title: Evolution of replicative DNA polymerases in archaea and their contributions to the eukaryotic replication machinery.
abstract: 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.
authors.affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health Bethesda, MD, USA.
authors.forename: Kira S
authors.initials: KS
authors.lastname: Makarova
authors.affiliation: Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur Paris, France.
authors.forename: Mart
authors.initials: M
authors.lastname: Krupovic
authors.affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health Bethesda, MD, USA.
authors.forename: Eugene V
authors.initials: EV
authors.lastname: Koonin
keywords: DNA polymerases; DNA replication; archaea; enzyme inactivation; mobile genetic elements
references.citation: Trends Microbiol. 2007 Feb;15(2):70-7
references.pmid: 17207624
references.citation: Virology. 2007 Jul 20;364(1):237-43
references.pmid: 17412384
references.citation: J Virol. 2013 Mar;87(6):3248-60
references.pmid: 23283946
references.citation: FEBS Lett. 2010 Aug 4;584(15):3370-5
references.pmid: 20598295
references.citation: Annu Rev Microbiol. 2002;56:263-87
references.pmid: 12142479
references.citation: FEBS Lett. 2011 Feb 4;585(3):452-8
references.pmid: 21192935
references.citation: PLoS One. 2013;8(1):e49044
references.pmid: 23326305
references.citation: Biochem Soc Trans. 2009 Feb;37(Pt 1):108-13
references.pmid: 19143612
references.citation: Nucleic Acids Res. 2004 Apr 30;32(8):2430-40
references.pmid: 15121900
references.citation: Virology. 2006 Jun 20;350(1):228-39
references.pmid: 16530800
references.citation: RNA Biol. 2013 May;10(5):803-16
references.pmid: 23470522
references.citation: J Bacteriol. 2008 Mar;190(5):1730-42
references.pmid: 18156258
references.citation: Nucleic Acids Res. 1994 Apr 11;22(7):1125-7
references.pmid: 8165123
references.citation: Biol Direct. 2012 Dec 14;7:46
references.pmid: 23241446
references.citation: Proc Natl Acad Sci U S A. 1998 Nov 24;95(24):14250-5
references.pmid: 9826686
references.citation: Biochem Soc Trans. 2011 Jan;39(1):104-6
references.pmid: 21265755
references.citation: Nature. 2010 Jun 24;465(7301):1039-43
references.pmid: 20577207
references.citation: Cell Rep. 2013 Sep 12;4(5):938-44
references.pmid: 24012761
references.citation: J Mol Biol. 2005 Jul 1;350(1):53-64
references.pmid: 15922358
references.citation: Nucleic Acids Res. 1998 Aug 15;26(16):3746-52
references.pmid: 9685491
references.citation: Biochemistry. 2014 May 6;53(17):2793-803
references.pmid: 24716551
references.citation: Nature. 2013 Nov 28;503(7477):544-547
references.pmid: 24185008
references.citation: Cold Spring Harb Perspect Biol. 2013 Nov 01;5(11):a012963
references.pmid: 23881942
references.citation: Genome Biol Evol. 2014 Jan;6(1):192-212
references.pmid: 24398374
references.citation: EMBO J. 2009 Jul 8;28(13):1978-87
references.pmid: 19494830
references.citation: J Biol. 2009;8(6):59
references.pmid: 19594957
references.citation: Adv Protein Chem. 2005;71:401-40
references.pmid: 16230118
references.citation: Mol Microbiol. 2002 Apr;44(1):283-96
references.pmid: 11967086
references.citation: Biochem Soc Trans. 2013 Dec;41(6):1392-400
references.pmid: 24256226
references.citation: Nucleic Acids Res. 2005 Jul 15;33(12):3875-96
references.pmid: 16027112
references.citation: Biol Direct. 2013 Apr 22;8:9
references.pmid: 23607440
references.citation: Nucleic Acids Res. 2014 Apr;42(6):3707-19
references.pmid: 24445805
references.citation: DNA Repair (Amst). 2007 Dec 1;6(12):1709-25
references.pmid: 17631059
references.citation: Cold Spring Harb Perspect Biol. 2014 Apr 01;6(4):a016188
references.pmid: 24691961
references.citation: J Mol Biol. 2006 Mar 10;356(5):1093-106
references.pmid: 16412462
references.citation: Front Biosci (Landmark Ed). 2012 Jan 01;17:509-44
references.pmid: 22201758
references.citation: J Virol. 2014 Feb;88(4):2354-8
references.pmid: 24335300
references.citation: Biol Direct. 2008 Aug 06;3:32
references.pmid: 18684330
references.citation: Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3600-5
references.pmid: 10097083
references.citation: J Bacteriol. 2013 May;195(10):2322-8
references.pmid: 23504010
references.citation: Mol Biol Evol. 1998 Sep;15(9):1207-17
references.pmid: 9729885
references.citation: Biochem Soc Trans. 2013 Feb 1;41(1):332-8
references.pmid: 23356307
references.citation: Biochem Soc Trans. 2013 Feb 1;41(1):451-7
references.pmid: 23356327
references.citation: Curr Opin Virol. 2013 Oct;3(5):558-65
references.pmid: 23870799
references.citation: Nat Rev Microbiol. 2003 Nov;1(2):127-36
references.pmid: 15035042
references.citation: J Virol. 2012 May;86(9):5067-79
references.pmid: 22357279
references.citation: PLoS One. 2010 Mar 10;5(3):e9490
references.pmid: 20224823
references.citation: PLoS One. 2012;7(5):e36972
references.pmid: 22615861
references.citation: Biol Direct. 2009 Mar 18;4:11
references.pmid: 19296856
references.citation: J Biol Chem. 2001 Jul 20;276(29):27376-83
references.pmid: 11319225
references.citation: J Biol Chem. 2011 Sep 9;286(36):31180-93
references.pmid: 21784862
references.citation: J Biol Chem. 2001 Nov 23;276(47):43487-90
references.pmid: 11579108
references.citation: Trends Microbiol. 2011 Dec;19(12):580-7
references.pmid: 22018741
references.citation: Philos Trans R Soc Lond B Biol Sci. 2004 Jan 29;359(1441):17-23
references.pmid: 15065652
references.citation: Annu Rev Biochem. 2002;71:333-74
references.pmid: 12045100
references.citation: J Biol Chem. 1999 Oct 1;274(40):28751-61
references.pmid: 10497247
references.citation: Biochemistry. 2012 Mar 6;51(9):1996-2007
references.pmid: 22339170
references.citation: Biochemistry. 2014 May 6;53(17):2781-92
references.pmid: 24716527
references.citation: Mutat Res. 2013 Mar-Apr;743-744:97-110
references.pmid: 23195997
references.citation: Mutat Res. 2010 Mar 1;685(1-2):45-53
references.pmid: 19682465
references.citation: Trends Biochem Sci. 1998 Sep;23(9):324-8
references.pmid: 9787636
references.citation: Trends Cell Biol. 2008 Nov;18(11):521-7
references.pmid: 18824354
references.citation: BMC Biol. 2014 May 19;12:36
references.pmid: 24884953
references.citation: J Mol Evol. 2002 Jun;54(6):763-73
references.pmid: 12029358
references.citation: Nucleic Acids Res. 2002 Jan 1;30(1):383-4
references.pmid: 11752343
references.citation: Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
references.pmid: 15034147
references.citation: Mol Biol Evol. 2010 Dec;27(12):2716-32
references.pmid: 20581330