Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

The cell biology of archaea

Nature Microbiology volume 7, pages 1744–1755 (2022)Cite this article

Subjects

Abstract

The past decade has revealed the diversity and ubiquity of archaea in nature, with a growing number of studies highlighting their importance in ecology, biotechnology and even human health. Myriad lineages have been discovered, which expanded the phylogenetic breadth of archaea and revealed their central role in the evolutionary origins of eukaryotes. These discoveries, coupled with advances that enable the culturing and live imaging of archaeal cells under extreme environments, have underpinned a better understanding of their biology. In this Review we focus on the shape, internal organization and surface structures that are characteristic of archaeal cells as well as membrane remodelling, cell growth and division. We also highlight some of the technical challenges faced and discuss how new and improved technologies will help address many of the key unanswered questions.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The wide spectrum of archaeal cell shapes and sizes schematically visualized to scale.
Fig. 2: The distribution of key components of different archaeal cell biology processes.
Fig. 3: The archaeal cell envelope.
Fig. 4: Fluorescence protein localization images from different archaeal cell biology studies.
Fig. 5: Schematic overview of the best understood cell-division mechanisms in archaea.

Similar content being viewed by others

References

  1. Caforio, A. & Driessen, A. J. M. Archaeal phospholipids: structural properties and biosynthesis. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1862, 1325–1339 (2017).

    Article  CAS  PubMed  Google Scholar 

  2. Albers, S. V. & Jarrell, K. F. The archaellum: how archaea swim. Front. Microbiol. 6, 23 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  3. Albers, S. V. & Jarrell, K. F. The archaellum: an update on the unique archaeal motility structure. Trends Microbiol. 26, 351–362 (2018).

    Article  CAS  PubMed  Google Scholar 

  4. Lyu, Z., Shao, N., Akinyemi, T. & Whitman, W. B. Methanogenesis. Curr. Biol. 28, R727–R732 (2018).

    Article  CAS  PubMed  Google Scholar 

  5. Adam, P. S., Borrel, G., Brochier-Armanet, C. & Gribaldo, S. The growing tree of archaea: new perspectives on their diversity, evolution and ecology. ISME J. 11, 2407–2425 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Spang, A., Caceres, E. F. & Ettema, T. J. G. Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science 357, eaaf3883 (2017).

    Article  PubMed  Google Scholar 

  7. Baker, B. J. et al. Diversity, ecology and evolution of archaea. Nat. Microbiol. 5, 887–900 (2020).

    Article  CAS  PubMed  Google Scholar 

  8. Youngblut, N. D. et al. Vertebrate host phylogeny influences gut archaeal diversity. Nat. Microbiol. 6, 1443–1454 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Geesink, P. & Ettema, T. J. G. The human archaeome in focus. Nat. Microbiol. 7, 10–11 (2022).

    Article  CAS  PubMed  Google Scholar 

  10. Thomas, C., Quemener, E. D.-L., Gribaldo, S. & Borrel, G. Factors shaping the abundance and diversity of archaea in the animal gut. Nat. Commun. 13, 3358 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Dombrowski, N., Lee, J.-H., Williams, T. A., Offre, P. & Spang, A. Genomic diversity, lifestyles and evolutionary origins of DPANN archaea. FEMS Microbiol. Lett. 366, fnz008 (2019).

  12. Spang, A. et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173–179 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Zaremba-Niedzwiedzka, K. et al. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541, 353–358 (2017).

    Article  CAS  PubMed  Google Scholar 

  14. Eme, L., Spang, A., Lombard, J., Stairs, C. W. & Ettema, T. J. G. Archaea and the origin of eukaryotes. Nat. Rev. Microbiol. 15, 711–723 (2017).

    Article  CAS  PubMed  Google Scholar 

  15. Imachi, H. et al. Isolation of an archaeon at the prokaryote-eukaryote interface. Nature 577, 519–525 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Walsh, J. C. et al. Division plane placement in pleomorphic archaea is dynamically coupled to cell shape. Mol. Microbiol. 112, 785–799 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Huber, H. et al. Ignicoccus gen. nov., a novel genus of hyperthermophilic, chemolithoautotrophic archaea, represented by two new species, Ignicoccus islandicus sp nov and Ignicoccus pacificus sp nov. and Ignicoccus pacificus sp. nov. Int. J. Syst. Evol. Microbiol. 50, 2093–2100 (2000).

    Article  PubMed  Google Scholar 

  18. Rachel, R., Wyschkony, I., Riehl, S. & Huber, H. The ultrastructure of Ignicoccus: evidence for a novel outer membrane and for intracellular vesicle budding in an archaeon. Archaea 1, 9–18 (2002).

    Article  CAS  PubMed  Google Scholar 

  19. Heimerl, T. et al. A complex endomembrane system in the archaeon Ignicoccus hospitalis tapped by Nanoarchaeum equitans. Front. Microbiol. 8, 1072 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Kuper, U., Meyer, C., Muller, V., Rachel, R. & Huber, H. Energized outer membrane and spatial separation of metabolic processes in the hyperthermophilic archaeon Ignicoccus hospitalis. Proc. Natl Acad. Sci. USA 107, 3152–3156 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Duggin, I. G. et al. CetZ tubulin-like proteins control archaeal cell shape. Nature 519, 362–365 (2015).

    Article  CAS  PubMed  Google Scholar 

  23. Abdul-Halim, M. F. et al. Lipid anchoring of archaeosortase substrates and midcell growth in Haloarchaea. mBio 11, e00349-20 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  24. de Silva, R. T. et al. Improved growth and morphological plasticity of Haloferax volcanii. Microbiology 167, 001012 (2021).

    Article  PubMed Central  Google Scholar 

  25. Bisson-Filho, A. W., Zheng, J. & Garner, E. Archaeal imaging: leading the hunt for new discoveries. Mol. Biol. Cell 29, 1675–1681 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Elkins, J. G. et al. A korarchaeal genome reveals insights into the evolution of the archaea. Proc. Natl Acad. Sci. USA 105, 8102–8107 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ettema, T. J. G., Lindås, A.-C. & Bernander, R. An actin-based cytoskeleton in archaea. Mol. Microbiol. 80, 1052–1061 (2011).

    Article  CAS  PubMed  Google Scholar 

  28. Zeikus, J. G. & Wolfe, R. S. Fine structure of Methanobacterium thermoautotrophicum: effect of growth temperature on morphology and ultrastructure. J. Bacteriol. 113, 461–467 (1973).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. La Cono, V. et al. Symbiosis between nanohaloarchaeon and haloarchaeon is based on utilization of different polysaccharides. Proc. Natl Acad. Sci. USA 117, 20223–20234 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Jahn, U. et al. Nanoarchaeum equitans and Ignicoccus hospitalis: new insights into a unique, intimate association of two archaea. J. Bacteriol. 190, 1743–1750 (2008).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  32. Wurch, L. et al. Genomics-informed isolation and characterization of a symbiotic nanoarchaeota system from a terrestrial geothermal environment. Nat. Commun. 7, 12115 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Waters, E. et al. The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism. Proc. Natl Acad. Sci. USA 100, 12984–12988 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Castelle, C. J. & Banfield, J. F. Major new microbial groups expand diversity and alter our understanding of the tree of life. Cell 172, 1181–1197 (2018).

    Article  CAS  PubMed  Google Scholar 

  35. de Sousa Machado, N. J., Albers, S.-V. & Daum, B. Towards elucidating the rotary mechanism of the archaellum machinery. Front. Microbiol. 13, 848597 (2022).

  36. Bharat, T. A. M., von Kügelgen, A. & Alva, V. Molecular logic of prokaryotic surface layer structures. Trends Microbiol. 29, 405–415 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  38. Rodrigues-Oliveira, T., Belmok, A., Vasconcellos, D., Schuster, B. & Kyaw, C. M. Archaeal S-layers: overview and current state of the art. Front. Microbiol. 8, 2597 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  39. Jarrell, K. F. et al. N-linked glycosylation in archaea: a structural, functional, and genetic analysis. Microbiol. Mol. Biol. Rev. 78, 304–341 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Engelhardt, H. Are S-layers exoskeletons? The basic function of protein surface layers revisited. J. Struct. Biol. 160, 115–124 (2007).

    Article  CAS  PubMed  Google Scholar 

  41. Zhang, C. et al. Cell structure changes in the hyperthermophilic crenarchaeon Sulfolobus islandicus lacking the S-layer. mBio 10, e01589-19 (2019).

  42. Banerjee, A. et al. FlaF is a β-sandwich protein that anchors the archaellum in the archaeal cell envelope by binding the S-layer protein. Structure 23, 863–872 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Tsai, C.-L. et al. The structure of the periplasmic FlaG–FlaF complex and its essential role for archaellar swimming motility. Nat. Microbiol. 5, 216–225 (2020).

    Article  CAS  PubMed  Google Scholar 

  44. Zhang, C., Phillips, A. P. R., Wipfler, R. L., Olsen, G. J. & Whitaker, R. J. The essential genome of the crenarchaeal model Sulfolobus islandicus. Nat. Commun. 9, 4908 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Wirth, R. et al. The mode of cell wall growth in selected archaea is similar to the general mode of cell wall growth in bacteria as revealed by fluorescent dye analysis. Appl. Environ. Microbiol. 77, 1556–1562 (2011).

    Article  CAS  PubMed  Google Scholar 

  46. Nickell, S., Hegerl, R., Baumeister, W. & Rachel, R. Pyrodictium cannulae enter the periplasmic space but do not enter the cytoplasm, as revealed by cryo-electron tomography. J. Struct. Biol. 141, 34–42 (2003).

    Article  PubMed  Google Scholar 

  47. Moissl, C., Rachel, R., Briegel, A., Engelhardt, H. & Huber, R. The unique structure of archaeal ‘hami’, highly complex cell appendages with nano-grappling hooks. Mol. Microbiol. 56, 361–370 (2005).

    Article  CAS  PubMed  Google Scholar 

  48. Perras, A. K. et al. Grappling archaea: ultrastructural analyses of an uncultivated, cold-loving archaeon, and its biofilm. Front. Microbiol. 5, 397 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Hartman, R. et al. The molecular mechanism of cellular attachment for an archaeal virus. Structure 27, 1634–1646 (2019).

    Article  CAS  PubMed  Google Scholar 

  50. Pohlschroder, M. & Esquivel, R. N. Archaeal type IV pili and their involvement in biofilm formation. Front. Microbiol. 6, 190 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  51. Tittes, C., Schwarzer, S. & Quax, T. E. F. Viral hijack of filamentous surface structures in archaea and bacteria. Viruses 13, 164 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Beeby, M., Ferreira, J. L., Tripp, P., Albers, S.-V. & Mitchell, D. R. Propulsive nanomachines: the convergent evolution of archaella, flagella and cilia. FEMS Microbiol. Rev. 44, 253–304 (2020).

    Article  CAS  PubMed  Google Scholar 

  53. Albers, S.-V., Szabó, Z. & Driessen, A. J. M. Protein secretion in the archaea: multiple paths towards a unique cell surface. Nat. Rev. Microbiol. 4, 537–547 (2006).

    Article  CAS  PubMed  Google Scholar 

  54. Driessen, A. J., Fekkes, P. & van der Wolk, J. P. The Sec system. Curr. Opin. Microbiol. 1, 216–222 (1998).

    Article  CAS  PubMed  Google Scholar 

  55. Rose, R. W., Brüser, T., Kissinger, J. C. & Pohlschröder, M. Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway. Mol. Microbiol. 45, 943–950 (2002).

    Article  CAS  PubMed  Google Scholar 

  56. Storf, S. et al. Mutational and bioinformatic analysis of haloarchaeal lipobox-containing proteins. Archaea 2010, 410975 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Makarova, K. S., Koonin, E. V. & Albers, S. V. Diversity and evolution of type IV pili systems in archaea. Front. Microbiol. 7, 667 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  58. Ayers, M., Howell, P. L. & Burrows, L. L. Architecture of the type II secretion and type IV pilus machineries. Future Microbiol. 5, 1203–1218 (2010).

    Article  CAS  PubMed  Google Scholar 

  59. Zolghadr, B., Klingl, A., Rachel, R., Driessen, A. J. M. & Albers, S.-V. The bindosome is a structural component of the Sulfolobus solfataricus cell envelope. Extremophiles 15, 235–244 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Costa, T. R. D. et al. Type IV secretion systems: advances in structure, function, and activation. Mol. Microbiol. 115, 436–452 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. van Wolferen, M., Wagner, A., van der Does, C. & Albers, S.-V. The archaeal Ced system imports DNA. Proc. Natl Acad. Sci. USA 113, 2496–2501 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  62. Eichler, J. Extreme sweetness: protein glycosylation in archaea. Nat. Rev. Microbiol. 11, 151–156 (2013).

    Article  CAS  PubMed  Google Scholar 

  63. Kaminski, L. et al. Add salt, add sugar: N-glycosylation in Haloferax volcanii. Biochem. Soc. Trans. 41, 432–435 (2013).

    Article  CAS  PubMed  Google Scholar 

  64. Meyer, B. H. & Albers, S. V. Hot and sweet: protein glycosylation in Crenarchaeota. Biochem. Soc. Trans. 41, 384–392 (2013).

    Article  CAS  PubMed  Google Scholar 

  65. van Wolferen, M. et al. Species-specific recognition of Sulfolobales mediated by UV-inducible pili and S-layer glycosylation patterns. mBio 11, e03014-19 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  66. Shalev, Y., Turgeman-Grott, I., Tamir, A., Eichler, J. & Gophna, U. Cell surface glycosylation is required for efficient mating of Haloferax volcanii. Front. Microbiol. 8, 1253 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  67. Chai, Q. et al. Organization of ribosomes and nucleoids in Escherichia coli cells during growth and in quiescence. J. Biol. Chem. 289, 11342–11352 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  70. Liu, J. et al. Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily. Cell 184, 3660–3673 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Liu, J. et al. Archaeal extracellular vesicles are produced in an ESCRT-dependent manner and promote gene transfer and nutrient cycling in extreme environments. ISME J. 15, 2892–2905 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Hatano, T. et al. Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery. Nat. Commun. 13, 3398 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. McBride, H. M. Mitochondria and endomembrane origins. Curr. Biol. 28, R367–R372 (2018).

    Article  CAS  PubMed  Google Scholar 

  74. Bagatolli, L., Gratton, E., Khan, T. K. & Chong, P. L. Two-photon fluorescence microscopy studies of bipolar tetraether giant liposomes from thermoacidophilic archaebacteria Sulfolobus acidocaldarius. Biophys. J. 79, 416–425 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Greci, M. D. & Bell, S. D. Archaeal DNA replication. Annu. Rev. Microbiol. 74, 65–80 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Takemata, N. & Bell, S. D. Emerging views of genome organization in archaea. J. Cell Sci. 133, jcs243782 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Pérez-Arnaiz, P., Dattani, A., Smith, V. & Allers, T. Haloferax volcanii—a model archaeon for studying DNA replication and repair. Open Biol. 10, 200293 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  78. Tarrason Risa, G. et al. The proteasome controls ESCRT-III-mediated cell division in an archaeon. Science 369, eaaz2532 (2020).

  79. Takemata, N., Samson, R. Y. & Bell, S. D. Physical and functional compartmentalization of archaeal chromosomes. Cell 179, 165–179 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Badel, C., Samson, R. Y. & Bell, S. D. Chromosome organization affects genome evolution in Sulfolobus archaea. Nat. Microbiol. 7, 820–830 (2022).

    Article  CAS  PubMed  Google Scholar 

  81. Henneman, B., van Emmerik, C., van Ingen, H. & Dame, R. T. Structure and function of archaeal histones. PLoS Genet. 14, e1007582 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  82. Stevens, K. M. & Warnecke, T. Histone variants in archaea—an undiscovered country. Semin. Cell Dev. Biol. https://doi.org/10.1016/j.semcdb.2022.02.016 (2022).

  83. Pulschen, A. A. et al. Live imaging of a hyperthermophilic archaeon reveals distinct roles for two ESCRT-III homologs in ensuring a robust and symmetric division. Curr. Biol. 30, 2852–2859 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Yen, C.-Y. et al. Chromosome segregation in archaea: SegA– and SegB–DNA complex structures provide insights into segrosome assembly. Nucleic Acids Res. 49, 13150–13164 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Wagstaff, J. & Lowe, J. Prokaryotic cytoskeletons: protein filaments organizing small cells. Nat. Rev. Microbiol. 16, 187–201 (2018).

    Article  CAS  PubMed  Google Scholar 

  87. Carballido-Lopez, R. & Errington, J. The bacterial cytoskeleton: in vivo dynamics of the actin-like protein Mbl of Bacillus subtilis. Dev. Cell 4, 19–28 (2003).

    Article  CAS  PubMed  Google Scholar 

  88. Garner, E. C. et al. Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 333, 222–225 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Izore, T., Kureisaite-Ciziene, D., McLaughlin, S. H. & Lowe, J. Crenactin forms actin-like double helical filaments regulated by arcadin-2. eLife 5, e21600 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  90. Akıl, C. & Robinson, R. C. Genomes of Asgard archaea encode profilins that regulate actin. Nature 562, 439–443 (2018).

    Article  PubMed  Google Scholar 

  91. Akıl, C. et al. Insights into the evolution of regulated actin dynamics via characterization of primitive gelsolin/cofilin proteins from Asgard archaea. Proc. Natl Acad. Sci. USA 117, 19904–19913 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  92. Hussain, S. et al. MreB filaments align along greatest principal membrane curvature to orient cell wall synthesis. eLife 7, e32471 (2018).

  93. Ithurbide, S., Gribaldo, S., Albers, S.-V. & Pende, N. Spotlight on FtsZ-based cell division in archaea. Trends Microbiol. https://doi.org/10.1016/j.tim.2022.01.005 (2022).

  94. Svitkina, T. The actin cytoskeleton and actin-based motility. Cold Spring Harb. Perspect. Biol. 10, a018267 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  95. Svitkina, T. M. Ultrastructure of the actin cytoskeleton. Curr. Opin. Cell Biol. 54, 1–8 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Jung, M. Y., Islam, M. A., Gwak, J. H., Kim, J. G. & Rhee, S. K. Nitrosarchaeum koreense gen. nov., sp. nov., an aerobic and mesophilic, ammonia-oxidizing archaeon member of the phylum Thaumarchaeota isolated from agricultural soil. Int. J. Syst. Evol. Microbiol. 68, 3084–3095 (2018).

    Article  CAS  PubMed  Google Scholar 

  97. Yutin, N. & Koonin, E. V. Archaeal origin of tubulin. Biol. Direct 7, 10 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Lee, K.-C. et al. Phylum Verrucomicrobia representatives share a compartmentalized cell plan with members of bacterial phylum Planctomycetes. BMC Microbiol. 9, 5 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  99. Bisson-Filho, A. W. et al. Treadmilling by FtsZ filaments drives peptidoglycan synthesis and bacterial cell division. Science 355, 739–743 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Stoten, C. L. & Carlton, J. G. ESCRT-dependent control of membrane remodelling during cell division. Semin. Cell Dev. Biol. 74, 50–65 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Liao, Y., Ithurbide, S., Evenhuis, C., Löwe, J. & Duggin, I. G. Cell division in the archaeon Haloferax volcanii relies on two FtsZ proteins with distinct functions in division ring assembly and constriction. Nat. Microbiol. 6, 594–605 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Pende, N. et al. SepF is the FtsZ anchor in archaea, with features of an ancestral cell division system. Nat. Commun. 12, 3214 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Nußbaum, P., Gerstner, M., Dingethal, M., Erb, C. & Albers, S.-V. The archaeal protein SepF is essential for cell division in Haloferax volcanii. Nat. Commun. 12, 3469 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  104. Nußbaum, P. et al. An oscillating MinD protein determines the cellular positioning of the motility machinery in archaea. Curr. Biol. 30, 4956–4972 (2020).

    Article  PubMed  Google Scholar 

  105. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  107. Pfitzner, A.-K. et al. An ESCRT-III polymerization sequence drives membrane deformation and fission. Cell 182, 1140–1155 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. 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).

    Article  CAS  PubMed  Google Scholar 

  110. Liu, J. et al. Functional assignment of multiple ESCRT-III homologs in cell division and budding in Sulfolobus islandicus. Mol. Microbiol. 105, 540–553 (2017).

    Article  CAS  PubMed  Google Scholar 

  111. 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 110, 10783–10787 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Aylett, C. H. S. & Duggin, I. G. The tubulin superfamily in archaea. Subcell. Biochem. 84, 393–417 (2017).

    Article  CAS  PubMed  Google Scholar 

  114. Ranjit, D. K., Liechti, G. W. & Maurelli, A. T. Chlamydial MreB directs cell division and peptidoglycan synthesis in Escherichia coli in the absence of FtsZ activity. mBio 11, e03222-19 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  115. Prangishvili, D., Forterre, P. & Garrett, R. A. Viruses of the Archaea: a unifying view. Nat. Rev. Microbiol. 4, 837–848 (2006).

    Article  CAS  PubMed  Google Scholar 

  116. Burns, D. G., Camakaris, H. M., Janssen, P. H. & Dyall-Smith, M. L. Cultivation of Walsby’s square haloarchaeon. FEMS Microbiol. Lett. 238, 469–473 (2004).

    CAS  PubMed  Google Scholar 

  117. Gambelli, L. et al. Architecture and modular assembly of Sulfolobus S-layers revealed by electron cryotomography. Proc. Natl Acad. Sci. USA 116, 25278–25286 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Anderson, I. et al. Complete genome sequence of Methanothermus fervidus type strain (V24ST). Stand. Genom. Sci. 3, 315–324 (2010).

    Article  Google Scholar 

  119. Burghardt, T. et al. The interaction of Nanoarchaeum equitans with Ignicoccus hospitalis: proteins in the contact site between two cells. Biochem. Soc. Trans. 37, 127–132 (2009).

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  121. Fiala, G. & Stetter, K. O. Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100 °C. Arch. Microbiol. 145, 56–61 (1986).

    Article  CAS  Google Scholar 

  122. Bang, C. & Schmitz, R. A. Archaea associated with human surfaces: not to be underestimated. FEMS Microbiol. Rev. 39, 631–648 (2015).

    Article  CAS  PubMed  Google Scholar 

  123. Turkowyd, B. et al. Establishing live-cell single-molecule localization microscopy imaging and single-particle tracking in the archaeon Haloferax volcanii. Front. Microbiol. 11, 583010 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  124. Cui, H.-L. & Dyall-Smith, M. L. Cultivation of halophilic archaea (class Halobacteria) from thalassohaline and athalassohaline environments. Mar. Life Sci. Technol. 3, 243–251 (2021).

    Article  CAS  Google Scholar 

  125. 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).

    Article  CAS  PubMed  Google Scholar 

  126. Roppelt, V. et al. The archaeal exosome localizes to the membrane. FEBS Lett. 584, 2791–2795 (2010).

    Article  CAS  PubMed  Google Scholar 

  127. Herzog, B. & Wirth, R. Swimming behavior of selected species of archaea. Appl. Environ. Microbiol. 78, 1670–1674 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Lassak, K. et al. Molecular analysis of the crenarchaeal flagellum. Mol. Microbiol. 83, 110–124 (2012).

    Article  CAS  PubMed  Google Scholar 

  129. Mora, M., Bellack, A., Ugele, M., Hopf, J. & Wirth, R. The temperature gradient-forming device, an accessory unit for normal light microscopes to study the biology of hyperthermophilic microorganisms. Appl. Environ. Microbiol. 80, 4764–4770 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  130. Haurat, M. F. et al. ArnS, a kinase involved in starvation-induced archaellum expression. Mol. Microbiol. 103, 181–194 (2017).

    Article  CAS  PubMed  Google Scholar 

  131. Wirth, R., Luckner, M. & Wanner, G. Validation of a hypothesis: colonization of black smokers by hyperthermophilic microorganisms. Front. Microbiol. 9, 524 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  132. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Charles-Orszag, A., Lord, S. J. & Mullins, R. D. High-temperature live-cell imaging of cytokinesis, cell motility, and cell–cell interactions in the thermoacidophilic crenarchaeon Sulfolobus acidocaldarius. Front. Microbiol. 12, 707124 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  134. Cava, F. et al. Expression and use of superfolder green fluorescent protein at high temperatures in vivo: a tool to study extreme thermophile biology. Environ. Microbiol. 10, 605–613 (2008).

    Article  CAS  PubMed  Google Scholar 

  135. Henche, A. L., Koerdt, A., Ghosh, A. & Albers, S. V. Influence of cell surface structures on crenarchaeal biofilm formation using a thermostable green fluorescent protein. Environ. Microbiol. 14, 779–793 (2012).

    Article  CAS  PubMed  Google Scholar 

  136. Khelaifia, S. & Drancourt, M. Susceptibility of archaea to antimicrobial agents: applications to clinical microbiology. Clin. Microbiol. Infect. 18, 841–848 (2012).

    Article  CAS  PubMed  Google Scholar 

  137. Atomi, H., Imanaka, T. & Fukui, T. Overview of the genetic tools in the archaea. Front. Microbiol. https://doi.org/10.3389/fmicb.2012.00337 (2012).

  138. Metcalf, W. W., Zhang, J. K., Apolinario, E., Sowers, K. R. & Wolfe, R. S. A genetic system for archaea of the genus Methanosarcina: liposome-mediated transformation and construction of shuttle vectors. Proc. Natl Acad. Sci. USA 94, 2626–2631 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Tumbula, D. L. & Whitman, W. B. Genetics of Methanococcus: possibilities for functional genomics in archaea. Mol. Microbiol. 33, 1–7 (1999).

    Article  CAS  PubMed  Google Scholar 

  140. Holmes, M. L. & Dyall-Smith, M. L. A plasmid vector with a selectable marker for halophilic archaebacteria. J. Bacteriol. 172, 756–761 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Peck, R. F., DasSarma, S. & Krebs, M. P. Homologous gene knockout in the archaeon Halobacterium salinarum with ura3 as a counterselectable marker. Mol. Microbiol. 35, 667–676 (2000).

    Article  CAS  PubMed  Google Scholar 

  142. Bitan-Banin, G., Ortenberg, R. & Mevarech, M. Development of a gene knockout system for the halophilic archaeon Haloferax volcanii by use of the pyrE gene. J. Bacteriol. 185, 772–778 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Allers, T., Ngo, H.-P., Mevarech, M. & Lloyd, R. G. Development of additional selectable markers for the halophilic archaeon Haloferax volcanii based on the leuB and trpA genes. Appl. Environ. Microbiol. 70, 943–953 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Sato, T., Fukui, T., Atomi, H. & Imanaka, T. Targeted gene disruption by homologous recombination in the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1. J. Bacteriol. 185, 210–220 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Lipscomb, G. L. et al. Natural competence in the hyperthermophilic archaeon Pyrococcus furiosus facilitates genetic manipulation: construction of markerless deletions of genes encoding the two cytoplasmic hydrogenases. Appl. Environ. Microbiol. 77, 2232–2238 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. She, Q. et al. Genetic analyses in the hyperthermophilic archaeon Sulfolobus islandicus. Biochem. Soc. Trans. 37, 92–96 (2009).

    Article  CAS  PubMed  Google Scholar 

  147. Wagner, M. et al. Versatile genetic tool box for the crenarchaeote Sulfolobus acidocaldarius. Front. Microbiol. 3, 214 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  148. Zhang, C. & Whitaker, R. J. A broadly applicable gene knockout system for the thermoacidophilic archaeon Sulfolobus islandicus based on simvastatin selection. Microbiology 158, 1513–1522 (2012).

    Article  CAS  PubMed  Google Scholar 

  149. Leigh, J. A., Albers, S.-V., Atomi, H. & Allers, T. Model organisms for genetics in the domain archaea: methanogens, halophiles, Thermococcales and Sulfolobales. FEMS Microbiol. Rev. 35, 577–608 (2011).

    Article  CAS  PubMed  Google Scholar 

  150. Zink, I. A., Wimmer, E. & Schleper, C. Heavily armed ancestors: CRISPR immunity and applications in archaea with a comparative analysis of CRISPR types in Sulfolobales. Biomolecules 10, 1523 (2020).

    Article  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgements

M.v.W. was supported by a Momentum grant from the VW Foundation (grant no. 94933). A.A.P. was supported by the Wellcome Trust (grant no. 203276/Z/16/Z) and HFSP (grant no. LT001027/2019). B.B. received generous support from the MRC-LMB, The Wellcome Trust (grant no. 203276/Z/16/Z), the VW Foundation (Life? grant no. 94933), the Gordon and Betty Moore Foundation’s Symbiosis in Aquatic Systems Initiative (grant no. 9346), and from the Moore-Simons Project on the Origin of the Eukaryotic Cell (Simons Foundation 735929LPI). S.G. acknowledges funding from the French National Agency for Research Grant Archaevol (grant no. ANR-16-CE02-0005-01) and the French Government’s Investissement d’Avenir programme, Laboratoire d’Excellence ‘Integrative Biology of Emerging Infectious Diseases’ (grant no. ANR-10-LABX-62-IBEID). S.-V.A. received funding from the Life grant Az96727 from the VW foundation and the SFB 1381/German Research Foundation under project no. 403222702-SFB 1381.

Author information

Authors and Affiliations

  1. Molecular Biology of Archaea, Institute of Biology II, Faculty of Biology, University of Freiburg, Freiburg, Germany

    Marleen van Wolferen & Sonja-Verena Albers

  2. Division of Cell Biology, MRC Laboratory of Molecular Biology, Cambridge, UK

    Andre Arashiro Pulschen & Buzz Baum

  3. Evolutionary Biology of the Microbial Cell Unit, CNRS UMR2001, Department of Microbiology, Institute Pasteur, Paris, France

    Simonetta Gribaldo

Authors
  1. Marleen van Wolferen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andre Arashiro Pulschen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Buzz Baum
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Simonetta Gribaldo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sonja-Verena Albers
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.v.W., A.A.P., B.B., S.G. and S.-V.A. contributed equally to all aspects of the article.

Corresponding authors

Correspondence to Buzz Baum, Simonetta Gribaldo or Sonja-Verena Albers.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Microbiology thanks Iain Duggin, Dyche Mullins and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

van Wolferen, M., Pulschen, A.A., Baum, B. et al. The cell biology of archaea. Nat Microbiol 7, 1744–1755 (2022). https://doi.org/10.1038/s41564-022-01215-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41564-022-01215-8

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology