1932

Abstract

It is now well recognized that the information processing machineries of archaea are far more closely related to those of eukaryotes than to those of their prokaryotic cousins, the bacteria. Extensive studies have been performed on the structure and function of the archaeal DNA replication origins, the proteins that define them, and the macromolecular assemblies that drive DNA unwinding and nascent strand synthesis. The results from various archaeal organisms across the archaeal domain of life show surprising levels of diversity at many levels—ranging from cell cycle organization to chromosome ploidy to replication mode and nature of the replicative polymerases. In the following, we describe recent advances in the field, highlighting conserved features and lineage-specific innovations.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-020518-115443
2020-09-08
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/74/1/annurev-micro-020518-115443.html?itemId=/content/journals/10.1146/annurev-micro-020518-115443&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Ausiannikava D, Mitchell L, Marriott H, Smith V, Hawkins M et al. 2018. Evolution of genome architecture in archaea: spontaneous generation of a new chromosome in Haloferax volcanii. Mol. Biol. Evol 35:1855–68
    [Google Scholar]
  2. 2. 
    Baranovskiy AG, Zhang Y, Suwa Y, Gu J, Babayeva ND et al. 2016. Insight into the human DNA primase interaction with template-primer. J. Biol. Chem. 291:4793–802
    [Google Scholar]
  3. 3. 
    Bell SD. 2017. Initiation of DNA replication in the archaea. Adv. Exp. Med. Biol. 1042:99–115
    [Google Scholar]
  4. 4. 
    Bell SD. 2019. Initiating DNA replication: a matter of prime importance. Biochem. Soc. Trans. 47:351–56
    [Google Scholar]
  5. 5. 
    Bell SD, Botchan MR. 2013. The minichromosome maintenance replicative helicase. Cold Spring Harb. Perspect. Biol. 5:a012807
    [Google Scholar]
  6. 6. 
    Bell SP, Labib K. 2016. Chromosome duplication in Saccharomyces cerevisiae. Genetics 203:1027–67
    [Google Scholar]
  7. 7. 
    Bernander R, Poplawski A. 1997. Cell cycle characteristics of thermophilic archaea. J. Bacteriol. 179:4963–69
    [Google Scholar]
  8. 8. 
    Boudet J, Devillier JC, Wiegand T, Salmon L, Meier BH et al. 2019. A small helical bundle prepares primer synthesis by binding two nucleotides that enhance sequence-specific recognition of the DNA template. Cell 176:154–66.e13
    [Google Scholar]
  9. 9. 
    Braithwaite DK, Ito J. 1993. Compilation, alignment, and phylogenetic relationships of DNA polymerases. Nucleic Acids Res 21:787–802
    [Google Scholar]
  10. 10. 
    Burkhart BW, Cubonova L, Heider MR, Kelman Z, Reeve JN, Santangelo TJ 2017. The GAN exonuclease or the flap endonuclease Fen1 and RNase HII are necessary for viability of Thermococcus kodakarensis. J. Bacteriol 199:13e00141–17
    [Google Scholar]
  11. 11. 
    Cann IK, Komori K, Toh H, Kanai S, Ishino Y 1998. A heterodimeric DNA polymerase: evidence that members of Euryarchaeota possess a distinct DNA polymerase. PNAS 95:14250–55
    [Google Scholar]
  12. 12. 
    Douglas ME, Ali FA, Costa A, Diffley JFX 2018. The mechanism of eukaryotic CMG helicase activation. Nature 555:265–68
    [Google Scholar]
  13. 13. 
    Dueber EL, Corn JE, Bell SD, Berger JM 2007. Replication origin recognition and deformation by a heterodimeric archaeal Orc1 complex. Science 317:1210–13
    [Google Scholar]
  14. 14. 
    Gaudier M, Schuwirth BS, Westcott SL, Wigley DB 2007. Structural basis of DNA replication origin recognition by an ORC protein. Science 317:1213–16
    [Google Scholar]
  15. 15. 
    Gehring AM, Astling DP, Matsumi R, Burkhart BW, Kelman Z et al. 2017. Genome replication in Thermococcus kodakarensis independent of Cdc6 and an origin of replication. Front. Microbiol. 8:2084
    [Google Scholar]
  16. 16. 
    Georgescu R, Yuan Z, Bai L, Santos RDLA, Sun J et al. 2017. Structure of eukaryotic CMG helicase at a replication fork and implications to replisome architecture and origin initiation. PNAS 114:E697–706
    [Google Scholar]
  17. 17. 
    Gomez-Llorente Y, Fletcher RJ, Chen XS, Carazo JM, San Martin C 2005. Polymorphism and double hexamer structure in the archaeal minichromosome maintenance (MCM) helicase from Methanobacterium thermoautotrophicum. J. Biol. Chem 280:40909–15
    [Google Scholar]
  18. 18. 
    Hawkins M, Malla S, Blythe MJ, Nieduszynski CA, Allers T 2013. Accelerated growth in the absence of DNA replication origins. Nature 503:544–47
    [Google Scholar]
  19. 19. 
    Holzer S, Yan J, Kilkenny ML, Bell SD, Pellegrini L 2017. Primer synthesis by a eukaryotic-like archaeal primase is independent of its Fe-S cluster. Nat. Commun. 8:1718
    [Google Scholar]
  20. 20. 
    Ishino Y, Komori K, Cann IK, Koga Y 1998. A novel DNA polymerase family found in Archaea. J. Bacteriol. 180:2232–36
    [Google Scholar]
  21. 21. 
    Jozwiakowski SK, Borazjani Gholami F, Doherty AJ 2015. Archaeal replicative primases can perform translesion DNA synthesis. PNAS 112:E633–38
    [Google Scholar]
  22. 22. 
    Kazlauskas D, Sezonov G, Charpin N, Venclovas C, Forterre P, Krupovic M 2018. Novel families of archaeo-eukaryotic primases associated with mobile genetic elements of bacteria and archaea. J. Mol. Biol. 430:737–50
    [Google Scholar]
  23. 23. 
    Kilkenny ML, Longo MA, Perera RL, Pellegrini L 2013. Structures of human primase reveal design of nucleotide elongation site and mode of Pol α tethering. PNAS 110:15961–66
    [Google Scholar]
  24. 24. 
    Killelea T, Palud A, Akcha F, Lemor M, L'haridon S et al. 2019. The interplay at the replisome mitigates the impact of oxidative damage on the genetic integrity of hyperthermophilic Archaea. eLife 8:e45320
    [Google Scholar]
  25. 25. 
    Lang S, Huang L. 2015. The Sulfolobus solfataricus GINS complex stimulates DNA binding and processive DNA unwinding by minichromosome maintenance helicase. J. Bacteriol. 197:3409–20
    [Google Scholar]
  26. 26. 
    Li MJ, Yi GS, Yu F, Zhou H, Chen JN et al. 2017. The crystal structure of Pyrococcus furiosus RecJ implicates it as an ancestor of eukaryotic Cdc45. Nucleic Acids Res 45:12551–64
    [Google Scholar]
  27. 27. 
    Liu B, Ouyang S, Makarova KS, Xia Q, Zhu Y et al. 2015. A primase subunit essential for efficient primer synthesis by an archaeal eukaryotic-type primase. Nat. Commun. 6:7300
    [Google Scholar]
  28. 28. 
    Liu J, Smith CL, DeRyckere D, DeAngelis K, Martin GS, Berger JM 2000. Structure and function of Cdc6/Cdc18: implications for origin recognition and checkpoint control. Mol. Cell 6:637–48
    [Google Scholar]
  29. 29. 
    Lundgren M, Andersson A, Chen L, Nilsson P, Bernander R 2004. Three replication origins in Sulfolobus species: synchronous initiation of chromosome replication and asynchronous termination. PNAS 101:7046–51
    [Google Scholar]
  30. 30. 
    Makarova KS, Koonin EV. 2013. Archaeology of eukaryotic DNA replication. Cold Spring Harb. Perspect. Biol. 5:a012963
    [Google Scholar]
  31. 31. 
    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 7:539–45
    [Google Scholar]
  32. 32. 
    Martinez-Alvarez L, Deng L, Peng X 2017. Formation of a viral replication focus in Sulfolobus cells infected by the rudivirus Sulfolobus islandicus rod-shaped virus 2. J. Virol 91:e00486-17 Erratum. 2018 J. Virol 92:e01991–17
    [Google Scholar]
  33. 33. 
    Matsunaga F, Forterre P, Ishino Y, Myllykallio H 2001. In vivo interactions of archaeal Cdc6/Orc1 and minichromosome maintenance proteins with the replication origin. PNAS 98:11152–57
    [Google Scholar]
  34. 34. 
    Matsunaga F, Norais C, Forterre P, Myllykallio H 2003. Identification of short ‘eukaryotic’ Okazaki fragments synthesized from a prokaryotic replication origin. EMBO Rep 4:154–58
    [Google Scholar]
  35. 35. 
    McGeoch AT, Trakselis MA, Laskey RA, Bell SD 2005. Organization of the archaeal MCM complex on DNA and implications for the helicase mechanism. Nat. Struct. Mol. Biol. 12:756–62
    [Google Scholar]
  36. 36. 
    Miller JM, Enemark EJ. 2015. Archaeal MCM proteins as an analog for the eukaryotic Mcm2–7 helicase to reveal essential features of structure and function. Archaea 2015:305497
    [Google Scholar]
  37. 37. 
    Moreau MJ, McGeoch AT, Lowe AR, Itzhaki LS, Bell SD 2007. ATPase site architecture and helicase mechanism of an archaeal MCM. Mol. Cell 28:304–14
    [Google Scholar]
  38. 38. 
    Myllykallio H, Lopez P, Lopez-Garcia P, Heilig R, Saurin W et al. 2000. Bacterial mode of replication with eukaryotic-like machinery in a hyperthermophilic archaeon. Science 288:2212–15
    [Google Scholar]
  39. 39. 
    Nagata M, Ishino S, Yamagami T, Ogino H, Simons JR et al. 2017. The Cdc45/RecJ-like protein forms a complex with GINS and MCM, and is important for DNA replication in Thermococcus kodakarensis. Nucleic Acids Res 45:10693–705
    [Google Scholar]
  40. 40. 
    Nagata M, Ishino S, Yamagami T, Simons JR, Kanai T et al. 2017. Possible function of the second RecJ-like protein in stalled replication fork repair by interacting with Hef. Sci. Rep. 7:16949
    [Google Scholar]
  41. 41. 
    O'Donnell ME, Li H. 2018. The ring-shaped hexameric helicases that function at DNA replication forks. Nat. Struct. Mol. Biol. 25:122–30
    [Google Scholar]
  42. 42. 
    Ogino H, Ishino S, Kohda D, Ishino Y 2017. The RecJ2 protein in the thermophilic archaeon Thermoplasma acidophilum is a 3′-5′ exonuclease that associates with a DNA replication complex. J. Biol. Chem. 292:7921–31
    [Google Scholar]
  43. 43. 
    Oyama T, Ishino S, Fujino S, Ogino H, Shirai T et al. 2011. Architectures of archaeal GINS complexes, essential DNA replication initiation factors. BMC Biol 9:28
    [Google Scholar]
  44. 44. 
    Oyama T, Ishino S, Shirai T, Yamagami T, Nagata M et al. 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 44:9505–17
    [Google Scholar]
  45. 45. 
    Pelve EA, Lindas AC, Knoppel A, Mira A, Bernander R 2012. Four chromosome replication origins in the archaeon Pyrobaculum calidifontis.Mol. Microbiol 85:986–95
    [Google Scholar]
  46. 46. 
    Perera HM, Trakselis MA. 2019. Amidst multiple binding orientations on fork DNA, Saccharolobus MCM helicase proceeds N-first for unwinding. eLife 8:e46096
    [Google Scholar]
  47. 47. 
    Poplawski A, Bernander R. 1997. Nucleoid structure and distribution in thermophilic Archaea. J. Bacteriol. 179:7625–30
    [Google Scholar]
  48. 48. 
    Raia P, Carroni M, Henry E, Pehau-Arnaudet G, Brule S et al. 2019. Structure of the DP1-DP2 PolD complex bound with DNA and its implications for the evolutionary history of DNA and RNA polymerases. PLOS Biol 17:e3000122
    [Google Scholar]
  49. 49. 
    Robinson NP, Blood KA, McCallum SA, Edwards PA, Bell SD 2007. Sister chromatid junctions in the hyperthermophilic archaeon Sulfolobus solfataricus. EMBO J 26:816–24
    [Google Scholar]
  50. 50. 
    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 116:25–38
    [Google Scholar]
  51. 51. 
    Rothenberg E, Trakselis MA, Bell SD, Ha T 2007. MCM forked substrate specificity involves dynamic interaction with the 5′-tail. J. Biol. Chem. 282:34229–34
    [Google Scholar]
  52. 52. 
    Sakakibara N, Kelman LM, Kelman Z 2009. Unwinding the structure and function of the archaeal MCM helicase. Mol. Microbiol. 72:286–96
    [Google Scholar]
  53. 53. 
    Samson RY, Abeyrathne PD, Bell SD 2016. Mechanism of archaeal MCM helicase recruitment to DNA replication origins. Mol. Cell 61:287–96
    [Google Scholar]
  54. 54. 
    Samson RY, Xu Y, Gadelha C, Stone TA, Faqiri JN et al. 2013. Specificity and function of archaeal DNA replication initiator proteins. Cell Rep 3:485–96
    [Google Scholar]
  55. 55. 
    Sauguet L, Raia P, Henneke G, Delarue M 2016. Shared active site architecture between archaeal PolD and multi-subunit RNA polymerases revealed by X-ray crystallography. Nat. Commun. 7:12227
    [Google Scholar]
  56. 56. 
    Soppa J. 2011. Ploidy and gene conversion in Archaea. Biochem. Soc. Trans. 39:150–54
    [Google Scholar]
  57. 57. 
    Takemata N, Samson RY, Bell SD 2019. Physical and functional compartmentalization of archaeal chromosomes. Cell 179:165–79.e18
    [Google Scholar]
  58. 58. 
    Tiengwe C, Marques CA, McCulloch R 2014. Nuclear DNA replication initiation in kinetoplastid parasites: new insights into an ancient process. Trends Parasitol 30:27–36
    [Google Scholar]
  59. 59. 
    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. PNAS 113:13390–95
    [Google Scholar]
  60. 60. 
    Yan J, Beattie TR, Rojas AL, Schermerhorn K, Gristwood T et al. 2017. Identification and characterization of a heterotrimeric archaeal DNA polymerase holoenzyme. Nat. Commun. 8:15075
    [Google Scholar]
  61. 61. 
    Yan J, Holzer S, Pellegrini L, Bell SD 2018. An archaeal primase functions as a nanoscale caliper to define primer length. PNAS 115:6697–702
    [Google Scholar]
  62. 62. 
    Yang H, Wu Z, Liu J, Liu X, Wang L et al. 2015. Activation of a dormant replication origin is essential for Haloferax mediterranei lacking the primary origins. Nat. Commun. 6:8321
    [Google Scholar]
/content/journals/10.1146/annurev-micro-020518-115443
Loading
/content/journals/10.1146/annurev-micro-020518-115443
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error