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  • Review Article
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The cell cycle of archaea

Nature Reviews Microbiology volume 11, pages 627–638 (2013)Cite this article

Subjects

Key Points

  • To date, species of the genus Sulfolobus have served as the main model organisms for investigations of the cell cycle in archaea.

  • Archaea have circular chromosomes with single or multiple replication origins. Replication is initiated in synchrony from all origins, whereas replication termination occurs asynchronously.

  • The archaeal replication machinery is entirely homologous to that of eukaryotes, with the exception of the DNA polymerase PolD.

  • Many archaea utilize a site-specific recombination system based on the tyrosine recombinase XerA to resolve chromosome dimers before genome segregation, similarly to the bacterial XerCD system.

  • A chromosome segregation machinery called SegAB has recently been identified in Sulfolobus spp., providing the first insights into archaeal genome segregation.

  • Euryarchaeotes use a bacterial-like FtsZ-based cell division mechanism, whereas crenarchaeotes and thaumarchaeotes use the newly discovered Cdv (cell division) machinery, which has homology to the eukaryotic ESCRT-III (endosomal sorting complex required for transport III) system.

  • Rod-shaped crenarchaeotes contain spiral-shaped intracellular cytoskeletal structures based on crenactin, a homologue of eukaryotic actin.

  • Although recent studies have greatly expanded our knowledge of the archaeal cell cycle, many of the mechanistic details and regulatory mechanisms involved remain to be elucidated.

Abstract

Growth and proliferation of all cell types require intricate regulation and coordination of chromosome replication, genome segregation, cell division and the systems that determine cell shape. Recent findings have provided insight into the cell cycle of archaea, including the multiple-origin mode of DNA replication, the initial characterization of a genome segregation machinery and the discovery of a novel cell division system. The first archaeal cytoskeletal protein, crenactin, was also recently described and shown to function in cell shape determination. Here, we outline the current understanding of the archaeal cell cycle and cytoskeleton, with an emphasis on species in the genus Sulfolobus, and consider the major outstanding questions in the field.

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Figure 1: The Sulfolobus spp. cell cycle.
Figure 2: The archaeal replisome.
Figure 3: Replication, recombination and resolution of circular chromosomes.
Figure 4: Genome segregation in bacteria and archaea.

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References

  1. Woese, C. R. & Fox, G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl Acad. Sci. USA 74, 5088–5090 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Pikuta, E. V., Hoover, R. B. & Tang, J. Microbial extremophiles at the limits of life. Crit. Rev. Microbiol. 33, 183–209 (2007).

    CAS  PubMed  Google Scholar 

  3. Robinson, C. E., Harris, J. K., Spear, J. R. & Pace, N. R. Phylogenetic diversity and ecology of environmental Archaea. Curr. Opin. Microbiol. 8, 638–642 (2005).

    Google Scholar 

  4. Woese, C. R., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA 87, 4576–4579 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Brochier-Armanet, C., Boussau, B., Gribaldo, S. & Forterre, P. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nature Rev. Microbiol. 6, 245–252 (2008).

    CAS  Google Scholar 

  6. Nunoura, T. et al. Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res. 39, 3204–3223 (2011).

    CAS  PubMed  Google Scholar 

  7. Kozubal, M. A. et al. Geoarchaeota: a new candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park. ISME J. 7, 622–634 (2013).

    CAS  PubMed  Google Scholar 

  8. Barns, S. M., Delwiche, C. F., Palmer, J. D. & Pace, N. R. Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences. Proc. Natl Acad. Sci. USA 93, 9188–9193 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Huber, H. et al. A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature 417, 63–67 (2002).

    CAS  PubMed  Google Scholar 

  10. Albers, S. V. & Meyer, B. H. The archaeal cell envelope. Nature Rev. Microbiol. 9, 414–426 (2011).

    CAS  Google Scholar 

  11. Olsen, G. J. & Woese, C. R. Archaeal genomics: an overview. Cell 89, 991–994 (1997).

    CAS  PubMed  Google Scholar 

  12. Bernander, R. Chromosome replication, nucleoid segregation and cell division in archaea. Trends Microbiol. 8, 278–283 (2000).

    CAS  PubMed  Google Scholar 

  13. Lindås, A.-C., Karlsson, E. A., Lindgren, M. T., Ettema, T. J. & Bernander, R. A unique cell division machinery in the Archaea. Proc. Natl Acad. Sci. USA 105, 18942–18946 (2008).

    PubMed  PubMed Central  Google Scholar 

  14. Samson, R. Y., Obita, T., Freund, S. M., Williams, R. L. & Bell, S. D. A role for the ESCRT system in cell division in archaea. Science 322, 1710–1713 (2008). Together with reference 13, this article describes the discovery of the Cdv cell division machinery in crenarchaeotes.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Ettema, T. J., Lindås, A.-C. & Bernander, R. An actin-based cytoskeleton in archaea. Mol. Microbiol. 80, 1052–1061 (2011). The discovery of the actin homologue crenactin, the first cytoskeletal structure described for archaea.

    CAS  PubMed  Google Scholar 

  16. Baumann, P. & Jackson, S. P. An archaebacterial homologue of the essential eubacterial cell division protein FtsZ. Proc. Natl Acad. Sci. USA 93, 6726–6730 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Margolin, W., Wang, R. & Kumar, M. Isolation of an ftsZ homolog from the archaebacterium Halobacterium salinarium: Implications for the evolution of FtsZ and tubulin. J. Bacteriol. 178, 1320–1327 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Wang, X. & Lutkenhaus, J. FtsZ ring: the eubacterial division apparatus conserved in archaebacteria. Mol. Microbiol. 21, 313–319 (1996). The first demonstration of an FtsZ-based division structure in archaea.

    CAS  PubMed  Google Scholar 

  19. Poplawski, A., Gullbrand, B. & Bernander, R. The ftsZ gene of Haloferax mediterranei: sequence, conserved gene order, and visualization of the FtsZ ring. Gene 242, 357–367 (2000).

    CAS  PubMed  Google Scholar 

  20. Tenorio-Salgado, S., Huerta-Saquero, A. & Perez-Rueda, E. New insights on gene regulation in archaea. Comput. Biol. Chem. 35, 341–346 (2011).

    CAS  PubMed  Google Scholar 

  21. Bernander, R. The cell cycle of Sulfolobus. Mol. Microbiol. 66, 557–562 (2007).

    CAS  PubMed  Google Scholar 

  22. Bernander, R. & Poplawski, A. Cell cycle characteristics of thermophilic archaea. J. Bacteriol. 179, 4963–4969 (1997). The first description of cell cycle organization in an archaeon.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Poplawski, A. & Bernander, R. Nucleoid structure and distribution in thermophilic Archaea. J. Bacteriol. 179, 7625–7630 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Hjort, K. & Bernander, R. Changes in cell size and DNA content in Sulfolobus cultures during dilution and temperature shift experiments. J. Bacteriol. 181, 5669–5675 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Lundgren, M., Malandrin, L., Eriksson, S., Huber, H. & Bernander, R. Cell cycle characteristics of Crenarchaeota: unity among diversity. J. Bacteriol. 190, 5362–5367 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Maisnier-Patin, S., Malandrin, L., Birkeland, N. K. & Bernander, R. Chromosome replication patterns in the hyperthermophilic euryarchaea Archaeoglobus fulgidus and Methanocaldococcus (Methanococcus) jannaschii. Mol. Microbiol. 45, 1443–1450 (2002).

    CAS  PubMed  Google Scholar 

  27. Pelve, E. A. et al. Cdv-based cell division and cell cycle organization in the thaumarchaeon Nitrosopumilus maritimus. Mol. Microbiol. 82, 555–566 (2011).

    CAS  PubMed  Google Scholar 

  28. Majernik, A. I., Lundgren, M., McDermott, P., Bernander, R. & Chong, J. P. DNA content and nucleoid distribution in Methanothermobacter thermautotrophicus. J. Bacteriol. 187, 1856–1858 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Breuert, S., Allers, T., Spohn, G. & Soppa, J. Regulated polyploidy in halophilic archaea. PLoS ONE 1, e92 (2006).

    PubMed  PubMed Central  Google Scholar 

  30. Malandrin, L., Huber, H. & Bernander, R. Nucleoid structure and partition in Methanococcus jannaschii: an archaeon with multiple copies of the chromosome. Genetics 152, 1315–1323 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Marie, D., Vaulot, D. & Partensky, F. Application of the novel nucleic acid dyes YOYO-1, YO-PRO-1, and PicoGreen for flow cytometric analysis of marine prokaryotes. Appl. Environ. Microbiol. 62, 1649–1655 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Robinson, N. P. et al. Identification of two origins of replication in the single chromosome of the archaeon Sulfolobus solfataricus. Cell 116, 25–38 (2004).

    CAS  PubMed  Google Scholar 

  33. Costa, A., Hood, I. V. & Berger, J. M. Mechanisms for initiating cellular DNA replication. Annu. Rev. Biochem. 82, 25–54 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Duderstadt, K. E. & Berger, J. M. A structural framework for replication origin opening by AAA+ initiation factors. Curr. Opin. Struct. Biol. 23, 1–10 (2012).

    Google Scholar 

  35. Dueber, E. C., Costa, A., Corn, J. E., Bell, S. D. & Berger, J. M. Molecular determinants of origin discrimination by Orc1 initiators in archaea. Nucl. Acids Res. 39, 3621–3631 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Grabowski, B. & Kelman, Z. Archeal DNA replication: eukaryal proteins in a bacterial context. Annu. Rev. Microbiol. 57, 487–516 (2003).

    CAS  PubMed  Google Scholar 

  37. Grainge, I. et al. Biochemical analysis of a DNA replication origin in the archaeon Aeropyrum pernix. J. Mol. Biol. 363, 355–369 (2006).

    CAS  PubMed  Google Scholar 

  38. Ishino, Y. & Ishino, S. Rapid progress of DNA replication studies in Archaea, the third domain of life. Sci. China Life Sci. 55, 386–403 (2012).

    CAS  PubMed  Google Scholar 

  39. Slaymaker, I. M. et al. Mini-chromosome maintenance complexes form a filament to remodel DNA structure and topology. Nucl. Acids Res. 41, 3446–3456 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Beattie, T. R. & Bell, S. D. Molecular machines in archaeal DNA replication. Curr. Opin. Chem. Biol. 15, 614–619 (2011).

    CAS  PubMed  Google Scholar 

  41. Cubonová, L. et al. Archaeal DNA polymerase D but not DNA polymerase B is required for genome replication in Thermococcus kodakarensis. J. Bacteriol. http://dx.doi.org/10.1128/JB.02037-12 (2013).

  42. Sarmiento, F., Mrázek, J. & Whitman, W. B. Genome-scale analysis of gene function in the hydrogenotrophic methanogenic archaeon Methanococcus maripaludis. Proc. Natl Acad. Sci. USA 110, 4726–4731 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Matsunaga, F., Norais, C., Forterre, P. & Myllykallio, H. Identification of short 'eukaryotic' Okazaki fragments synthesized from a prokaryotic replication origin. EMBO J. 4, 154–158 (2003). The demonstration that archaeal Okazaki fragments are similar in length to those of eukaryotes.

    CAS  Google Scholar 

  44. Spang, A. et al. Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol. 18, 331–340 (2010).

    CAS  PubMed  Google Scholar 

  45. Wadsworth, R. I. & White, M. F. Identification and properties of the crenarchaeal single-stranded DNA binding protein from Sulfolobus solfataricus. Nucleic Acids Res. 9, 914–920 (2001).

    Google Scholar 

  46. Lundgren, M., Andersson, A., Chen, L., Nilsson, P. & Bernander, R. Three replication origins in Sulfolobus species: synchronous initiation of chromosome replication and asynchronous termination. Proc. Natl Acad. Sci. USA 101, 7046–7051 (2004). Together with reference 32, this work revealed that there can be multiple replication origins in the chromosome of a prokaryote.

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Myllykallio, H. et al. Bacterial mode of replication with eukaryotic-like machinery in a hyperthermophilic archaeon. Science 288, 2212–2215 (2000). The initial description of a chromosome replication origin in an archaeon.

    CAS  PubMed  Google Scholar 

  48. Pelve, E. A., Lindås, A.-C., Knöppel, A., Mira, A. & Bernander, R. Four chromosome replication origins in the archaeon Pyrobaculum calidifontis. Mol. Microbiol. 85, 986–995 (2012).

    CAS  PubMed  Google Scholar 

  49. Reyes-Lamothe, R., Nicolas, E. & Sherratt, D. J. Chromosome replication and segregation in bacteria. Annu. Rev. Genet. 46, 121–143 (2012).

    CAS  PubMed  Google Scholar 

  50. Masai, H., Matsumoto, S., You, Z., Yoshizawa-Sugata, N. & Oda, M. Eukaryotic chromosome DNA replication: where, when, and how? Annu. Rev. Biochem. 79, 89–130 (2010).

    CAS  PubMed  Google Scholar 

  51. Robinson, N. P. & Bell, S. D. Extrachromosomal element capture and the evolution of multiple replication origins in archaeal chromosomes. Proc. Natl Acad. Sci. USA 104, 5806–5811 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. French, S. L. et al. Transcription and translation are coupled in archaea. Mol. Biol. Evol. 24, 893–895 (2007).

    CAS  PubMed  Google Scholar 

  53. Samson, R. Y. et al. Specificity and function of archaeal DNA replication initiator proteins. Cell Rep. 3, 485–496 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Norais, C. et al. Genetic and physical mapping of DNA replication origins in Haloferax volcanii. PLoS Genet. 3, e77 (2007).

    PubMed  PubMed Central  Google Scholar 

  55. Berquist, B. R. & DasSarma, S. An archaeal chromosomal autonomously replicating sequence element from an extreme halophile, Halobacterium sp. strain NRC-1. J. Bacteriol. 185, 5959–5966 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Andersson, A. F. et al. Replication-biased genome organisation in the crenarchaeon Sulfolobus. BMC Genomics 11, 454 (2010).

    PubMed  PubMed Central  Google Scholar 

  57. Lundgren, M. & Bernander, R. Genome-wide transcription map of an archaeal cell cycle. Proc. Natl Acad. Sci. USA 104, 2939–2944 (2007). The first genome-wide transcription map of cell cycle-specific gene expression in an archaeon.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Erzberger, J. P., Pirruccello, M. M. & Berger, J. M. The structure of bacterial DnaA: implications for general mechanisms underlying DNA replication initiation. EMBO J. 21, 4763–4773 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Gristwood, T., Duggin, I. G., Wagner, M., Albers, S. V. & Bell, S. D. The sub-cellular localization of Sulfolobus DNA replication. Nucleic Acids Res. 40, 5487–5496 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Cortez, D. et al. Evidence for a Xer/dif system for chromosome resolution in archaea. PLoS Genet. 6, e1001166 (2010).

    PubMed  PubMed Central  Google Scholar 

  61. Gerdes, K., Howard, M. & Szardenings, F. Pushing and pulling in prokaryotic DNA segregation. Cell 141, 927–942 (2010).

    CAS  PubMed  Google Scholar 

  62. Duggin, I. G., Dubarry, N. & Bell, S. D. Replication termination and chromosome dimer resolution in the archaeon Sulfolobus solfataricus. EMBO J. 30, 145–153 (2011).

    CAS  PubMed  Google Scholar 

  63. Serre, M.-C. et al. The carboxy-terminal αN helix of the archaeal XerA tyrosine recombinase is a molecular switch to control site-specific recombination. PLoS ONE 8, e63010 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Grainge, I., Lesterlin, C. & Sherratt, D. J. Activation of XerCD-dif recombination by the FtsK DNA translocase. Nucleic Acids Res. 39, 5140–5148 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Robinson, N. P., Blood, K. A., McCallum, S. A., Edwards, P. A. & Bell, S. D. Sister chromatid junctions in the hyperthermophilic archaeon Sulfolobus solfataricus. EMBO J. 26, 816–824 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Ebersbach, G. & Gerdes, K. Plasmid segregation mechanisms. Annu. Rev. Genet. 39, 453–479 (2005).

    CAS  PubMed  Google Scholar 

  67. Ptacin, J. L. et al. A spindle-like apparatus guides bacterial chromosome segregation. Nature Cell Biol. 12, 791–798 (2010).

    CAS  PubMed  Google Scholar 

  68. Lutkenhaus, J. Min oscillation in bacteria. Adv. Exp. Med. Biol. 641, 49–61 (2008).

    CAS  PubMed  Google Scholar 

  69. Sullivan, S. M. & Maddock, J. R. Bacterial sporulation: pole-to-pole protein oscillation. Curr. Biol. 10, R159–R161 (2000).

    CAS  PubMed  Google Scholar 

  70. Toro, E. & Shapiro, L. Bacterial chromosome organization and segregation. Cold Spring Harb. Perspect. Biol. 2, a000349 (2010).

    PubMed  PubMed Central  Google Scholar 

  71. Kalliomaa-Sanford, A. K. et al. Chromosome segregation in Archaea mediated by a hybrid DNA partition machine. Proc. Natl Acad. Sci. USA 109, 3754–3759 (2012). The initial characterization of the archaeal genome segregation system, SegAB.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. McIntosh, J. R., Molodtsov, M. I. & Ataullakhanov, F. I. Biophysics of mitosis. Q. Rev. Biophys. 45, 147–207 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Gérard, E., Labedan, B. & Forterre, P. Isolation of a minD-like gene in the hyperthermophilic archaeon Pyrococcus AL585, and phylogenetic characterization of related proteins in the three domains of life. Gene 222, 99–106 (1998).

    PubMed  Google Scholar 

  74. Carter, S. D. & Sjögren, C. The SMC complexes, DNA and chromosome topology: right or knot? Crit. Rev. Biochem. Mol. Biol. 47, 1–16 (2012).

    CAS  PubMed  Google Scholar 

  75. Long, S. W. & Faguy, D. M. Anucleate and titan cell phenotypes caused by insertional inactivation of the structural maintenance of chromosomes (smc) gene in the archaeon Methanococcus voltae. Mol. Microbiol. 52, 1567–1577 (2004).

    CAS  PubMed  Google Scholar 

  76. Herrmann, U. & Soppa, J. Cell cycle-dependent expression of an essential SMC-like protein and dynamic chromosome localization in the archaeon Halobacterium salinarum. Mol. Microbiol. 46, 395–409 (2002).

    CAS  PubMed  Google Scholar 

  77. Makarova, K. S., Yutin, N., Bell, S. D. & Koonin, E. V. Evolution of diverse cell division and vesicle formation systems in Archaea. Nature Rev. Microbiol. 8, 731–741 (2010).

    CAS  Google Scholar 

  78. Margolin, W. FtsZ and the division of prokaryotic cells and organelles. Nature Rev. Mol. Cell. Biol. 6, 862–871 (2005).

    CAS  Google Scholar 

  79. Wu, L. J. & Errington, J. Nucleoid occlusion and bacterial cell division. Nature Rev. Microbiol. 10, 8–12 (2011).

    Google Scholar 

  80. Lutkenhaus, J., Pichoff, S. & Du, S. Bacterial cytokinesis: from Z ring to divisome. Cytoskeleton 69, 778–790 (2012).

    CAS  PubMed  Google Scholar 

  81. Bernander, R. & Ettema, T. J. FtsZ-less cell division in archaea and bacteria. Curr. Opin. Microbiol. 13, 747–752 (2010).

    CAS  PubMed  Google Scholar 

  82. Cohen, G. N. et al. An integrated analysis of the genome of the hyperthermophilic archaeon Pyrococcus abyssi. Mol. Microbiol. 47, 1495–1512 (2003).

    CAS  PubMed  Google Scholar 

  83. Burns, D. G. et al. Haloquadratum walsbyi gen. nov., sp. nov., the square haloarchaeon of Walsby, isolated from saltern crystallizers in Australia and Spain. Int. J. Syst. Evol. Microbiol. 57, 387–392 (2007).

    CAS  PubMed  Google Scholar 

  84. Carlton, J. The ESCRT machinery: a cellular apparatus for sorting and scission. Biochem. Soc. Trans. 38, 1397–1412 (2010).

    CAS  PubMed  Google Scholar 

  85. Samson, R. Y. et al. Molecular and structural basis of ESCRT-III recruitment to membranes during archaeal cell division. Mol. Cell 41, 186–196 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Dobro, M. J. et al. Electron cryotomography of ESCRT assemblies and dividing Sulfolobus cells suggest spiraling filaments are involved in membrane scission. Mol. Biol. Cell http://dx.doi.org/10.1091/mbc.E12-11-0785 (2013).

  87. Moriscot, C. et al. Crenarchaeal CdvA forms double-helical filaments containing DNA and interacts with ESCRT-III-like CdvB. PLoS ONE 6, e21921 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Busiek, K. K. & Margolin, W. Split decision: a thaumarchaeon encoding both FtsZ and Cdv cell division proteins chooses Cdv for cytokinesis. Mol. Microbiol. 82, 535–538 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Ng, K.-H., Srinivas, V., Srinivasan, R. & Balasubramanian, M. The Nitrosopumilus maritimus CdvB, but not FtsZ, assembles into polymers. Archaea 2013, 104147 (2013).

    PubMed  PubMed Central  Google Scholar 

  90. Ettema, T. J. & Bernander, R. Cell division and the ESCRT complex: a surprise from the archaea. Commun. Integr. Biol. 2, 86–88 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Snyder, J. C., Samson, R. Y., Brumfield, S. K., Bell, S. D. & Young, M. J. Functional interplay between a virus and the ESCRT machinery in Archaea. Proc. Natl Acad. Sci. USA http://dx.doi.org/10.1073/pnas.1301605110 (2013).

  92. Ellen, A. F. et al. Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components. Extremophiles 13, 67–79 (2009).

    CAS  PubMed  Google Scholar 

  93. Henne, W. M., Buchkovich, N. J. & Emr, S. D. The ESCRT pathway. Dev. Cell 21, 77–91 (2011).

    CAS  PubMed  Google Scholar 

  94. Hurley, J. H. ESCRT complexes and the biogenesis of multivesicular bodies. Curr. Opin. Cell Biol. 20, 4–11 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Carlton, J. G. & Martin-Serrano, J. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908–1912 (2007).

    CAS  PubMed  Google Scholar 

  96. Morita, E. et al. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J. 26, 4215–4227 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Völkl, P. et al. Pyrobaculum aerophilum sp. nov., a novel nitrate-reducing hyperthermophilic archaeum. Appl. Environ. Microbiol. 59, 2918–2926 (1993).

    PubMed  PubMed Central  Google Scholar 

  98. Sonobe, S. et al. Proliferation of the hyperthermophilic archaeon Pyrobaculum islandicum by cell fission. Extremophiles 14, 403–407 (2010).

    PubMed  Google Scholar 

  99. Horn, C., Paulmann, B., Kerlen, G., Junker, N. & Huber, H. In vivo observation of cell division of anaerobic hyperthermophiles by using a high-intensity dark-field microscope. J. Bacteriol. 181, 5114–5118 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Pollard, T. D. Mechanics of cytokinesis in eukaryotes. Curr. Opin. Cell Biol. 22, 50–56 (2010).

    CAS  PubMed  Google Scholar 

  101. Vats, P. & Rothfield, L. Duplication and segregation of the actin (MreB) cytoskeleton during the prokaryotic cell cycle. Proc. Natl Acad. Sci. USA 104, 17795–17800 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Typas, A., Banzhaf, M., Gross, C. A. & Vollmer, W. From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nature Rev. Microbiol. 10, 123–136 (2011).

    Google Scholar 

  103. Margolin, W. Sculpting the bacterial cell. Curr. Biol. 19, R812–R822 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Vats, P., Yu, J. & Rothfield, L. The dynamic nature of the bacterial cytoskeleton. Cell. Mol. Life Sci. 66, 3353–3362 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Ouellette, S. P., Karimova, G., Subtil, A. & Ladant, D. Chlamydia co-opts the rod shape-determining proteins MreB and Pbp2 for cell division. Mol. Microbiol. 85, 164–178 (2012).

    CAS  PubMed  Google Scholar 

  106. Osawa, M., Anderson, D. E. & Erickson, H. P. Reconstitution of contractile FtsZ rings in liposomes. Science 320, 792–794 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Könneke, M. et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543–546 (2005).

    PubMed  Google Scholar 

  108. Junglas, B. et al. Ignicoccus hospitalis and Nanoarchaeum equitans: ultrastructure, cell–cell interaction, and 3D reconstruction from serial sections of freeze-substituted cells and by electron cryotomography. Arch. Microbiol. 190, 395–408 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Bernander, R., Poplawski, A. & Grogan, D. W. Altered patterns of cellular growth, morphology, replication and division in conditional-lethal mutants of the thermophilic archaeon Sulfolobus acidocaldarius. Microbiology 146, 749–757 (2000).

    CAS  PubMed  Google Scholar 

  110. Hjort, K. & Bernander, R. Cell cycle regulation in the hyperthermophilic crenarchaeon Sulfolobus acidocaldarius. Mol. Microbiol. 40, 225–234 (2001).

    CAS  PubMed  Google Scholar 

  111. Toro, E., Hong, S. H., McAdams, H. H. & Shapiro, L. Caulobacter requires a dedicated mechanism to initiate chromosome segregation. Proc. Natl Acad. Sci. USA 105, 15435–15440 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the Swedish Research Council (grant 621-2010-5551). This Review is dedicated to the memory of Carl Woese, who discovered archaea.

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  1. Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Svante Arrhenius väg 20C, Stockholm, SE-106 91, Sweden

    Ann-Christin Lindås & Rolf Bernander

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  1. Ann-Christin Lindås
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  2. Rolf Bernander
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Correspondence to Rolf Bernander.

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The authors declare no competing financial interests.

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Glossary

Polyploid

Containing multiple copies of the chromosome (or chromosomes). In archaea and bacteria, the chromosome copies are identical.

Okazaki fragments

Short single-stranded DNA fragments that are synthesized during DNA replication and are rapidly ligated together to form the lagging strand.

Core gene

A gene that is conserved in all, or most, sequenced members of an evolutionary lineage. Core genes are often essential and highly expressed.

Marker frequency analysis

An assay in which the relative copy number of markers (short DNA sequences) distributed along the chromosome is measured. In DNA isolated from an exponentially growing cell population, the markers form a copy number gradient from the replication origin (or origins) to the termination region, provided that replication always initiates from a fixed position.

Replication initiation point mapping

A method for determining the position at which DNA replication is initiated. A short DNA oligonucleotide complementary to a sequence close to a replication origin is hybridized to chromosomal DNA isolated from actively replicating cells. DNA polymerization initiated from the primer continues until the end of the newly synthesized DNA template strand is reached, which marks the replication initiation point.

Centromere

A chromosomal region that functions as the attachment site for spindle fibres during eukaryotic chromosomal segregation (mitosis) and which also holds replicated sister chromatids together.

MinD

A protein belonging to the bacterial MinCDE complex, which prevents cell division from occurring at the cell poles by blocking FtsZ polymerization.

Late endosomes

Membrane-bound compartments in which material destined for degradation in the lysosome is sorted in eukaryotic cells. Late endosomes have passed through several stages of endosome maturation.

Exosome

A multiprotein complex that is involved in RNA degradation in eukaryotes and archaea.

Autophagy

The lysosomal degradation and recycling of defective cellular components in eukaryotes.

Actin–myosin ring

A contractile ring structure that is made of non-muscle myosin and actin filaments, and is responsible for cell constriction during the division process (cytokinesis) in eukaryotic cells.

Structural maintenance of chromosomes family

A family of ATPases that are involved in different aspects of higher-order chromosomal organization and dynamics in all three domains of life.

Tubulin family

A family of GTP-binding globular proteins, each of which forms the structural subunit of a eukaryotic microtubule. Microtubules are involved in a wide range of cellular functions, including shape maintenance, motility, and formation of the spindle fibres that pull chromosomes apart during mitosis.

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Lindås, AC., Bernander, R. The cell cycle of archaea. Nat Rev Microbiol 11, 627–638 (2013). https://doi.org/10.1038/nrmicro3077

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