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.

  • Article
  • Published:

Solution structure and DNA-binding properties of a thermostable protein from the archaeon Sulfolobus solfataricus

Nature Structural Biology volume 1, pages 808–819 (1994)Cite this article

Abstract

The archaeon Sulfolobus solfataricus expresses large amounts of a small basic protein, Sso7d, which was previously identified as a DNA-binding protein possibly involved in compaction of DNA. We have determined the solution structure of Sso7d. The protein consists of a triple-stranded anti-parallel β-sheet onto which an orthogonal double-stranded β-sheet is packed. This topology is very similar to that found in eukaryotic Src homology-3 (SH3) domains. Sso7d binds strongly (Kd < 10 μM) to double-stranded DNA and protects it from thermal denaturation. In addition, we note that ɛ-mono-methylation of lysine side chains of Sso7d is governed by cell growth temperatures, suggesting that methylation is related to the heat-shock response.

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

Similar content being viewed by others

References

  1. Kornberg, R. & Lorch, Y. Chromatin structure and transcription. A. Rev. Cell. Biol. 8, 563–587 (1992).

    Article  CAS  Google Scholar 

  2. Schmid, M.B. More than just “histone-like” proteins. Cell 63, 451–453 (1990).

    Article  CAS  Google Scholar 

  3. Dijk, J. & Reinhardt, R. The structure of DNA-binding proteins from eu and archaebacteria. In Bacterial chromatin (Eds, Gualerzi, C.O. and Pon, C.L.) 185–218, (Springer-Verlag, Berlin, 1986)

    Chapter  Google Scholar 

  4. Pettijohn, D. Histone-like proteins and bacterial chromosome structure. J. biol. Chem. 236, 12793–12796 (1988).

    Google Scholar 

  5. Drlica, K. & Rouviere-Yaniv, J. Histonelike proteins in bacteria. Microbiol. Rev. 51, 301–319 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Grayling, R.A., Sandman, K. & Reeve, J.N. Archaeal DNA binding proteins and chromosome structure. System. appl. Micobiol. 16, 582–590 (1994).

    Article  CAS  Google Scholar 

  7. 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. 84, 54–68 (1972).

    Article  CAS  Google Scholar 

  8. Thomm, M., Stetter, K.O. & Zillig, W. Histone-like proteins in eu and archaebacteria. Zentralbl. Bakteriol. Mikrobiol. Hyg., I. Abt. Orig. C 3, 128–139 (1982).

    CAS  Google Scholar 

  9. Kimura, M., Kimura, J., Davie, P., Reinhardt, R. & Dijk, J. The amino acid sequence of a small DNA binding protein from the archaebacterium Sulfolobus solfataricus. FEBS Letts. 176, 176–178 (1984).

    Article  CAS  Google Scholar 

  10. Grote, M., Dijk, J. & Reinhardt, R. Ribosomal and DNA binding proteins of the thermoacidophilic archaebacterium Sulfolobus acidocaldarius. Biochim. biophys. Acta 873, 405–413 (1986).

    Article  CAS  Google Scholar 

  11. Choli, T., Wittmann-Liebold, B. & Reinhardt, R. Microsequence analysis of DNA-binding proteins 7a, 7b and 7e from the archaebacterium Sulfolobus acidocaldarius. J. biol. Chem. 263, 7087–7093 (1988).

    CAS  PubMed  Google Scholar 

  12. Choli, T., Henning, P., Wittmann-Liebold, B. & Reinhardt, R. Isolation, characterization and microsequence analysis of a small basic methylated DNA-binding protein from the archaebacterium Sulfolobus solfataricus. Biochim. biophys. Acta 950, 193–203 (1988).

    Article  CAS  Google Scholar 

  13. Saraste, M., Sibbald, P.R. & Wittinghofer, A., The P-loop - a common motif in ATP- and GTP-binding proteins. Trends biochem. Sci 15, 430–434 (1990).

    Article  Google Scholar 

  14. Guagliardi, A., Cerchia, L., Camardella, L., Rossi, M. & Bartolucci, S. DBF (disulfide bond forming) enzyme from the hyperthermophilic archaebacterium Sulfolobus solfataricus behaves like a molecular chaperone. Biocatalysis (in the press)

  15. Fusi, P., Tedeschi, G., Aliverti, A., Ronchi, S., Tortora, P. & Guerritore, P. Ribonucleases from the extreme thermophilic archaebacterium S. solfataricus. Eur. J. Biochem. 211, 305–310 (1993).

    Article  CAS  Google Scholar 

  16. Jentoft, N. & Dearborn, D. Protein labeling by reductive alkylation. Meths. Enzymol. 91, 570–579 (1983).

    Article  CAS  Google Scholar 

  17. Stein, D.B. & Searcy, D.G. Physiologically important stabilization of DNA by a prokaryotic histone-like protein. Science 202, 219–221 (1978).

    Article  CAS  Google Scholar 

  18. Wüthrich, K. NMR of proteins and nucleic acids. (Wiley, New York, 1986)

    Book  Google Scholar 

  19. Bax, A. Two-dimensional NMR and protein structure. A. Rev. Biochem. 58, 223–256 (1989).

    Article  CAS  Google Scholar 

  20. Pawson, T. & Schlessinger, J. SH2 and SH3 domains. Curr. Biol. 3, 434–442 (1993).

    Article  CAS  Google Scholar 

  21. Kuriyan, J. & Cowburn, D. Structures of SH2 and SH3 domains. Curr. Opin. struct. Biol. 3, 828–837 (1993).

    Article  CAS  Google Scholar 

  22. Koyama, S. et al. Structure of the P13K SH3 domain and analysis of the SH3 family. Cell 72, 945–952 (1993).

    Article  CAS  Google Scholar 

  23. Musacchio, A., Noble, M., Pauptit, R., Wierenga, R. & Saraste, M. Crystal structure of a src-homology 3 (SH3) domain. Nature 359, 851–855 (1992).

    Article  CAS  Google Scholar 

  24. Noble, M.E.M., Musacchio, A., Saraste, M., Courtneidge, S.A. & Wierenga, R.K. Crystal structure of the SH3 domain in human Fyn; comparison of the three-dimansional structures of SH3 domains in tyrosine kinases and spectrin. EMBO J. 12, 2617–2624 (1993).

    Article  CAS  Google Scholar 

  25. Falzone, C.J., Kao, Y.-H., Zhao, J., Bryant, D.A. & Lecomte, J.T.J. Three-dimensional solution structure of PsaE from the cyanobacterium Synechococcus sp. strain PCC 7002, a photosystem I protein that shows structural homology with SH3 domains. Biochemistry 33, 6052–6062 (1994).

    Article  CAS  Google Scholar 

  26. Wilson, K.P., Shewchuk, L.M., Brennan, R.G., Otsuka, J. & Matthews, B.W. Eschericia coli biotin holoenzyme synthetase/bio repressor crystal structure delineates the biotin- and DNA-binding domains. Proc. natn. Acad. Sci. U.S.A. 89, 9257–9261 (1992).

    Article  CAS  Google Scholar 

  27. Zillig, W. et al. The sulfolobus-“Caldariella” group: taxonomy on the basis of the structure of DNA-dependent RNA polymerase. Arch. Microbiol. 125, 259–269 (1980).

    Article  CAS  Google Scholar 

  28. Cantor, C.R., Schimmel, P. Biophysical chemistry. Part II, Chapter 7, (Freeman, San Francisco, 1980)

    Google Scholar 

  29. Lundbäck, T., Zilliacus, J., Gustafsson, J.-Å., Carlstedt-Duke, J. & Härd, T. Thermodynamics of sequence-specific glucocorticoid receptor-DNA interactions. Biochemistry 33, 5955–5965 (1994).

    Article  Google Scholar 

  30. States, D.J., Haberkorn, R.A. & Ruben, R.J. A 2D NMR experiment with pure absorption phase in four quadrants. J. magn. Reson. 48, 286–295 (1982).

    CAS  Google Scholar 

  31. Rance, M. et al. Improved spectral resolution in COSY 1H NMR spectra of proteins via double quantum coherence. Biochem biophys. Res. Comm. 117, 479–485 (1983).

    Article  CAS  Google Scholar 

  32. Macura, A. & Ernst, R.R. Elucidation of crossrelaxation in liquids by 2D NMR spectroscopy. Molec. Phys. 41, 95–117 (1980).

    Article  CAS  Google Scholar 

  33. Griesinger, C., Otting, G., Wüthrich, K. & Ernst, R.R. Clean TOCSY for 1H spin system identification in macromolecules. J. Am. chem. Soc. 110, 7870–7872 (1988).

    Article  CAS  Google Scholar 

  34. Davis, A.L., Keeler, J., Laue, E.D. & Moskau, D. Experiments for recording pure-absorption heteronuclear correlation spectra using pulsed field gradients. J. magn. Reson. 98, 207–216 (1992).

    CAS  Google Scholar 

  35. Smallcombe, S.H. Solvent suppression with symmetrically-shifted pulses. J. Am. chem. Soc. 115, 4776–4785 (1993).

    Article  CAS  Google Scholar 

  36. Patt, S.L. Single- and multiple-frequency-shifted laminar pulses. J. magn Reson. 96, 94–102 (1992).

    CAS  Google Scholar 

  37. Brown, S.C., Weber, P.L. & Mueller, L. Toward complete 1H NMR spectra in proteins. J. magn. Reson. 77, 166–169 (1988).

    CAS  Google Scholar 

  38. Kraulis, P.J. ANSIG: a program for the assignment of protein 1H 2D NMR spectra by interactive computer graphics. J. magn. Reson. 84, 627–633 (1989).

    CAS  Google Scholar 

  39. Hyberts, S., Märki, W. & Wagner, G. Stereospecific assignments of side-chain protons and characterization of torsion angles in eglin c. Eur. J. Biochem. 164, 625–635 (1987).

    Article  CAS  Google Scholar 

  40. Cavanagh, J., Chazin, W. & Rance, M. The time dependence of coherence transfer in homonuclear isotropic mixing experiments. J. magn. Reson. 87, 110–131 (1990).

    CAS  Google Scholar 

  41. Zuiderweg, E.R.P., Boelens, R. & Kaptein, R. Stereospecific assignments of 1H-NMR methyl lines and conformation of valyl residues in the lac repressor headpiece. Biopolymers 24, 601–611 (1985).

    Article  CAS  Google Scholar 

  42. Bartik, K. & Redfield, C. A method for the estimation of χ1 torsion angles in proteins. J. biol. NMR 3, 415–428 (1993).

    Article  CAS  Google Scholar 

  43. Koning, T.M.G., Boelens, R. & Kaptein, R. Calculation of the nuclear Overhauser effect and the determination of proton-proton distances in the presence of internal motions. J. magn. Reson. 90, 111–123 (1990).

    CAS  Google Scholar 

  44. Nilges, M., Gronenborn, A.M., Brünger, A.T. & Clore, G.M. Determination of three-dimensional structures of proteins by simulated annealing with interproton distance restraints. Application to crambin, potato carboxypeptidase inhibitor and barley serine protease inhibitor 2. Prot. Engng. 2, 27–38 (1988).

    Article  CAS  Google Scholar 

  45. Brünger, A.T. X-PLOR manual. Version 3.0 (Yale University, New Haven, Connecticut, 1992).

    Google Scholar 

  46. Hyberts, S.G., Goldberg, M.S., Havel, T.F. & Wagner, G. The solution structure of eglin c based on measurements of many NOEs and coupling constants and its comparison with X-ray structures. Prot. Sci. 1, 736–751 (1992).

    Article  CAS  Google Scholar 

  47. Brooks, B.R. et al. CHARMM: a program for macromolecular energy, minimization and dynamics calculations. J. comput. Chem. 4, 187–217 (1983).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Center for Structural Biochemistry, Karolinska Institutet, NOVUM, S-141 57, Huddinge, Sweden

    Herbert Baumann, Stefan Knapp, Thomas Lundbäck, Rudolf Ladenstein & Torleif Härd

Authors
  1. Herbert Baumann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefan Knapp
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas Lundbäck
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rudolf Ladenstein
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Torleif Härd
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baumann, H., Knapp, S., Lundbäck, T. et al. Solution structure and DNA-binding properties of a thermostable protein from the archaeon Sulfolobus solfataricus. Nat Struct Mol Biol 1, 808–819 (1994). https://doi.org/10.1038/nsb1194-808

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nsb1194-808

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

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