Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1990 Mar;172(3):1478–1484. doi: 10.1128/jb.172.3.1478-1484.1990

Acquired thermotolerance and heat shock in the extremely thermophilic archaebacterium Sulfolobus sp. strain B12.

J D Trent 1, J Osipiuk 1, T Pinkau 1
PMCID: PMC208623  PMID: 2106513

Abstract

The extreme thermophile Sulfolobus sp. strain B12 exhibits an acquired thermotolerance response. Thus, survival of cells from a 70 degrees C culture at the lethal temperature of 92 degrees C was enhanced by as much as 6 orders of magnitude over a 2-h period if the culture was preheated to 88 degrees C for 60 min or longer before being exposed to the lethal temperature. In eubacteria and eucaryotes, acquired thermotolerance correlates with the induced synthesis of a dozen or so proteins known as heat shock proteins. In this Sulfolobus species, it correlates with the preferential synthesis of primarily one major protein (55 kilodaltons) and, to a much lesser extent, two minor proteins (28 and 35 kilodaltons). Since the synthesis of all other proteins was radically reduced and these proteins were apparently not degraded or exported, their relative abundance within the cell increased during the time the cells were becoming thermotolerant. They could not yet be related to known heat shock proteins. In immunoassays, they were not cross-reactive with antibodies against heat shock proteins from Escherichia coli (DnaK and GroE), which are highly conserved between eubacteria and eucaryotes. However, it appears that if acquired thermotolerance depends on the synthesis of protective proteins, then in this extremely thermophilic archaebacterium it depends primarily on one protein.

Full text

PDF
1478

Images in this article

1480FIG. 2
on p.1480
1481FIG. 3
on p.1481
1482FIG. 4
on p.1482

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bardwell J. C., Craig E. A. Major heat shock gene of Drosophila and the Escherichia coli heat-inducible dnaK gene are homologous. Proc Natl Acad Sci U S A. 1984 Feb;81(3):848–852. doi: 10.1073/pnas.81.3.848. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bochkareva E. S., Lissin N. M., Girshovich A. S. Transient association of newly synthesized unfolded proteins with the heat-shock GroEL protein. Nature. 1988 Nov 17;336(6196):254–257. doi: 10.1038/336254a0. [DOI] [PubMed] [Google Scholar]
  3. Bosch T. C., Krylow S. M., Bode H. R., Steele R. E. Thermotolerance and synthesis of heat shock proteins: these responses are present in Hydra attenuata but absent in Hydra oligactis. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7927–7931. doi: 10.1073/pnas.85.21.7927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brock T. D., Brock K. M., Belly R. T., Weiss R. L. Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch Mikrobiol. 1972;84(1):54–68. doi: 10.1007/BF00408082. [DOI] [PubMed] [Google Scholar]
  5. Carper S. W., Duffy J. J., Gerner E. W. Heat shock proteins in thermotolerance and other cellular processes. Cancer Res. 1987 Oct 15;47(20):5249–5255. [PubMed] [Google Scholar]
  6. Chamberlain J. P. Fluorographic detection of radioactivity in polyacrylamide gels with the water-soluble fluor, sodium salicylate. Anal Biochem. 1979 Sep 15;98(1):132–135. doi: 10.1016/0003-2697(79)90716-4. [DOI] [PubMed] [Google Scholar]
  7. Cheng M. Y., Hartl F. U., Martin J., Pollock R. A., Kalousek F., Neupert W., Hallberg E. M., Hallberg R. L., Horwich A. L. Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature. 1989 Feb 16;337(6208):620–625. doi: 10.1038/337620a0. [DOI] [PubMed] [Google Scholar]
  8. Daniels C. J., McKee A. H., Doolittle W. F. Archaebacterial heat-shock proteins. EMBO J. 1984 Apr;3(4):745–749. doi: 10.1002/j.1460-2075.1984.tb01878.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Deshaies R. J., Koch B. D., Werner-Washburne M., Craig E. A., Schekman R. A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature. 1988 Apr 28;332(6167):800–805. doi: 10.1038/332800a0. [DOI] [PubMed] [Google Scholar]
  10. Gerner E. W., Schneider M. J. Induced thermal resistance in HeLa cells. Nature. 1975 Aug 7;256(5517):500–502. doi: 10.1038/256500a0. [DOI] [PubMed] [Google Scholar]
  11. Hall B. G. Yeast thermotolerance does not require protein synthesis. J Bacteriol. 1983 Dec;156(3):1363–1365. doi: 10.1128/jb.156.3.1363-1365.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Johnston R. N., Kucey B. L. Competitive inhibition of hsp70 gene expression causes thermosensitivity. Science. 1988 Dec 16;242(4885):1551–1554. doi: 10.1126/science.3201244. [DOI] [PubMed] [Google Scholar]
  13. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  14. Laszlo A., Li G. C. Heat-resistant variants of Chinese hamster fibroblasts altered in expression of heat shock protein. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8029–8033. doi: 10.1073/pnas.82.23.8029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Laszlo A. The relationship of heat-shock proteins, thermotolerance, and protein synthesis. Exp Cell Res. 1988 Oct;178(2):401–414. doi: 10.1016/0014-4827(88)90409-0. [DOI] [PubMed] [Google Scholar]
  16. Li G. C., Werb Z. Correlation between synthesis of heat shock proteins and development of thermotolerance in Chinese hamster fibroblasts. Proc Natl Acad Sci U S A. 1982 May;79(10):3218–3222. doi: 10.1073/pnas.79.10.3218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lindquist S., Craig E. A. The heat-shock proteins. Annu Rev Genet. 1988;22:631–677. doi: 10.1146/annurev.ge.22.120188.003215. [DOI] [PubMed] [Google Scholar]
  18. Minton K. W., Karmin P., Hahn G. M., Minton A. P. Nonspecific stabilization of stress-susceptible proteins by stress-resistant proteins: a model for the biological role of heat shock proteins. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7107–7111. doi: 10.1073/pnas.79.23.7107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mizzen L. A., Welch W. J. Characterization of the thermotolerant cell. I. Effects on protein synthesis activity and the regulation of heat-shock protein 70 expression. J Cell Biol. 1988 Apr;106(4):1105–1116. doi: 10.1083/jcb.106.4.1105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Neidhardt F. C., VanBogelen R. A., Vaughn V. The genetics and regulation of heat-shock proteins. Annu Rev Genet. 1984;18:295–329. doi: 10.1146/annurev.ge.18.120184.001455. [DOI] [PubMed] [Google Scholar]
  21. Pelham H. R. Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell. 1986 Sep 26;46(7):959–961. doi: 10.1016/0092-8674(86)90693-8. [DOI] [PubMed] [Google Scholar]
  22. Plesset J., Palm C., McLaughlin C. S. Induction of heat shock proteins and thermotolerance by ethanol in Saccharomyces cerevisiae. Biochem Biophys Res Commun. 1982 Oct 15;108(3):1340–1345. doi: 10.1016/0006-291x(82)92147-7. [DOI] [PubMed] [Google Scholar]
  23. Riabowol K. T., Mizzen L. A., Welch W. J. Heat shock is lethal to fibroblasts microinjected with antibodies against hsp70. Science. 1988 Oct 21;242(4877):433–436. doi: 10.1126/science.3175665. [DOI] [PubMed] [Google Scholar]
  24. Thole J. E., Hindersson P., de Bruyn J., Cremers F., van der Zee J., de Cock H., Tommassen J., van Eden W., van Embden J. D. Antigenic relatedness of a strongly immunogenic 65 kDA mycobacterial protein antigen with a similarly sized ubiquitous bacterial common antigen. Microb Pathog. 1988 Jan;4(1):71–83. doi: 10.1016/0882-4010(88)90049-6. [DOI] [PubMed] [Google Scholar]
  25. VanBogelen R. A., Acton M. A., Neidhardt F. C. Induction of the heat shock regulon does not produce thermotolerance in Escherichia coli. Genes Dev. 1987 Aug;1(6):525–531. doi: 10.1101/gad.1.6.525. [DOI] [PubMed] [Google Scholar]
  26. Woese C. R., Olsen G. J. Archaebacterial phylogeny: perspectives on the urkingdoms. Syst Appl Microbiol. 1986;7:161–177. doi: 10.1016/s0723-2020(86)80001-7. [DOI] [PubMed] [Google Scholar]
  27. Yamamori T., Yura T. Genetic control of heat-shock protein synthesis and its bearing on growth and thermal resistance in Escherichia coli K-12. Proc Natl Acad Sci U S A. 1982 Feb;79(3):860–864. doi: 10.1073/pnas.79.3.860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Zale S. E., Klibanov A. M. Why does ribonuclease irreversibly inactivate at high temperatures? Biochemistry. 1986 Sep 23;25(19):5432–5444. doi: 10.1021/bi00367a014. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES