Abstract
Organisms within the archaeal domain of life possess a simplified version of the eukaryotic DNA replication machinery. While some archaea possess a bacterial-like mode of DNA replication with single origins of replication per chromosome, the majority of species characterized to date possess chromosomes with multiple replication origins. Genetic, structural, and biochemical studies have revealed the nature of archaeal origin specification. Recent work has begun to shed light on the mechanisms of replication initiation in these organisms.
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References
Barry ER, Bell SD (2006) DNA replication in the archaea. Microbiol Mol Biol Rev 70(4):876–887. https://doi.org/10.1128/mmbr.00029-06
Bell SD (2012) Archaeal orc1/cdc6 proteins. Subcell Biochem 62:59–69. https://doi.org/10.1007/978-94-007-4572-8_4
Bell SP, Labib K (2016) Chromosome duplication in Saccharomyces cerevisiae. Genetics 203(3):1027–1067. https://doi.org/10.1534/genetics.115.186452
Bleichert F, Botchan MR, Berger JM (2017) Mechanisms for initiating cellular DNA replication. Science 355:eaah6317. https://doi.org/10.1126/science.aah6317
Bochman ML, Schwacha A (2009) The Mcm complex: unwinding the mechanism of a replicative helicase. Microbiol Mol Biol Rev 73(4):652–683. https://doi.org/10.1128/mmbr.00019-09
Breuert S, Allers T, Spohn G, Soppa J (2006) Regulated polyploidy in halophilic archaea. PLoS One 1(1):e92. https://doi.org/10.1371/journal.pone.0000092
Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6(3):245–252. https://doi.org/10.1038/nrmicro1852
Chen YJ, Yu XO, Kasiviswanathan R, Shin JH, Kelman Z, Egelman EH (2005) Structural polymorphism of Methanothermobacter thermautotrophicus MCM. J Mol Biol 346(2):389–394. https://doi.org/10.1016/j.jmb.2004.11.076
Costa A, Onesti S (2009) Structural biology of MCM helicases. Crit Rev Biochem Mol Biol 44(5):326–342. https://doi.org/10.1080/10409230903186012
Costa A, Ilves I, Tamberg N, Petojevic T, Nogales E, Botchan MR, Berger JM (2011) The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat Struct Mol Biol 18(4):471-U110. https://doi.org/10.1038/nsmb.2004
Dueber ELC, Corn JE, Bell SD, Berger JM (2007) Replication origin recognition and deformation by a heterodimeric archaeal Orc1 complex. Science 317(5842):1210–1213. https://doi.org/10.1126/science.1143690
Dueber EC, Costa A, Corn JE, Bell SD, Berger JM (2011) Molecular determinants of origin discrimination by Orc1 initiators in archaea. Nucleic Acids Res 39(9):3621–3631. https://doi.org/10.1093/nar/gkq1308
Duggin IG, McCallum SA, Bell SD (2008) Chromosome replication dynamics in the archaeon Sulfolobus acidocaldarius. Proc Natl Acad Sci U S A 105(43):16737–16742. https://doi.org/10.1073/pnas.0806414105
Edgell DR, Doolittle WF (1997) Archaea and the origin(s) of DNA replication proteins. Cell 89(7):995–998
Forterre P (2015) The universal tree of life: an update. Front Microbiol 6:717. https://doi.org/10.3389/fmicb.2015.00717
Frols S, Gordon PM, Panlilio MA, Duggin IG, Bell SD, Sensen CW, Schleper C (2007) Response of the hyperthermophilic archaeon Sulfolobus solfataricus to UV damage. J Bacteriol 189(23):8708–8718. https://doi.org/10.1128/JB.01016-07
Gaudier M, Schuwirth BS, Westcott SL, Wigley DB (2007) Structural basis of DNA replication origin recognition by an ORC protein. Science 317(5842):1213–1216. https://doi.org/10.1126/science.1143664
Gotz D, Paytubi S, Munro S, Lundgren M, Bernander R, White MF (2007) Responses of hyperthermophilic crenarchaea to UV irradiation. Genome Biol 8(10):R220. https://doi.org/10.1186/gb-2007-8-10-r220
Grainge I, Gaudier M, Schuwirth BS, Westcott SL, Sandall J, Atanassova N, Wigley DB (2006) Biochemical analysis of a DNA replication origin in the archaeon Aeropyrum pernix. J Mol Biol 363(2):355–369. https://doi.org/10.1016/jmb.2006.07.076
Guy L, Ettema TJ (2011) The archaeal ‘TACK’ superphylum and the origin of eukaryotes. Trends Microbiol 19(12):580–587. https://doi.org/10.1016/j.tim.2011.09.002
Hawkins M, Malla S, Blythe MJ, Nieduszynski CA, Allers T (2013) Accelerated growth in the absence of DNA replication origins. Nature 503(7477):544–547. https://doi.org/10.1038/nature12650
Hildenbrand C, Stock T, Lange C, Rother M, Soppa J (2011) Genome copy numbers and gene conversion in methanogenic archaea. J Bacteriol 193:734–743
Kelman LM, Kelman Z (2014) Archaeal DNA replication. Annu Rev Genet 48:71–97. https://doi.org/10.1146/annurev-genet-120213-092148
Labib K, Gambus A (2007) A key role for the GINS complex at DNA replication forks. Trends Cell Biol 17(6):271–278. https://doi.org/10.1016/j.tcb.2007.04.002
Lang S, Huang L (2015) The Sulfolobus solfataricus GINS complex stimulates DNA binding and processive DNA unwinding by minichromosome maintenance helicase. J Bacteriol 197(21):3409–3420. https://doi.org/10.1128/JB.00496-15
Li Z, Pan M, Santangelo TJ, Chemnitz W, Yuan W, Edwards JL, Hurwitz J, Reeve JN, Kelman Z (2011) A novel DNA nuclease is stimulated by association with the GINS complex. Nucleic Acids Res 39(14):6114–6123. https://doi.org/10.1093/nar/gkr181
Lundgren M, Andersson A, Chen LM, Nilsson P, Bernander R (2004) Three replication origins in Sulfolobus species: synchronous initiation of chromosome replication and asynchronous termination. Proc Natl Acad Sci U S A 101(18):7046–7051. https://doi.org/10.1073/pnas.0400656101
Lundgren M, Malandrin L, Eriksson S, Huber H, Bernander R (2008) Cell cycle characteristics of Crenarchaeota: unity among diversity. J Bacteriol 190(15):5362–5367. https://doi.org/10.1128/jb.00330-08
Maaty WS, Wiedenheft B, Tarlykov P, Schaff N, Heinemann J, Robison-Cox J, Valenzuela J, Dougherty A, Blum P, Lawrence CM, Douglas T, Young MJ, Bothner B (2009) Something old, something new, something borrowed; how the thermoacidophilic archaeon Sulfolobus solfataricus responds to oxidative stress. PLoS One 4(9):e6964. https://doi.org/10.1371/journal.pone.0006964
MacNeill SA (2010) Structure and function of the GINS complex, a key component of the eukaryotic replisome. Biochem J 425(3):489–500. https://doi.org/10.1042/BJ20091531
Makarova KS, Koonin EV, Kelman Z (2012) The CMG (CDC45/RecJ, MCM, GINS) complex is a conserved component of the DNA replication system in all archaea and eukaryotes. Biol Direct 7:7. https://doi.org/10.1186/1745-6150-7-7
Majernik AI, Chong JP (2008) A conserved mechanism for replication origin recognition and binding in archaea. Biochem J 409(2):511–518
Marinsek N, Barry ER, Makarova KS, Dionne I, Koonin EV, Bell SD (2006) GINS, a central nexus in the archaeal DNA replication fork. EMBO Rep 7(5):539–545. https://doi.org/10.1038/sj.embor.7400649
McGeoch AT, Bell SD (2008) Extra-chromosomal elements and the evolution of cellular DNA replication machineries. Nat Rev Mol Cell Biol 9(7):569–574. https://doi.org/10.1038/nrm2426
Michel B, Bernander R (2014) Chromosome replication origins: do we really need them? BioEssays 36(6):585–590. https://doi.org/10.1002/bies.201400003
Myllykallio H, Lopez P, Lopez-Garcia P, Heilig R, Saurin W, Zivanovic Y, Philippe H, Forterre P (2000) Bacterial mode of replication with eukaryotic-like machinery in a hyperthermophilic archaeon. Science 288(5474):2212–2215
Naor A, Lapierre P, Mevarech M, Papke RT, Gophna U (2012) Low species barriers in halophilic archaea and the formation of recombinant hybrids. Curr Biol 22(15):1444–1448. https://doi.org/10.1016/j.cub.2012.05.056
Norais C, Hawkins M, Hartman AL, Eisen JA, Myllykallio H, Allers T (2007) Genetic and physical mapping of DNA replication origins in Haloferax volcanii. PLoS Genet 3:729–743. https://doi.org/10.1371/journal.pgen.0030077
Oyama T, Ishino S, Fujino S, Ogino H, Shirai T, Mayanagi K, Saito M, Nagasawa N, Ishino Y, Morikawa K (2011) Architectures of archaeal GINS complexes, essential DNA replication initiation factors. BMC Biol 9:28. https://doi.org/10.1186/1741-7007-9-28
Oyama T, Ishino S, Shirai T, Yamagami T, Nagata M, Ogino H, Kusunoki M, Ishino Y (2016) Atomic structure of an archaeal GAN suggests its dual roles as an exonuclease in DNA repair and a CMG component in DNA replication. Nucleic Acids Res 44(19):9505–9517. https://doi.org/10.1093/nar/gkw789
Pape T, Meka H, Chen SX, Vicentini G, van Heel M, Onesti S (2003) Hexameric ring structure of the full-length archaeal MCM protein complex. EMBO Rep 4(11):1079–1083. https://doi.org/10.1038/sj.embor.7400010
Pelve EA, Lindas AC, Knoppel A, Mira A, Bernander R (2012) Four chromosome replication origins in the archaeon Pyrobaculum calidifontis. Mol Microbiol 85(5):986–995. https://doi.org/10.1111/j.1365-2958.2012.08155.x
Pelve EA, Martens-Habbena W, Stahl DA, Bernander R (2013) Mapping of active replication origins in vivo in thaum- and euryarchaeal replicons. Mol Microbiol 90(3):538–550. https://doi.org/10.1111/mmi.12382
Rivera MC, Lake JA (2004) The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431(7005):152–155. https://doi.org/10.1038/nature02848
Robinson NP, Bell SD (2007) Extrachromosomal element capture and the evolution of multiple replication origins in archaeal chromosomes. Proc Natl Acad Sci U S A 104(14):5806–5811. https://doi.org/10.1073/pnas.0700206104
Robinson NP, Dionne I, Lundgren M, Marsh VL, Bernander R, Bell SD (2004) Identification of two origins of replication in the single chromosome of the Archaeon Sulfolobus solfataricus. Cell 116(1):25–38
Robinson NP, Blood KA, McCallum SA, Edwards PAW, Bell SD (2007) Sister chromatid junctions in the hyperthermophilic archaeon Sulfolobus solfataricus. EMBO J 26(3):816–824. https://doi.org/10.1038/sj.emboj.7601529
Sakakibara N, Kelman LM, Kelman Z (2009) How is the archaeal MCM helicase assembled at the origin? Possible mechanisms. Biochem Soc Trans 37(Pt 1):7–11. https://doi.org/10.1042/BST0370007
Samel SA, Fernandez-Cid A, Sun J, Riera A, Tognetti S, Herrera MC, Li H, Speck C (2014) A unique DNA entry gate serves for regulated loading of the eukaryotic replicative helicase MCM2-7 onto DNA. Genes Dev 28(15):1653–1666. https://doi.org/10.1101/gad.242404.114
Samson RY, Bell SD (2014) Archaeal chromosome biology. J Mol Microbiol Biotechnol 24(5–6):420–427. https://doi.org/10.1159/000368854
Samson RY, Bell SD (2016) Archaeal DNA replication origins and recruitment of the MCM replicative helicase. Enzyme 39:169–190. https://doi.org/10.1016/bs.enz.2016.03.002
Samson RY, Xu Y, Gadelha C, Stone TA, Faqiri JN, Li D, Qin N, Pu F, Liang YX, She Q, Bell SD (2013) Specificity and function of archaeal DNA replication initiator proteins. Cell Rep 3(2):485–496. https://doi.org/10.1016/j.celrep.2013.01.002
Samson RY, Abeyrathne PD, Bell SD (2016) Mechanism of archaeal MCM helicase recruitment to DNA replication origins. Mol Cell 61(2):287–296. https://doi.org/10.1016/j.molcel.2015.12.005
Sanchez-Pulido L, Ponting CP (2011) Cdc45: the missing RecJ ortholog in eukaryotes? Bioinformatics 27(14):1885–1888. https://doi.org/10.1093/bioinformatics/btr332
Sherratt DJ (2003) Bacterial chromosome dynamics. Science 301(5634):780–785
Siddiqui K, On KF, Diffley JF (2013) Regulating DNA replication in eukarya. Cold Spring Harb Perspect Biol 5(9):a010371. https://doi.org/10.1101/cshperspect.a012930
Simon AC, Sannino V, Costanzo V, Pellegrini L (2016) Structure of human Cdc45 and implications for CMG helicase function. Nat Commun 7:11638. https://doi.org/10.1038/ncomms11638
Slaymaker IM, Fu Y, Toso DB, Ranatunga N, Brewster A, Forsburg SL, Zhou ZH, Chen XS (2013) Mini-chromosome maintenance complexes form a filament to remodel DNA structure and topology. Nucleic Acids Res 41(5):3446–3456. https://doi.org/10.1093/nar/gkt022
Tanaka S, Araki H (2013) Helicase activation and establishment of replication forks at chromosomal origins of replication. Cold Spring Harb Perspect Biol 5(12):a010371. https://doi.org/10.1101/cshperspect.a010371
Tiengwe C, Marcello L, Farr H, Gadelha C, Burchmore R, Barry JD, Bell SD, McCulloch R (2012) Identification of ORC1/CDC6-interacting factors in Trypanosoma brucei reveals critical features of origin recognition complex architecture. PLoS One 7(3):e32674. https://doi.org/10.1371/journal.pone.0032674
Williams TA, Foster PG, Cox CJ, Embley TM (2013) An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504(7479):231–236. https://doi.org/10.1038/nature12779
Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A 74(11):5088–5090
Xu Y, Gristwood T, Hodgson B, Trinidad JC, Albers SV, Bell SD (2016) Archaeal orthologs of Cdc45 and GINS form a stable complex that stimulates the helicase activity of MCM. Proc Natl Acad Sci U S A 113(47):13390–13395. https://doi.org/10.1073/pnas.1613825113
Yang H, Wu Z, Liu J, Liu X, Wang L, Cai S, Xiang H (2015) Activation of a dormant replication origin is essential for Haloferax mediterranei lacking the primary origins. Nat Commun 6:8321. https://doi.org/10.1038/ncomms9321
Yao NY, O’Donnell ME (2016) Evolution of replication machines. Crit Rev Biochem Mol Biol 51(3):135–149. https://doi.org/10.3109/10409238.2015.1125845
Yardimci H, Walter JC (2014) Prereplication-complex formation: a molecular double take? Nat Struct Mol Biol 21(1):20–25. https://doi.org/10.1038/nsmb.2738
Yoshimochi T, Fujikane R, Kawanami M, Matsunaga F, Ishino Y (2008) The GINS complex from Pyrococcus furiosus stimulates the MCM helicase activity. J Biol Chem 283(3):1601–1609. https://doi.org/10.1074/jbc.M707654200
Zerulla K, Soppa J (2014) Polyploidy in haloarchaea: advantages for growth and survival. Front Microbiol 5:274. https://doi.org/10.3389/fmicb.2014.00274
Zerulla K, Chimileski S, Nather D, Gophna U, Papke RT, Soppa J (2014) DNA as a phosphate storage polymer and the alternative advantages of polyploidy for growth or survival. PLoS One 9(4):e94819. https://doi.org/10.1371/journal.pone.0094819
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I would like to thank Rachel Samson for helpful discussions of this material.
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Bell, S.D. (2017). Initiation of DNA Replication in the Archaea. In: Masai, H., Foiani, M. (eds) DNA Replication. Advances in Experimental Medicine and Biology, vol 1042. Springer, Singapore. https://doi.org/10.1007/978-981-10-6955-0_5
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