved from the archaeal ancestors that themselves show considerable complexity. Here we discuss the comparative genomic and phylogenetic analysis of the core replication enzymes, the DNA polymerases, in archaea and their relationships with the euk...

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Main Authors: Kira S Makarova, Mart eKrupovic, Eugene V. Koonin
Format: Article
Language:English
Published: Frontiers Media S.A. 2014-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fmicb.2014.00354/full
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author Kira S Makarova
Mart eKrupovic
Eugene V. Koonin
author_facet Kira S Makarova
Mart eKrupovic
Eugene V. Koonin
author_sort Kira S Makarova
collection DOAJ
description The elaborate eukaryotic DNA replication machinery evolved from the archaeal ancestors that themselves show considerable complexity. Here we discuss the comparative genomic and phylogenetic analysis of the core replication enzymes, the DNA polymerases, in archaea and their relationships with the eukaryotic polymerases. In archaea, there are three groups of family B DNA polymerases, historically known as PolB1, PolB2 and PolB3. All three groups appear to descend from the last common ancestors of the extant archaea but their subsequent evolutionary trajectories seem to have been widely different. Although PolB3 is present in all archaea, with the exception of Thaumarchaeota, and appears to be directly involved in lagging strand replication, the evolution of this gene does not follow the archaeal phylogeny, conceivably due to multiple horizontal transfers and/or dramatic differences in evolutionary rates. In contrast, PolB1 is missing in Euryarchaeota but otherwise seems to have evolved vertically. The third archaeal group of family B polymerases, PolB2, includes primarily proteins in which the catalytic centers of the polymerase and exonuclease domains are disrupted and accordingly the enzymes appear to be inactivated. The members of the PolB2 group are scattered across archaea and might be involved in repair or regulation of replication along with inactivated members of the RadA family ATPases and an additional, uncharacterized protein that are encoded within the same predicted operon. In addition to the family B polymerases, all archaea, with the exception of the Crenarchaeota, encode enzymes of a distinct family D the origin of which is unclear. We examine multiple considerations that appear compatible with the possibility that family D polymerases are highly derived homologs of family B. The eukaryotic DNA polymerases show a highly complex relationship with their archaeal ancestors including contributions of proteins and domains from both the family B and the fam
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spelling doaj.art-7285ed996f58459b83350a7b774468812022-12-21T18:47:20ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2014-07-01510.3389/fmicb.2014.00354103336Evolution of replicative DNA polymerases in archaea and their contributions to the eukaryotic replication machineryKira S Makarova0Mart eKrupovic1Eugene V. Koonin2National Center for Biotechnology Information, National Library of Medicine, National Institutes of HealthInstitut PasteurNational Center for Biotechnology Information, National Library of Medicine, National Institutes of HealthThe elaborate eukaryotic DNA replication machinery evolved from the archaeal ancestors that themselves show considerable complexity. Here we discuss the comparative genomic and phylogenetic analysis of the core replication enzymes, the DNA polymerases, in archaea and their relationships with the eukaryotic polymerases. In archaea, there are three groups of family B DNA polymerases, historically known as PolB1, PolB2 and PolB3. All three groups appear to descend from the last common ancestors of the extant archaea but their subsequent evolutionary trajectories seem to have been widely different. Although PolB3 is present in all archaea, with the exception of Thaumarchaeota, and appears to be directly involved in lagging strand replication, the evolution of this gene does not follow the archaeal phylogeny, conceivably due to multiple horizontal transfers and/or dramatic differences in evolutionary rates. In contrast, PolB1 is missing in Euryarchaeota but otherwise seems to have evolved vertically. The third archaeal group of family B polymerases, PolB2, includes primarily proteins in which the catalytic centers of the polymerase and exonuclease domains are disrupted and accordingly the enzymes appear to be inactivated. The members of the PolB2 group are scattered across archaea and might be involved in repair or regulation of replication along with inactivated members of the RadA family ATPases and an additional, uncharacterized protein that are encoded within the same predicted operon. In addition to the family B polymerases, all archaea, with the exception of the Crenarchaeota, encode enzymes of a distinct family D the origin of which is unclear. We examine multiple considerations that appear compatible with the possibility that family D polymerases are highly derived homologs of family B. The eukaryotic DNA polymerases show a highly complex relationship with their archaeal ancestors including contributions of proteins and domains from both the family B and the famhttp://journal.frontiersin.org/Journal/10.3389/fmicb.2014.00354/fullArchaeaDNA Replicationmobile genetic elementsDNA polymerasesenzyme inactivation
spellingShingle Kira S Makarova
Mart eKrupovic
Eugene V. Koonin
Evolution of replicative DNA polymerases in archaea and their contributions to the eukaryotic replication machinery
Frontiers in Microbiology
Archaea
DNA Replication
mobile genetic elements
DNA polymerases
enzyme inactivation
title Evolution of replicative DNA polymerases in archaea and their contributions to the eukaryotic replication machinery
title_full Evolution of replicative DNA polymerases in archaea and their contributions to the eukaryotic replication machinery
title_fullStr Evolution of replicative DNA polymerases in archaea and their contributions to the eukaryotic replication machinery
title_full_unstemmed Evolution of replicative DNA polymerases in archaea and their contributions to the eukaryotic replication machinery
title_short Evolution of replicative DNA polymerases in archaea and their contributions to the eukaryotic replication machinery
title_sort evolution of replicative dna polymerases in archaea and their contributions to the eukaryotic replication machinery
topic Archaea
DNA Replication
mobile genetic elements
DNA polymerases
enzyme inactivation
url http://journal.frontiersin.org/Journal/10.3389/fmicb.2014.00354/full
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