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:	Makarova, Kira S., Krupovic, Mart, Koonin, Eugene V.
Format:	Online
Language:	English
Published:	Frontiers Media S.A. 2014
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4104785/

id	pubmed-4104785
recordtype	oai_dc
spelling	pubmed-41047852014-08-06 Evolution of replicative DNA polymerases in archaea and their contributions to the eukaryotic replication machinery Makarova, Kira S. Krupovic, Mart Koonin, Eugene V. Microbiology 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 family D archaeal polymerases. Frontiers Media S.A. 2014-07-21 /pmc/articles/PMC4104785/ /pubmed/25101062 http://dx.doi.org/10.3389/fmicb.2014.00354 Text en Copyright © 2014 Makarova, Krupovic and Koonin. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Makarova, Kira S. Krupovic, Mart Koonin, Eugene V.
spellingShingle	Makarova, Kira S. Krupovic, Mart Koonin, Eugene V. Evolution of replicative DNA polymerases in archaea and their contributions to the eukaryotic replication machinery
author_facet	Makarova, Kira S. Krupovic, Mart Koonin, Eugene V.
author_sort	Makarova, Kira S.
title	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_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_sort	evolution of replicative dna polymerases in archaea and their contributions to the eukaryotic replication machinery
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 family D archaeal polymerases.
publisher	Frontiers Media S.A.
publishDate	2014
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4104785/
_version_	1613116028743581696

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

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