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  • Review Article
  • Published:

Minimal protein-folding systems in hyperthermophilic archaea

Nature Reviews Microbiology volume 2, pages 315–324 (2004)Cite this article

Key Points

  • Even hyperthermophiles, which grow optimally at temperatures of more than 80°C, require a functional heat-shock response to cope with exposure to temperatures that exceed their optimal growth temperatures.

  • Owing to the rapid accumulation of complete genome sequences, comparative bioinformatic studies of protein folding in Archaea are now possible. Using this as a basis, the authors review the heat-shock protein complement of archaeal species, concentrating on hyperthermophiles.

  • Surprisingly, the major chaperone classes Hsp100 and Hsp90/Hsp83 are absent from the genomes of the hyperthermophilic archaea, although they are present in mesophilic archaea.

  • High-molecular mass chaperones have AAA domains — a domain that is typical of proteins that have activities associated with ATPases. Heat-shock-regulated proteins that harbour AAA domains have been found in archaeal species, and the authors speculate on the role that these proteins might have in the hyperthermophilic heat-shock response.

  • The authors discuss the roles that archaeal versions of Hsp60 and Hsp70 (chaperones) have in the hyperthermophilic heat-shock response.

  • The number of small heat shock protein (sHSP) homologues in archaeal species ranges from 1–3 copies per genome. Structures of two of these sHSPs have been solved, and the roles of the hyperthermophilic sHSPs in protein refolding are described.

  • Methanosarcina acetivorans, which has one of the largest archaeal genomes sequenced so far, has all versions of chaperonins and Hsp100 proteins, and has features in common with bacterial and eukaryotic heat shock systems.

  • Finally, the authors discuss whether genome 'downsizing' in hyperthermophilic archaeal species has been accompanied by a reduction in the number of heat-shock-response proteins, to produce a minimal protein-folding system to cope with heat stress.

Abstract

Although many archaeal species thrive in extreme environments, including hydrothermal vents, geothermal springs, acid seeps or hypersaline pools, there are also numerous species that are mesophilic. Mesophilic archaeal genomes encode complex protein-folding systems, which include combinations of bacterial and eukaryotic heat-shock proteins. Hyperthermophilic archaea, however, typically have reduced genomes that encode simplified heat-shock systems, with chaperones that are homologous to eukaryotic chaperones, and are reviewed here.

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Figure 1: Phylogenetic tree of archaeal AAA proteins.
Figure 2: Heat-shock inducible promoters of AAA-encoding genes in Pyrococcus furiosus and Pyrococcus abyssi.

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References

  1. Karner, M. B., DeLong, E. F. & Karl, D. M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001).

    Article  CAS  PubMed  Google Scholar 

  2. 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). Recognition of the Archaea as a distinct Domain with many molecular properties resembling Eukaryotes.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Woese, C. R. On the evolution of cells. Proc. Natl Acad. Sci. USA 99, 8742–8747 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Hickey, A. J., Conway de Macario, E. & Macario, A. J. Transcription in the archaea: basal factors, regulation, and stress-gene expression. Crit. Rev. Biochem. Mol. Biol. 37, 537–599 (2002). Comprehensive state-of-the-art review of archaeal transcription and the regulation of stress responses.

    Article  CAS  PubMed  Google Scholar 

  6. Kelman, L. M. & Kelman, Z. Archaea: an archetype for replication initiation studies? Mol. Microbiol. 48, 605–615 (2003).

    Article  CAS  PubMed  Google Scholar 

  7. White, M. F. & Bell, S. D. Holding it together: chromatin in the Archaea. Trends Genet. 18, 621–626 (2002).

    Article  CAS  PubMed  Google Scholar 

  8. Neuwald, A. F., Aravind, L., Spouge, J. L. & Koonin, E. V. AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9, 27–43 (1999).

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  11. Vierke, G., Engelmann, A., Hebbeln, C. & Thomm, M. A novel archaeal transcriptional regulator of heat shock response. J. Biol. Chem. 278, 18–26 (2003).

    Article  CAS  PubMed  Google Scholar 

  12. Yamauchi, K., Doi, K. & Kinoshita, M. Archaebacterial lipid models: stable liposomes from 1-alky1-2-phytanyl-sn-glycero-3-phosphocholines. Biochim. Biophys. Acta 1283, 163–169 (1996).

    Article  PubMed  Google Scholar 

  13. Komatsu, H. & Chong, P. L. Low permeability of liposomal membranes composed of bipolar tetraether lipids from thermoacidophilic archaebacterium Sulfolobus acidocaldarius. Biochemistry 37, 107–115 (1998).

    Article  CAS  PubMed  Google Scholar 

  14. Kashefi, K. & Lovley, D. R. Extending the upper temperature limit for life. Science 301, 934 (2003). Evidence for survival, and possibly growth, in excess of 121°C.

    Article  CAS  PubMed  Google Scholar 

  15. Schleper, C. et al. Picrophilus gen. nov., fam. nov.: a novel aerobic, heterotrophic, thermoacidophilic genus and family comprising archaea capable of growth around pH 0. J. Bacteriol. 177, 7050–7059 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 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 

  17. Ritossa, F. A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia 18, 571–573 (1962).

    Article  CAS  Google Scholar 

  18. Tissieres, A., Mitchell, H. K. & Tracy, U. M. Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. J. Mol. Biol. 85, 389–398 (1974).

    Article  Google Scholar 

  19. Phipps, B. M., Hoffmann, A., Stetter, K. O. & Baumeister, W. A novel ATPase complex selectively accumulated upon heat shock is a major cellular component of thermophilic archaebacteria. EMBO J. 10, 1711–1722 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Trent, J. D., Gabrielsen, M., Jensen, B., Neuhard, J. & Olsen, J. Acquired thermotolerance and heat shock proteins in thermophiles from the three phylogenetic domains. J. Bacteriol. 176, 6148–6152 (1994). Pioneering work recognizing the major components of heat-shock regulation in all Domains.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Laksanalamai, P., Maeder, D. L. & Robb, F. T. Regulation and mechanism of action of the small heat shock protein from the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 183, 5198–5202 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Usui, K., Yoshida, T., Maruyama, T. & Yohda, M. Small heat shock protein of a hyperthermophilic archaeum, Thermococcus sp. strain KS-1, exists as a spherical 24-mer and its expression is highly induced under heat-stress conditions. J. Biosci. Bioeng. 92, 161–166 (2001).

    Article  CAS  PubMed  Google Scholar 

  23. Robb, F. T. in Microbial Genomes (eds Fraser, C. M. & Nelson, K. E.) (Humana Press, 2003).

    Google Scholar 

  24. Macario, A. J. & Conway De Macario, E. The molecular chaperone system and other anti-stress mechanisms in archaea. Front. Biosci. 6, D262–D283 (2001).

    Article  CAS  PubMed  Google Scholar 

  25. Nathan, D. F., Vos, M. H. & Lindquist, S. In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc. Natl Acad. Sci. USA 94, 12949–12956 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Trent, J. D. A review of acquired thermotolerance, heat-shock proteins, and molecular chaperones in archaea. FEMS Microbiol. Rev. 18, 249–258 (1996).

    Article  CAS  Google Scholar 

  27. Trent, J. D., Kagawa, H. K. & Yaoi, T. The role of chaperonins in vivo: the next frontier. Ann. NY Acad. Sci. 851, 36–47 (1998).

    Article  CAS  PubMed  Google Scholar 

  28. Archibald, J. M., Logsdon, J. M. & Doolittle, W. F. Recurrent paralogy in the evolution of archaeal chaperonins. Curr. Biol. 9, 1053–1056 (1999).

    Article  CAS  PubMed  Google Scholar 

  29. Matthews, R. C. et al. Stress proteins in fungal diseases. Med. Mycol. 36 (Suppl.), S45–S51 (1998).

    Google Scholar 

  30. Macario, A. J., Lange, M., Ahring, B. K. & De Macario, E. C. Stress genes and proteins in the archaea. Microbiol. Mol. Biol. Rev. 63, 923–967 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Fareleira, P. et al. Response of a strict anaerobe to oxygen: survival strategies in Desulfovibrio gigas. Microbiology 149, 1513–1522 (2003).

    Article  CAS  PubMed  Google Scholar 

  32. Sanchez, Y. & Lindquist, S. L. HSP104 required for induced thermotolerance. Science 248, 1112–1115 (1990).

    Article  CAS  PubMed  Google Scholar 

  33. Gill, R. T., Valdes, J. J. & Bentley, W. E. A comparative study of global stress gene regulation in response to overexpression of recombinant proteins in Escherichia coli. Metab. Eng. 2, 178–189 (2000).

    Article  CAS  PubMed  Google Scholar 

  34. Schlieker, C., Bukau, B. & Mogk, A. Prevention and reversion of protein aggregation by molecular chaperones in the E. coli cytosol: implications for their applicability in biotechnology. J. Biotechnol. 96, 13–21 (2002).

    Article  CAS  PubMed  Google Scholar 

  35. Wickner, S. et al. A molecular chaperone, ClpA, functions like DnaK and DnaJ. Proc. Natl Acad. Sci. USA 91, 12218–12222 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Pak, M. & Wickner, S. Mechanism of protein remodeling by ClpA chaperone. Proc. Natl Acad. Sci. USA 94, 4901–4906 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Konieczny, I. & Liberek, K. Cooperative action of Escherichia coli ClpB protein and DnaK chaperone in the activation of a replication initiation protein. J. Biol. Chem. 277, 18483–18488 (2002).

    Article  CAS  PubMed  Google Scholar 

  38. Netzer, W. J. & Hartl, F. U. Protein folding in the cytosol: chaperonin-dependent and -independent mechanisms. Trends Biochem. Sci. 23, 68–73 (1998).

    Article  CAS  PubMed  Google Scholar 

  39. Zolkiewski, M. ClpB cooperates with DnaK, DnaJ, and GrpE in suppressing protein aggregation. A novel multi-chaperone system from Escherichia coli. J. Biol. Chem. 274, 28083–28086 (1999).

    Article  CAS  PubMed  Google Scholar 

  40. Figueiredo, L. et al. Functional characterization of an archaeal GroEL/GroES chaperonin system: significance of substrate encapsulation. J. Biol. Chem. 279, 1090–1099 (2004).

    Article  CAS  PubMed  Google Scholar 

  41. Chuang, S. E., Burland, V., Plunkett, G., Daniels, D. L. & Blattner, F. R. Sequence analysis of four new heat-shock genes constituting the hslTS/ibpAB and hslVU operons in Escherichia coli. Gene 134, 1–6 (1993).

    Article  CAS  PubMed  Google Scholar 

  42. Maupin-Furlow, J. A., Kaczowka, S. J., Reuter, C. J., Zuobi-Hasona, K. & Gil, M. A. Archaeal proteasomes: potential in metabolic engineering. Metab. Eng. 5, 151–163 (2003).

    Article  CAS  PubMed  Google Scholar 

  43. Ramachandran, R., Hartmann, C., Song, H. K., Huber, R. & Bochtler, M. Functional interactions of HslV (ClpQ) with the ATPase HslU (ClpY). Proc. Natl Acad. Sci. USA 99, 7396–7401 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Rohrwild, M. et al. The ATP-dependent HslVU protease from Escherichia coli is a four-ring structure resembling the proteasome. Nature Struct. Biol. 4, 133–139 (1997).

    Article  CAS  PubMed  Google Scholar 

  45. Rohrwild, M. et al. HslV–HslU: a novel ATP-dependent protease complex in Escherichia coli related to the eukaryotic proteasome. Proc. Natl Acad. Sci. USA 93, 5808–5813 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Schirmer, E. C., Glover, J. R., Singer, M. A. & Lindquist, S. HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem. Sci. 21, 289–296 (1996).

    Article  CAS  PubMed  Google Scholar 

  47. Dougan, D. A., Mogk, A. & Bukau, B. Protein folding and degradation in bacteria: to degrade or not to degrade? That is the question. Cell. Mol. Life Sci. 59, 1607–1616 (2002).

    Article  CAS  PubMed  Google Scholar 

  48. Bochtler, M. et al. The structures of HsIU and the ATP-dependent protease HsIU–HsIV. Nature 403, 800–805 (2000).

    Article  CAS  PubMed  Google Scholar 

  49. Sousa, M. C. et al. Crystal and solution structures of an HslUV protease–chaperone complex. Cell 103, 633–643 (2000).

    Article  CAS  PubMed  Google Scholar 

  50. Lenzen, C. U., Steinmann, D., Whiteheart, S. W. & Weis, W. I. Crystal structure of the hexamerization domain of N-ethylmaleimide-sensitive fusion protein. Cell 94, 525–536 (1998).

    Article  CAS  PubMed  Google Scholar 

  51. Matveeva, E. A., He, P. & Whiteheart, S. W. N-ethylmaleimide-sensitive fusion protein contains high and low affinity ATP-binding sites that are functionally distinct. J. Biol. Chem. 272, 26413–26418 (1997).

    Article  CAS  PubMed  Google Scholar 

  52. Whiteheart, S. W., Schraw, T. & Matveeva, E. A. N-ethylmaleimide sensitive factor (NSF) structure and function. Int. Rev. Cytol. 207, 71–112 (2001).

    Article  CAS  PubMed  Google Scholar 

  53. May, A. P., Misura, K. M., Whiteheart, S. W. & Weis, W. I. Crystal structure of the amino-terminal domain of N-ethylmaleimide-sensitive fusion protein. Nature Cell Biol. 1, 175–182 (1999).

    Article  CAS  PubMed  Google Scholar 

  54. Cao, K., Nakajima, R., Meyer, H. H. & Zheng, Y. The AAA-ATPase Cdc48/p97 regulates spindle disassembly at the end of mitosis. Cell 115, 355–367 (2003).

    Article  CAS  PubMed  Google Scholar 

  55. Mayer, M. P. et al. Multistep mechanism of substrate binding determines chaperone activity of Hsp70. Nature Struct. Biol. 7, 586–593 (2000).

    Article  CAS  PubMed  Google Scholar 

  56. Burston, S. G. & Clarke, A. R. Molecular chaperones: physical and mechanistic properties. Essays Biochem. 29, 125–136 (1995).

    CAS  PubMed  Google Scholar 

  57. Kagawa, H. K. et al. The 60 kDa heat shock proteins in the hyperthermophilic archaeon Sulfolobus shibatae. J. Mol. Biol. 253, 712–725 (1995).

    Article  CAS  PubMed  Google Scholar 

  58. Gupta, R. S. Evolution of the chaperonin families (Hsp60, Hsp10 and Tcp-1) of proteins and the origin of eukaryotic cells. Mol. Microbiol. 15, 1–11 (1995).

    Article  CAS  PubMed  Google Scholar 

  59. Trent, J. D., Nimmesgern, E., Wall, J. S., Hartl, F. U. & Horwich, A. L. A molecular chaperone from a thermophilic archaebacterium is related to the eukaryotic protein T-complex polypeptide-1. Nature 354, 490–493 (1991).

    Article  CAS  PubMed  Google Scholar 

  60. Waldmann, T., Lupas, A., Kellermann, J., Peters, J. & Baumeister, W. Primary structure of the thermosome from Thermoplasma acidophilum. Biol. Chem. Hoppe Seyler 376, 119–126 (1995).

    Article  CAS  PubMed  Google Scholar 

  61. Quaite-Randall, E., Trent, J. D., Josephs, R. & Joachimiak, A. Conformational cycle of the archaeosome, a TCP1-like chaperonin from Sulfolobus shibatae. J. Biol. Chem. 270, 28818–28823 (1995).

    Article  CAS  PubMed  Google Scholar 

  62. Yaoi, T., Kagawa, H. K. & Trent, J. D. Chaperonin filaments: their formation and an evaluation of methods for studying them. Arch. Biochem. Biophys. 356, 55–62 (1998).

    Article  CAS  PubMed  Google Scholar 

  63. Klumpp, M. & Baumeister, W. The thermosome: archetype of group II chaperonins. FEBS Lett. 430, 73–77 (1998).

    Article  CAS  PubMed  Google Scholar 

  64. Kagawa, H. K. et al. The composition, structure and stability of a group II chaperonin are temperature regulated in a hyperthermophilic archaeon. Mol. Microbiol. 48, 143–156 (2003).

    Article  CAS  PubMed  Google Scholar 

  65. Xu, Z., Horwich, A. L. & Sigler, P. B. The crystal structure of the asymmetric GroEL–GroES–(ADP)7 chaperonin complex. Nature 388, 741–750 (1997).

    Article  CAS  PubMed  Google Scholar 

  66. Fiaux, J., Bertelsen, E. B., Horwich, A. L. & Wuthrich, K. NMR analysis of a 900K GroEL–GroES complex. Nature 418, 207–211 (2002).

    Article  CAS  PubMed  Google Scholar 

  67. Ditzel, L. et al. Crystal structure of the thermosome, the archaeal chaperonin and homolog of CCT. Cell 93, 125–138 (1998).

    Article  CAS  PubMed  Google Scholar 

  68. Steinbacher, S. & Ditzel, L. Review: nucleotide binding to the thermoplasma thermosome: implications for the functional cycle of group II chaperonins. J. Struct. Biol. 135, 147–156 (2001).

    Article  CAS  PubMed  Google Scholar 

  69. Trent, J. D., Kagawa, H. K., Yaoi, T., Olle, E. & Zaluzec, N. J. Chaperonin filaments: the archaeal cytoskeleton? Proc. Natl Acad. Sci. USA 94, 5383–5388 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Trent, J. D. et al. Intracellular localization of a group II chaperonin indicates a membrane-related function. Proc. Natl Acad. Sci. USA 100, 15589–15594 (2003). Identification of membrane-bound chaperonins in a hyperthermophile. Introduces the idea of cellular functions beyond protein folding.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Hayer-Hartl, M. K., Weber, F. & Hartl, F. U. Mechanism of chaperonin action: GroES binding and release can drive GroEL-mediated protein folding in the absence of ATP hydrolysis. EMBO J. 15, 6111–6121 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Hartl, F. U. Molecular chaperones in cellular protein folding. Nature 381, 571–579 (1996).

    Article  CAS  PubMed  Google Scholar 

  73. Langer, T., Pfeifer, G., Martin, J., Baumeister, W. & Hartl, F. U. Chaperonin-mediated protein folding: GroES binds to one end of the GroEL cylinder, which accommodates the protein substrate within its central cavity. EMBO J. 11, 4757–4765 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Kusmierczyk, A. R. & Martin, J. Chaperonins — keeping a lid on folding proteins. FEBS Lett. 505, 343–347 (2001).

    Article  CAS  PubMed  Google Scholar 

  75. Kusmierczyk, A. R. & Martin, J. Assembly of chaperonin complexes. Mol. Biotechnol. 19, 141–152 (2001).

    Article  CAS  PubMed  Google Scholar 

  76. Yoshida, T. et al. Archaeal group II chaperonin mediates protein folding in the cis-cavity without a detachable GroES-like co-chaperonin. J. Mol. Biol. 315, 73–85 (2002).

    Article  CAS  PubMed  Google Scholar 

  77. Iizuka, R. et al. ATP binding is critical for the conformational change from an open to closed state in archaeal group II chaperonin. J. Biol. Chem. 278, 44959–44965 (2003).

    Article  CAS  PubMed  Google Scholar 

  78. Pfund, C., Huang, P., Lopez-Hoyo, N. & Craig, E. A. Divergent functional properties of the ribosome-associated molecular chaperone Ssb compared with other Hsp70s. Mol. Biol. Cell. 12, 3773–3782 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Hartl, F. U. & Hayer-Hartl, M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852–1858 (2002).

    Article  CAS  PubMed  Google Scholar 

  80. Gribaldo, S. et al. Discontinuous occurrence of the hsp70 (dnaK) gene among Archaea and sequence features of HSP70 suggest a novel outlook on phylogenies inferred from this protein. J. Bacteriol. 181, 434–443 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Han, W. & Christen, P. Mechanism of the targeting action of DnaJ in the DnaK molecular chaperone system. J. Biol. Chem. 278, 19038–19043 (2003).

    Article  CAS  PubMed  Google Scholar 

  82. Bukau, B. & Horwich, A. L. The Hsp70 and Hsp60 chaperone machines. Cell 92, 351–366 (1998).

    Article  CAS  PubMed  Google Scholar 

  83. Young, J. C., Hoogenraad, N. J. & Hartl, F. U. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112, 41–50 (2003).

    Article  CAS  PubMed  Google Scholar 

  84. Laksanalamai, P. & Robb, F. T. Small heat shock protein from extremophiles: a review. Extremophiles 8, 1–11 (2004). Comprehensive description of the chaperonins in microorganisms that are adapted to extreme environments.

    Article  CAS  PubMed  Google Scholar 

  85. Caspers, G. J., Leunissen, J. A. & de Jong, W. W. The expanding small heat-shock protein family, and structure predictions of the conserved 'α-crystallin domain'. J. Mol. Evol. 40, 238–248 (1995).

    Article  CAS  PubMed  Google Scholar 

  86. de Jong, W. W., Caspers, G. J. & Leunissen, J. A. Genealogy of the α-crystallin small heat-shock protein superfamily. Int. J. Biol. Macromol. 22, 151–162 (1998).

    Article  CAS  PubMed  Google Scholar 

  87. Narberhaus, F. α-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol. Mol. Biol. Rev. 66, 64–93 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Haslbeck, M. sHsps and their role in the chaperone network. Cell. Mol. Life Sci. 59, 1649–1657 (2002).

    Article  CAS  PubMed  Google Scholar 

  89. Muchowski, P. J. & Clark, J. I. ATP-enhanced molecular chaperone functions of the small heat shock protein human αB crystallin. Proc. Natl Acad. Sci. USA 95, 1004–1009 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Muchowski, P. J., Hays, L. G., Yates, J. R. & Clark, J. I. ATP and the core 'α-crystallin' domain of the small heat-shock protein αB-crystallin. J. Biol. Chem. 274, 30190–30195 (1999).

    Article  CAS  PubMed  Google Scholar 

  91. Horwitz, J. α-crystallin can function as a molecular chaperone. Proc. Natl Acad. Sci. USA 89, 10449–10453 (1992). First recognition of the protein stabilization role of the α-crystallins.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Laksanalamai, P., Jiemjit, A., Bu, Z., Maeder, L. & Robb, F. T. Multi-subunit assembly of the Pyrococcus furiosus small heat shock protein is essential for cellular protection at high temperature. Extremophiles 7, 79–83 (2003).

    Article  CAS  PubMed  Google Scholar 

  93. Sun, W., Van Montagu, M. & Verbruggen, N. Small heat shock proteins and stress tolerance in plants. Biochim. Biophys. Acta 1577, 1–9 (2002).

    Article  CAS  PubMed  Google Scholar 

  94. Scharf, K. D., Siddique, M. & Vierling, E. The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing α-crystallin domains (Acd proteins). Cell Stress Chaperones 6, 225–237 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Ruepp, A., Rockel, B., Gutsche, I., Baumeister, W. & Lupas, A. N. The chaperones of the archaeon Thermoplasma acidophilum. J. Struct. Biol. 135, 126–138 (2001).

    Article  CAS  PubMed  Google Scholar 

  96. Kim, K. K., Kim, R. & Kim, S. H. Crystal structure of a small heat-shock protein. Nature 394, 595–599 (1998).

    Article  CAS  PubMed  Google Scholar 

  97. Kim, K. K. et al. Purification, crystallization, and preliminary X-ray crystallographic data analysis of small heat shock protein homolog from Methanococcus jannaschii, a hyperthermophile. J. Struct. Biol. 121, 76–80 (1998).

    Article  CAS  PubMed  Google Scholar 

  98. van Montfort, R. L., Basha, E., Friedrich, K. L., Slingsby, C. & Vierling, E. Crystal structure and assembly of a eukaryotic small heat shock protein. Nature Struct. Biol. 8, 1025–1030 (2001).

    Article  CAS  PubMed  Google Scholar 

  99. Kim, D. R., Lee, I., Ha, S. C. & Kim, K. K. Activation mechanism of HSP16.5 from Methanococcus jannaschii. Biochem. Biophys. Res. Commun. 307, 991–998 (2003).

    Article  CAS  PubMed  Google Scholar 

  100. Kim, R., Kim, K. K., Yokota, H. & Kim, S. H. Small heat shock protein of Methanococcus jannaschii, a hyperthermophile. Proc. Natl Acad. Sci. USA 95, 9129–9133 (1998). Groundbreaking paper describing the cloning and expression of an sHsp from a hyperthermophile.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Roy, S. K., Hiyama, T. & Nakamoto, H. Purification and characterization of the 16-kDa heat-shock-responsive protein from the thermophilic cyanobacterium Synechococcus vulcanus, which is an α-crystallin-related, small heat shock protein. Eur. J. Biochem. 262, 406–416 (1999).

    Article  CAS  PubMed  Google Scholar 

  102. Chang, Z. et al. Mycobacterium tuberculosis 16-kDa antigen (Hsp16.3) functions as an oligomeric structure in vitro to suppress thermal aggregation. J. Biol. Chem. 271, 7218–7223 (1996).

    Article  CAS  PubMed  Google Scholar 

  103. Lee, G. J., Pokala, N. & Vierling, E. Structure and in vitro molecular chaperone activity of cytosolic small heat shock proteins from pea. J. Biol. Chem. 270, 10432–10438 (1995).

    Article  CAS  PubMed  Google Scholar 

  104. Schumacher, R. J. et al. Cooperative action of Hsp70, Hsp90, and DnaJ proteins in protein renaturation. Biochemistry 35, 14889–14898 (1996).

    Article  CAS  PubMed  Google Scholar 

  105. Schumacher, R. J. et al. ATP-dependent chaperoning activity of reticulocyte lysate. J. Biol. Chem. 269, 9493–9499 (1994).

    CAS  PubMed  Google Scholar 

  106. Siegers, K. et al. TRiC/CCT cooperates with different upstream chaperones in the folding of distinct protein classes. EMBO J. 22, 5230–5240 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Lee, G. J. & Vierling, E. A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol. 122, 189–198 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Shockley, K. R. et al. Heat shock response by the hyperthermophilic archaeon Pyrococcus furiosus. Appl. Environ. Microbiol. 69, 2365–2371 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Leroux, M. R. et al. MtGimC, a novel archaeal chaperone related to the eukaryotic chaperonin cofactor GimC/prefoldin. EMBO J. 18, 6730–6743 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Klunker, D. et al. Coexistence of group I and group II chaperonins in the archaeon Methanosarcina mazei. J. Biol. Chem. 278, 33256–33267 (2003).

    Article  CAS  PubMed  Google Scholar 

  111. Thomsen, J. et al. The basal transcription factors TBP and TFB from the mesophilic archaeon Methanosarcina mazeii: structure and conformational changes upon interaction with stress-gene promoters. J. Mol. Biol. 309, 589–603 (2001).

    Article  CAS  PubMed  Google Scholar 

  112. Galagan, J. E. et al. The genome of M. acetivorans reveals extensive metabolic and physiological diversity. Genome Res. 12, 532–542 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Conway de Macario, E., Maeder, D. L. & Macario, A. J. Breaking the mould: archaea with all four chaperoning systems. Biochem. Biophys. Res. Commun. 301, 811–822 (2003).

    Article  CAS  PubMed  Google Scholar 

  114. Huber, H., Hohn, M. J., Stetter, K. O. & Rachel, R. The phylum Nanoarchaeota: present knowledge and future perspectives of a unique form of life. Res. Microbiol. 154, 165–171 (2003).

    Article  CAS  PubMed  Google Scholar 

  115. 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 

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

    Article  CAS  PubMed  Google Scholar 

  117. Peak, J. G., Ito, T., Robb, F. T. & Peak, M. J. DNA damage produced by exposure of supercoiled plasmid DNA to high- and low-LET ionizing radiation: effects of hydroxyl radical quenchers. Int. J. Radiat. Biol. 67, 1–6 (1995).

    Article  CAS  PubMed  Google Scholar 

  118. Di Ruggiero, J., Santangelo, N., Nackerdien, Z., Ravel, J. & Robb, F. T. Repair of extensive ionizing-radiation DNA damage at 95°C in the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 179, 4643–4645 (1997).

    Article  CAS  Google Scholar 

  119. Forterre, P. & Philippe, H. The last universal common ancestor (LUCA), simple or complex? Biol. Bull. 196, 373–375; discussion 375–377 (1999).

    Article  CAS  PubMed  Google Scholar 

  120. Forterre, P. Genomics and early cellular evolution. The origin of the DNA world. C. R. Acad. Sci. III 324, 1067–1076 (2001).

    Article  CAS  PubMed  Google Scholar 

  121. Nesbo, C. L., Boucher, Y. & Doolittle, W. F. Defining the core of nontransferable prokaryotic genes: the euryarchaeal core. J. Mol. Evol. 53, 340–350 (2001).

    Article  CAS  PubMed  Google Scholar 

  122. Walker, J. E., Saraste, M., Runswick, M. J. & Gay, N. J. Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1, 945–951 (1982). Classic paper recognizing the universal Walker motifs from ATPases and ATP synthases.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Davey, M. J., Jeruzalmi, D., Kuriyan, J. & O'Donnell, M. Motors and switches: AAA+ machines within the replisome. Nature Rev. Mol. Cell. Biol. 3, 826–835 (2002). Thorough summary of the versatile AAA+ proteins, molecular motors powering replication, protein secretion, proteolysis and many other cellular functions.

    Article  CAS  Google Scholar 

  124. Swaffield, J. C., Melcher, K. & Johnston, S. A. A highly conserved ATPase protein as a mediator between acidic activation domains and the TATA-binding protein. Nature 374, 88–91 (1995).

    Article  CAS  PubMed  Google Scholar 

  125. Swaffield, J. C. & Purugganan, M. D. The evolution of the conserved ATPase domain (CAD): reconstructing the history of an ancient protein module. J. Mol. Evol. 45, 549–563 (1997).

    Article  CAS  PubMed  Google Scholar 

  126. Beyer, A. Sequence analysis of the AAA protein family. Protein Sci. 6, 2043–2058 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Maupin-Furlow, J. A., Wilson, H. L., Kaczowka, S. J. & Ou, M. S. Proteasomes in the archaea: from structure to function. Front. Biosci. 5 (Suppl.), D837–D865 (2000).

    CAS  PubMed  Google Scholar 

  128. Imamura, S., Ojima, N. & Yamashita, M. Cold-inducible expression of the cell division cycle gene CDC48 and its promotion of cell proliferation during cold acclimation in zebrafish cells. FEBS Lett. 549, 14–20 (2003).

    Article  CAS  PubMed  Google Scholar 

  129. Schepers, A. & Diffley, J. F. Mutational analysis of conserved sequence motifs in the budding yeast Cdc6 protein. J. Mol. Biol. 308, 597–608 (2001).

    Article  CAS  PubMed  Google Scholar 

  130. Furst, J., Sutton, R. B., Chen, J., Brunger, A. T. & Grigorieff, N. Electron cryomicroscopy structure of N-ethyl maleimide sensitive factor at 11 Å resolution. EMBO J. 22, 4365–4374 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Chen, J. Z., Furst, J., Chapman, M. S. & Grigorieff, N. Low-resolution structure refinement in electron microscopy. J. Struct. Biol. 144, 144–151 (2003).

    Article  PubMed  Google Scholar 

  132. Guo, F., Maurizi, M. R., Esser, L. & Xia, D. Crystal structure of ClpA, an Hsp100 chaperone and regulator of ClpAP protease. J. Biol. Chem. 277, 46743–46752 (2002).

    Article  CAS  PubMed  Google Scholar 

  133. Vainberg, I. E. et al. Prefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperonin. Cell 93, 863–873 (1998).

    Article  CAS  PubMed  Google Scholar 

  134. Fandrich, M. et al. Observation of the noncovalent assembly and disassembly pathways of the chaperone complex MtGimC by mass spectrometry. Proc. Natl Acad. Sci. USA 97, 14151–14155 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Vainberg, I. E. et al. Prefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperonin. Cell 93, 863–873 (1998).

    Article  CAS  PubMed  Google Scholar 

  136. Siegert, R., Leroux, M. R., Scheufler, C., Hartl, F. U. & Moarefi, I. Structure of the molecular chaperone prefoldin: unique interaction of multiple coiled coil tentacles with unfolded proteins. Cell 103, 621–632 (2000). Description of the functions of a classic 'holdase' chaperone in terms of structural analysis.

    Article  CAS  PubMed  Google Scholar 

  137. Robb, F. T. & Laksanalamai, P. Enhanced protein thermostability and temperature resistance. US Patent 6,579,703 (2003).

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Acknowledgements

The authors wish to acknowledge support from the National Science Foundation. We thank J. Mineller for advice concerning the phylogeny of the AAA+ protein family. This is Contribution Number 04-616 from the Center of Marine Biotechnology.

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Authors and Affiliations

  1. Center of Marine Biotechnology, University of Maryland, 701 East Pratt Street, Baltimore, 21202, Maryland, USA

    Pongpan Laksanalamai & Frank T. Robb

  2. Department of Chemical Engineering, University of California, Berkeley, California, USA

    Timothy A. Whitehead

Authors
  1. Pongpan Laksanalamai
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  2. Timothy A. Whitehead
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  3. Frank T. Robb
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Correspondence to Frank T. Robb.

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Related links

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DATABASES

Entrez

Methanosarcina acetivorans

Methanosarcina mazei

Methanothermobacter thermautotrophicus

Nanoarchaeum equitans

Pyrococcus abyssi

Pyrococcus furiosus

Thermoplasma acidophilum

SwissProt

ClpA

ClpP

GrpE

HslU

HslV

Hsp40

Hsp70

α-subunit

β-subunit

The Protein Data Bank

HslU/V

M. jannaschii sHsp

wheat sHSP

FURTHER INFORMATION

Frank T. Robb's laboratory

Glossary

MESOPHILIC

Organisms that have an optimal growth temperature between 20°C and 60°C.

CHAPERONES

A class of proteins that assist in the correct folding of non-native proteins through non-covalent binding. The assignment of a protein as a chaperone is based on its ability to bind non-native proteins — but chaperones vary considerably in their ability to fold proteins. Two types of chaperones, 'holdases' and 'foldases', can be distinguished.

PARALOGY

The relationship between two genes that diverge after a duplication event, as opposed to a speciation event.

SOLFATARIC

Habitats that contain sulphur, and are named after the Solfatara Crater in Italy. Solfataric fields consist of soils, mud holes and surface waters heated by volcanic exhalations from magma chambers a few kilometres below. Solfataric fields are often situated close to active volcanoes.

HYPERTHERMOPHILES

Organisms that have an optimal growth temperature above 80°C.

LATERAL GENE TRANSFER

The transfer of genetic material from one genome to another, specifically between divergent lineages or different species. Also known as horizontal gene transfer.

CDC48

A protein of the AAA+ family of ATPases, required for cell division and homotypic membrane fusion in eukaryotic cells.

BITOROIDAL

A complex that forms a double-ring structure.

PROTOEUKARYOTE

The last common ancestor of eukaryotes, which developed a membrane around its nuclear material.

THERMOPHILIC

A term used to describe organisms that have an optimal growth temperature above 60°C and below 80°C.

CO-CHAPERONE

A protein that increases the efficiency of a chaperone, but which is not able to bind cooperatively to non-native protein structures by itself.

HALOPHILES

Organisms that require hypersaline conditions for growth.

LAST UNIVERSAL COMMON ANCESTOR

(LUCA). The single progenitor from which all current life is thought to have evolved.

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Laksanalamai, P., Whitehead, T. & Robb, F. Minimal protein-folding systems in hyperthermophilic archaea. Nat Rev Microbiol 2, 315–324 (2004). https://doi.org/10.1038/nrmicro866

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