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Archaeology of Eukaryotic DNA Replication Downloaded from http://cshperspectives.cshlp.org/ on September 27, 2021 - Published by Cold Spring Harbor Laboratory Press Archaeology of Eukaryotic DNA Replication Kira S. Makarova and Eugene V. Koonin National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland 20894 Correspondence: [email protected] Recent advances in the characterization of the archaeal DNA replication system together with comparative genomic analysis have led to the identification of several previously un- characterized archaeal proteins involved in replication and currently reveal a nearly com- plete correspondence between the components of the archaeal and eukaryotic replication machineries. It can be inferred that the archaeal ancestor of eukaryotes and even the last common ancestor of all extant archaea possessed replication machineries that were compa- rable in complexity to the eukaryotic replication system. The eukaryotic replication system encompasses multiple paralogs of ancestral components such that heteromeric complexes in eukaryotes replace archaeal homomeric complexes, apparently along with subfunctionali- zation of the eukaryotic complex subunits. In the archaea, parallel, lineage-specific dupli- cations of many genes encoding replication machinery components are detectable as well; most of these archaeal paralogs remain to be functionally characterized. The archaeal rep- lication system shows remarkable plasticity whereby even some essential components such as DNA polymerase and single-stranded DNA-binding protein are displaced by unrelated proteins with analogous activities in some lineages. ouble-stranded DNA is the molecule that Okazaki fragments (Kornberg and Baker 2005; Dcarries genetic information in all cellular Barry and Bell 2006; Hamdan and Richardson life-forms; thus, replication of this genetic ma- 2009; Hamdan and van Oijen 2010). Thus, it terial is a fundamental physiological process was a major surprise when it became clear that that requires high accuracy and efficiency the protein machineries responsible for this (Kornberg and Baker 2005). The general mech- complex process are drastically different, espe- anism and principles of DNA replication are cially in bacteria compared with archaea and common in all three domains of life—archaea, eukarya. The core components of the bacterial bacteria, and eukaryotes—and include recog- replication systems, such as DNA polymerase, nition of defined origins, melting DNA with primase, and replication helicase, are unrelated the aid of dedicated helicases, RNA priming or only distantly related to their counterparts in by the dedicated primase, recruitment of DNA the archaeal/eukaryotic replication apparatus polymerases and processivity factors, replica- (Edgell 1997; Leipe et al. 1999). tion fork formation, and simultaneous replica- The existence of two distinct molecular tion of leading and lagging strands, the latter via machines for genome replication has raised Editors: Stephen D. Bell, Marcel Me´chali, and Melvin L. DePamphilis Additional Perspectives on DNA Replication available at www.cshperspectives.org Copyright # 2013 Cold Spring Harbor Laboratory Press; all rights reserved. Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a012963 1 Downloaded from http://cshperspectives.cshlp.org/ on September 27, 2021 - Published by Cold Spring Harbor Laboratory Press K.S. Makarova and E.V. Koonin obvious questions on the nature of the replica- Krupovic et al. 2010). Replicon fusion also is a tion system in the last universal common ances- plausible path from a single origin of replication tor (LUCA) of all extant cellular life-forms, and that is typical of bacteria to multiple origins three groups of hypotheses have been proposed present in archaea and eukaryotes. However, (Leipe et al. 1999; Forterre 2002; Koonin 2005, all the evidence in support of frequent replicon 2006, 2009; Glansdorff 2008; McGeoch and Bell fusion and the plausibility of replicon takeover 2008): (1) The replication systems in Bacte- notwithstanding, there is no evidence of dis- ria and in the archaeo–eukaryotic lineage placement of the bacterial replication apparatus originated independently from an RNA-ge- with the archaeal version introduced by mobile nome LUCA or from a noncellular ancestral elements, or vice versa, displacement of the ar- state that encompassed a mix of genetic ele- chaeal machinery with the bacterial version, de- ments with diverse replication strategies and spite the rapid accumulation of diverse bacterial molecular machineries. (2) The LUCA was a and archaeal genome sequences. Thus, the dis- typical cellular life-form that possessed either placement scenarios of DNA replication ma- the archaeal or the bacterial replication appara- chinery evolution are so far not supported by tus in which several key components have been comparative genomic data. replaced in the other major cellular lineage. (3) Regardless of the nature of the DNA replica- The LUCAwas a complex cellular life-form that tion system (if any) in the LUCA and the under- possessed both replication systems, so that the lying causes of the archaeo–bacterial dichotomy differentiation of the bacterial and the ar- of replication machineries, the similarity be- chaeo–eukaryotic replication machineries oc- tween the archaeal and eukaryotic replication curred as a result of genome streamlining in systems is striking (Table 1). Generally, the ar- both lines of descent that was accompanied by chaeal replication protein core appears to be differential loss of components. With regard to the same as the eukaryotic core, but eukaryotes the possible substitution of replication systems, typically possess multiple paralogous subunits a plausible mechanism could be replicon take- within complexes that are homomeric in ar- over (Forterre 2006; McGeoch and Bell 2008). chaea, many additional components interacting Under the replicon takeover hypothesis, mobile with the core ones and more complex regulation elements introduce into cells a new replication (Leipe et al. 1999; Bell and Dutta 2002; Bohlke system or its components, which can displace et al. 2002; Kelman and White 2005; Barry and the original replication system through one or Bell 2006). Thus, the archaeal replication system several instances of integration of the given ele- appears to be an ancestral version of the eukary- ment into the host genome accompanied by in- otic system and hence a good model for func- activation of the host replication genes and/or tional and structural studies aimed at gaining origins of replication. This scenario is compat- mechanistic insights into eukaryotic replication. ible with the experimental results showing that In the last few years, there has been substan- DNA replication DNA in Escherichia coli with tial progress in the study of the archaeal replica- an inactivated DnaAgene or origin of replica- tion systems that has led to an apparently com- tion can be rescued by the replication appara- plete delineation of all proteins that are essential tus of R1 or F1 plasmids integrated into the for replication (Berquist et al. 2007; Beattie and bacterial chromosome (Bernander et al. 1991; Bell 2011a; MacNeill 2011). The combination of Koppes 1992). Furthermore, genome analysis experimental, structural, and bioinformatics suggests frequent replicon fusion in archaea studies has led to the discovery of archaeal ho- and bacteria (McGeoch and Bell 2008); in par- mologs (orthologs) for several components of ticular, such events are implied by the observa- the replication system that have been previously tion that in archaeal genomes, genes encoding deemed specific for eukaryotes (Barry and multiple paralogs of the replication helicase Bell 2006; MacNeill 2010, 2011; Makarova MCM and origins of replication are associated et al. 2012). Furthermore, complex evolutionary with mobile elements (Robinson and Bell 2007; events that involve multiple lineage-specific 2 Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a012963 Downloaded from http://cshperspectives.cshlp.org/ on September 27, 2021 - Published by Cold Spring Harbor Laboratory Press Evolution of DNA Replication Table 1. The relationship between archaeal and eukaryotic replication systems Archaea Eukaryotes (projection for LACA) (projection for LECA) Comments ORC complex arORC1 Orc1, Cdc6 In LACA the ORC/Cdc6 complex probably arORC2 Orc2, Orc3, Orc4, Orc5 consisted of two distinct subunits, and in TFIIB or homologa Orc6 LECA of six distinct. WhiP or other Cdt1 Both complexes might possess additional Orc6 wHTH proteina and Cdt1 components. CMG complex Archaeal Cdc45/RecJ Cdc45 In many archaea and eukaryotes, CDC45/RecJ Mcm Mcm2, Mcm3, Mcm4, apparently contain inactive DHH Mcm5, Mcm6, Mcm7 phosphoesterase domains. Gins23 Gins2, Gins3 The RecJ family is triplicated in euryarchaea, Gins15 Gins1, Gins5 and some of the paralogs could be involved in Inactivated MCM Mcm10 repair. homologa MCM is independently duplicated in several lineages of euryarchaea. CMG activation factors — RecQ/Sld2 There is no evidence that kinases and — Treslin/Sld3 phosphatases in archaea are directly involved — TopBP1/Dpb11 in replication, although they probably STK CDK, DDK regulate cell division. PP2C PP2C Primases Prim1/p48 PriS In eukaryotes, Pol a is involved in priming by Prim2a/p58 PriL adding short DNA fragments to RNA DnaG — primers. In archaea, DnaG might be involved
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