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Evolution of diverse cell division and vesicle formation systems in Archaea

Key Points

  • Recently, the unexpected discovery was made that the hyperthermophilic crenarchaeote Sulfolobus spp. use a novel cell division system that consists of homologues of eukaryotic endosomal secretion complex required for transport III (ESCRT-III) proteins.

  • Comparative genomic analysis shows that Archaea possess at least three distinct membrane remodelling systems, namely, the FtsZ-based bacterial-type systems present in most Euryarchaeota, the ESCRT-III-based system that is responsible for cell division in the Desulphorococcales and the Sulfolobales, and a putative novel system centred around the archaeal actin-related protein in the Thermoproteales.

  • Many archaeal genomes, in particular those of 'Candidatus Korarchaeum cryptophilum', the Thaumarchaeota and some of the Thermococci, encode assortments of components from different membrane remodelling systems.

  • Evolutionary reconstructions suggest that the last common ancestor of the extant archaea possessed a complex membrane remodelling apparatus, different components of which were lost during subsequent evolution of archaeal lineages.

  • Eukaryotes seem to have inherited the ancestral membrane remodelling systems in their entire complexity.

Abstract

Recently a novel cell division system comprised of homologues of eukaryotic ESCRT-III (endosomal sorting complex required for transport III) proteins was discovered in the hyperthermophilic crenarchaeote Sulfolobus acidocaldarius. On the basis of this discovery, we undertook a comparative genomic analysis of the machineries for cell division and vesicle formation in Archaea. Archaea possess at least three distinct membrane remodelling systems: the FtsZ-based bacterial-type system, the ESCRT-III-based eukaryote-like system and a putative novel system that uses an archaeal actin-related protein. Many archaeal genomes encode assortments of components from different systems. Evolutionary reconstruction from these findings suggests that the last common ancestor of the extant Archaea possessed a complex membrane remodelling apparatus, different components of which were lost during subsequent evolution of archaeal lineages. By contrast, eukaryotes seem to have inherited all three ancestral systems.

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Figure 1: Representative gene neighbourhoods of known and predicted membrane remodelling and cell division systems in the Archaea.
Figure 2: The distribution of the key components of membrane manipulation systems among the Archaea.
Figure 3: A hypothetical evolutionary scenario for archaeal and eukaryotic membrane remodelling systems.

References

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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Hildebrandt, E. R. & Hoyt, M. A. Mitotic motors in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1496, 99–116 (2000).

    CAS  Article  PubMed  Google Scholar 

  3. Kunda, P. & Baum, B. The actin cytoskeleton in spindle assembly and positioning. Trends Cell Biol. 19, 174–179 (2009).

    CAS  Article  PubMed  Google Scholar 

  4. Lowe, J. & Amos, L. A. Evolution of cytomotive filaments: the cytoskeleton from prokaryotes to eukaryotes. Int. J. Biochem. Cell Biol. 41, 323–329 (2009).

    Article  PubMed  Google Scholar 

  5. Lowe, J., van den Ent, F. & Amos, L. A. Molecules of the bacterial cytoskeleton. Annu. Rev. Biophys. Biomol. Struct. 33, 177–198 (2004).

    Article  PubMed  Google Scholar 

  6. van den Ent, F., Amos, L. A. & Lowe, J. Prokaryotic origin of the actin cytoskeleton. Nature 413, 39–44 (2001).

    CAS  Article  PubMed  Google Scholar 

  7. Adams, D. W. & Errington, J. Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nature Rev. Microbiol. 7, 642–653 (2009).

    CAS  Article  Google Scholar 

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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Makarova, K. S. & Koonin, E. V. Comparative genomics of archaea: how much have we learned in six years, and what's next? Genome Biol. 4, 115 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Gribaldo, S. & Brochier-Armanet, C. The origin and evolution of Archaea: a state of the art. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1007–1022 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Bernander, R. The archaeal cell cycle: current issues. Mol. Microbiol. 48, 599–604 (2003).

    CAS  Article  PubMed  Google Scholar 

  12. Bernander, R., Lundgren, M. & Ettema, T. J. Comparative and functional analysis of the archaeal cell cycle. Cell Cycle 9, 794–806 (2010).

    Article  PubMed  Google Scholar 

  13. 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  Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Samson, R. Y. & Bell, S. D. Ancient ESCRTs and the evolution of binary fission. Trends Microbiol. 17, 507–513 (2009).

    CAS  Article  PubMed  Google Scholar 

  16. 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).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Lindas, 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). This study and that described in reference 16 provide evidence that Sulfolobus spp. homologues of ESCRT-III and VPS4 are involved in cell division.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Hanson, P. I., Shim, S. & Merrill, S. A. Cell biology of the ESCRT machinery. Curr. Opin. Cell Biol. 21, 568–574 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. Michelet, X., Djeddi, A. & Legouis, R. Developmental and cellular functions of the ESCRT machinery in pluricellular organisms. Biol. Cell 102, 191–202 (2010).

    CAS  Article  PubMed  Google Scholar 

  20. Wollert, T. & Hurley, J. H. Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464, 864–869 (2010). This article describes the in vitro reconstitution of the eukaryotic ESCRT system with purified proteins and model giant unilamellar vesicles. The work shows that ESCRT-I and ESCRT-II form membrane buds that are then cleaved at the neck by ESCRT-III.

  21. Ortmann, A. C. et al. Transcriptome analysis of infection of the archaeon Sulfolobus solfataricus with Sulfolobus turreted icosahedral virus. J. Virol. 82, 4874–4883 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Scott, A. et al. Structure and ESCRT-III protein interactions of the MIT domain of human VPS4A. Proc. Natl Acad. Sci. USA 102, 13813–13818 (2005).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. Stuchell-Brereton, M. D. et al. ESCRT-III recognition by VPS4 ATPases. Nature 449, 740–744 (2007).

    CAS  Article  PubMed  Google Scholar 

  24. Wurtzel, O. et al. A single-base resolution map of an archaeal transcriptome. Genome Res. 20, 133–141 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Hett, E. C. & Rubin, E. J. Bacterial growth and cell division: a mycobacterial perspective. Microbiol. Mol. Biol. Rev. 72, 126–156 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. Sureka, K. et al. Novel role of phosphorylation-dependent interaction between FtsZ and FipA in mycobacterial cell division. PLoS One 5, e8590 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  27. Thakur, M. & Chakraborti, P. K. GTPase activity of mycobacterial FtsZ is impaired due to its transphosphorylation by the eukaryotic-type Ser/Thr kinase, PknA. J. Biol. Chem. 281, 40107–40113 (2006).

    CAS  Article  PubMed  Google Scholar 

  28. Adindla, S., Inampudi, K. K., Guruprasad, K. & Guruprasad, L. Identification and analysis of novel tandem repeats in the cell surface proteins of archaeal and bacterial genomes using computational tools. Comp. Funct. Genomics 5, 2–16 (2004).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. Iwaya, N. et al. A common substrate recognition mode conserved between katanin P60 and VPS4 governs microtubule severing and membrane skeleton reorganization. J. Biol. Chem. 285, 16822–16829 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Vaughan, S., Wickstead, B., Gull, K. & Addinall, S. G. Molecular evolution of FtsZ protein sequences encoded within the genomes of Archaea, Bacteria, and Eukaryota. J. Mol. Evol. 58, 19–29 (2004).

    CAS  Article  PubMed  Google Scholar 

  31. Makarova, K. S. & Koonin, E. V. Two new families of the FtsZ-tubulin protein superfamily implicated in membrane remodeling in diverse bacteria and archaea. Biol. Direct 5, 33 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Hamoen, L. W., Meile, J. C., de Jong, W., Noirot, P. & Errington, J. SepF, a novel FtsZ-interacting protein required for a late step in cell division. Mol. Microbiol. 59, 989–999 (2006).

    CAS  Article  PubMed  Google Scholar 

  33. Marbouty, M., Saguez, C., Cassier-Chauvat, C. & Chauvat, F. Characterization of the FtsZ-interacting septal proteins SepF and Ftn6 in the spherical-celled cyanobacterium Synechocystis strain PCC 6803. J. Bacteriol. 191, 6178–6185 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 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  Article  Google Scholar 

  35. 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  Article  PubMed  PubMed Central  Google Scholar 

  36. Yutin, N., Wolf, M. Y., Wolf, Y. I. & Koonin, E. V. The origins of phagocytosis and eukaryogenesis. Biol. Direct 4, 9 (2009). This study describes archaeal actin-like proteins and suggests a hypothetical scenario of eukaryogenesis. In this scenario, the archaeal ancestor of eukaryotes possessed an actin-based cytoskeleton, including branched filaments, that allowed this organism to produce actin-supported membrane protrusions, and these protrusions facilitated engulfment of other bacteria and archaea.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Pollard, T. D. & Cooper, J. A. Actin, a central player in cell shape and movement. Science 326, 1208–1212 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Easter, J. Jr & Gober, J. W. ParB-stimulated nucleotide exchange regulates a switch in functionally distinct ParA activities. Mol. Cell 10, 427–434 (2002).

    CAS  Article  PubMed  Google Scholar 

  39. Springer, T. A. Complement and the multifaceted functions of VWA and integrin I domains. Structure 14, 1611–1616 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Whittaker, C. A. & Hynes, R. O. Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol. Biol. Cell 13, 3369–3387 (2002).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Prangishvili, D. et al. Sulfolobicins, specific proteinaceous toxins produced by strains of the extremely thermophilic archaeal genus Sulfolobus. J. Bacteriol. 182, 2985–2988 (2000).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. 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). This work demonstrates that Sulfolobus spp. ESCRT-III and VPS4 homologues are found in secreted vesicles, suggesting that they may play a part in the biogenesis of these vesicles.

    CAS  Article  PubMed  Google Scholar 

  43. Soler, N., Marguet, E., Verbavatz, J. M. & Forterre, P. Virus-like vesicles and extracellular DNA produced by hyperthermophilic archaea of the order Thermococcales. Res. Microbiol. 159, 390–399 (2008).

    CAS  Article  PubMed  Google Scholar 

  44. Makarova, K. S., Sorokin, A. V., Novichkov, P. S., Wolf, Y. I. & Koonin, E. V. Clusters of orthologous genes for 41 archaeal genomes and implications for evolutionary genomics of archaea. Biol. Direct 2, 33 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Csuros, M. & Miklos, I. Streamlining and large ancestral genomes in Archaea inferred with a phylogenetic birth-and-death model. Mol. Biol. Evol. 26, 2087–2095 (2009). A sophisticated maximum-likelihood reconstruction of archaeal genome evolution that infers highly complex ancestors of the Archaea.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Embley, T. M. & Martin, W. Eukaryotic evolution, changes and challenges. Nature 440, 623–630 (2006).

    CAS  Article  PubMed  Google Scholar 

  47. Pisani, D., Cotton, J. A. & McInerney, J. O. Supertrees disentangle the chimerical origin of eukaryotic genomes. Mol. Biol. Evol. 24, 1752–1760 (2007).

    CAS  Article  PubMed  Google Scholar 

  48. Cox, C. J., Foster, P. G., Hirt, R. P., Harris, S. R. & Embley, T. M. The archaebacterial origin of eukaryotes. Proc. Natl Acad. Sci. USA 105, 20356–20361 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. Yutin, N., Makarova, K. S., Mekhedov, S. L., Wolf, Y. I. & Koonin, E. V. The deep archaeal roots of eukaryotes. Mol. Biol. Evol. 25, 1619–1630 (2008). This and references 47 and 48 provide detailed analyses of the contributions of different groups of archaea to the evolution of eukaryotes.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. Carballido-Lopez, R. & Formstone, A. Shape determination in Bacillus subtilis. Curr. Opin. Microbiol. 10, 611–616 (2007).

    CAS  Article  PubMed  Google Scholar 

  51. Graumann, P. L. Dynamics of bacterial cytoskeletal elements. Cell. Motil. Cytoskeleton 66, 909–914 (2009).

    CAS  Article  PubMed  Google Scholar 

  52. Leaver, M., Dominguez-Cuevas, P., Coxhead, J. M., Daniel, R. A. & Errington, J. Life without a wall or division machine in Bacillus subtilis. Nature 457, 849–853 (2009). An intriguing study showing that, under highly defined conditions, FtsZ can be dispensible for viability in B. subtilis . The cells lacking FtsZ and cell walls divide by a bizarre budding–extrusion mechanism.

    Google Scholar 

  53. Jenkins, C. et al. Genes for the cytoskeletal protein tubulin in the bacterial genus Prosthecobacter. Proc. Natl Acad. Sci. USA 99, 17049–17054 (2002).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. Pilhofer, M., Rosati, G., Ludwig, W., Schleifer, K. H. & Petroni, G. Coexistence of tubulins and ftsZ in different Prosthecobacter species. Mol. Biol. Evol. 24, 1439–1442 (2007).

    CAS  Article  PubMed  Google Scholar 

  55. McDonald, B. & Martin-Serrano, J. No strings attached: the ESCRT machinery in viral budding and cytokinesis. J. Cell Sci. 122, 2167–2177 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  56. Shestakova, A. et al. Assembly of the AAA ATPase Vps4 on ESCRT-III. Mol. Biol. Cell 21, 1059–1071 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  58. 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). This work, along with that described in reference 57, provides the first evidence that the ESCRT machinery localizes to the midbody and is required for membrane abscission in human cells.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  59. Yang, D. et al. Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B. Nature Struct. Mol. Biol. 15, 1278–1286 (2008). This investigation shows that an ESCRT-III protein, Chmp1b, recruits the microtubule-severing ATPase, spastin, to the midbody through a MIT domain–MIM3 interaction.

    CAS  Article  Google Scholar 

  60. Koonin, E. V. Orthologs, paralogs and evolutionary genomics. Annu. Rev. Genet. 39, 309–338 (2005).

    CAS  Article  PubMed  Google Scholar 

  61. Tatusov, R. L. et al. The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4, 41 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  62. Tatusov, R. L., Koonin, E. V. & Lipman, D. J. A genomic perspective on protein families. Science 278, 631–637 (1997).

    CAS  Article  PubMed  Google Scholar 

  63. 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  Article  Google Scholar 

  64. 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).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  65. Yarza, P. et al. The All-Species Living Tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst. Appl. Microbiol. 31, 241–50 (2008).

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank Y. Wolf for useful discussions and help with the preparation of figure 3. The authors' research is supported by the Intramural Research Program of the US National Institutes of Health, National Library of Medicine (K.S.M., N.Y. and E.V.K.) and by the Edward Penley Abraham Trust (S.D.B.).

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Correspondence to Stephen D. Bell or Eugene V. Koonin.

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Supplementary information

Supplementary information S1 (box)

The NCBI Refseq database1 was used for retrieval of information on genomic context. (PDF 100 kb)

Supplementary information S2 (table)

Central components of various cell division and membrane remodelling systems (XLS 57 kb)

Supplementary information S3 (figure)

MIT domains of VSP4 ATPase (PDF 138 kb)

Supplementary information S4 (figure)

Architecture of operons of all organisms mentioned in this Analysis article (PDF 250 kb)

Supplementary information S5 (table)

Neighbourhoods of all genes relevant to this work with genome context and gene coordinates (XLS 131 kb)

Supplementary information S6 (table)

Uncharacterized putative components of membrane remodelling systems in archaea (PDF 175 kb)

Supplementary information S7 (figure)

Alignment of Snf7 family proteins (PDF 93 kb)

Supplementary information S8 (figure)

Phylogenetic tree of VPS4 and related ATPases (PDF 209 kb)

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arCOG

Glossary

Orthologue

One of two or more homologous genes (or the encoded proteins) that are derived by vertical descent from a common ancestor.

Paralogue

One of two or more homologous genes (or their encoded proteins) that have evolved following duplication of an ancestral gene.

FHA domain

A domain that binds phosphopeptides. Most FHA domains recognize phosphothreonine, with additional specificity contributed by residues that are carboxy–terminal to the phosphothreonine.

AAA+ ATPase

A member of the vast superfamily of ATPases associated with various cellular activities (AAA+). These proteins utilize the energy of ATP binding, hydrolysis and release to remodel macromolecular substrates.

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Makarova, K., Yutin, N., Bell, S. et al. Evolution of diverse cell division and vesicle formation systems in Archaea. Nat Rev Microbiol 8, 731–741 (2010). https://doi.org/10.1038/nrmicro2406

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