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.

  • Letter
  • Published:

DNA protection by stress-induced biocrystallization

Nature volume 400, pages 83–85 (1999)Cite this article

Abstract

The crystalline state is considered to be incompatible with life. However, in living systems exposed to severe environmental assaults, the sequestration of vital macromolecules in intracellular crystalline assemblies may provide an efficient means for protection. Here we report a generic defence strategy found in Escherichia coli, involving co-crystallization of its DNA with the stress-induced protein Dps1,2. We show that when purified Dps and DNA interact, extremely stable crystals form almost instantaneously, within which DNA is sequestered and effectively protected against varied assaults. Crystalline structures with similar lattice spacings are formed in E. coli in which Dps is slightly over expressed, as well as in starved wild-type bacteria. Hence, DNA–Dps co-crystallization is proposed to represent a binding mode that provides wide-range protection of DNA by sequestration. The rapid induction and large-scale production of Dps in response to stress, as well as the presence of Dps homologues in many distantly related bacteria, indicate that DNA protection by biocrystallization may be crucial and widespread in prokaryotes.

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

Figure 1: Electron microscopy of Dps and Dps–DNA complexes.
Figure 2: In situ DNA–Dps assemblies.

Similar content being viewed by others

References

  1. Kolter, R., Siegele, D. A. & Tormo, A. The stationary phase of bacterial life cycle. Annu. Rev. Microbiol. 47, 855–874 (1993).

    Article  CAS  Google Scholar 

  2. Almiron, M., Link, A. J., Furlong, D. & Kolter, R. Anovel DNA-binding protein with regulatory and protective roles in starved E. coli. Genes Dev. 6, 2646–2654 (1992).

    Article  CAS  Google Scholar 

  3. Altuvia, S., Almiron, M., Huisman, G., Kolter, R. & Storz, G. The dps promoter is activated by OxyR during growth and by IHF and sigma S in stationary phase. Mol. Microbiol. 13, 265–272 (1994).

    Article  CAS  Google Scholar 

  4. Martinez, A. & Kolter, R. Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J. Bacteriol. 179, 5188–5194 (1997).

    Article  CAS  Google Scholar 

  5. Grant, R. A., Filman, D. J., Finkel, S. E., Kolter, R. & Hogle, J. M. The crystal structure of Dps, a ferritin homolog that binds and protects DNA. Nature Struct. Biol. 5, 294–303 (1998).

    Article  CAS  Google Scholar 

  6. Loewen, P. C. & Hengge-Aronis, R. The role of the sigma factor sigma S (KatF) in bacterial global regulation. Annu. Rev. Microbiol. 48, 53–80 (1994).

    Article  CAS  Google Scholar 

  7. Radler, J. O., Koltover, I., Salditt, T. & Safinya, C. R. Structure of DNA-cationic liposome complexes: DNA intercalation in multilamellar membranes in distinct interhelical packing regimes. Science 275, 810–814 (1997).

    Article  CAS  Google Scholar 

  8. Pinsince, J. M. & Griffith, J. D. Early stages in RecA protein-catalyzed pairing. Analysis of coaggregate formation and non-homologous DNA contacts. J. Mol. Biol. 228, 409–420 (1992).

    Article  CAS  Google Scholar 

  9. Tupper, A. E. et al . The chromatin-associated protein H-NS alters DNA topology in vitro. EMBO J. 13, 258–268 (1994).

    Article  CAS  Google Scholar 

  10. Griffith, J., Makhov, A., Santiago, L. L. & Setlow, P. Electron microscopic studies of the interaction between a Bacillus subtilis alpha/beta-type small, acid-soluble spore protein with DNA: protein binding is cooperative, stiffens the DNA, and induces negative supercoiling. Proc. Natl Acad. Sci. USA 91, 8224–8228 (1994).

    Article  ADS  CAS  Google Scholar 

  11. Allen, M. J., Bradbury, E. M. Balhorn, R. AFM analysis of DNA-protamine complexes bound to mica. Nucleic Acids Res. 25, 2221–2226 (1997).

    Article  CAS  Google Scholar 

  12. Bernardin, W. D., Losa, R. & Koller, T. Formation and characterization of soluble complexes of histone H1 with supercoiled DNA. J. Mol. Biol. 189, 503–517 (1986).

    Article  Google Scholar 

  13. Hobot, J. A. et al . Shape and fine structure of nucleoids observed on sections of ultrarapidly frozen and cryosubstituted bacteria. J. Bacteriol. 162, 960–971 (1985).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Flärdh, K., Cohen, P. S. & Kjelleberg, S. Ribosomes exist in large excess over the apparent demand for protein synthesis during carbon starvation in marine Vibrio sp. strain CCUG 15956. J. Bacteriol. 174, 6780–6788 (1992).

    Article  Google Scholar 

  15. Frazier, B. A. et al . Paracrystalline inclusions of a novel ferritin containing nonheme iron, produced by the human gastric pathogen Helicobacter pylori: evidence for a third class of ferritins. J. Bacteriol. 175, 966–972 (1993).

    Article  CAS  Google Scholar 

  16. Evans, D. J., Evans, D. G., Lampert, H. C. & Nakano, H. Identification of four new prokaryotic bacterioferritins, from Helicobacter pylori, Anabaena variabilis, Bacillus subtilis and Treponema pallidum, by analysis of gene sequences. Gene 153, 123–127 (1995).

    Article  CAS  Google Scholar 

  17. Pena, M. M. & Bullerhahn, G. S. The DpsA protein of Synechococcus sp. strain PCC7942 is a DNA-binding hemoprotein. Linkage of the Dps and bacterioferritin protein families. J. Biol. Chem. 270, 22478–22482 (1995).

    Article  CAS  Google Scholar 

  18. Pena, M. M., Burkhart, W. & Bullerhahn, G. S. Purification and characterization of a Synechococcus sp. strain PCC 7942 polypeptide structurally similar to the stress-induced Dps/PexB protein of E. coli. Arch. Microbiol. 163, 337–344 (1995).

    Article  CAS  Google Scholar 

  19. Chen, L. & Helmann, J. D. Bacillus subtilis MrgA is a Dps(PexB) homologue: evidence for metalloregulation of an oxidative-stress gene. Mol. Microbiol. 18, 295–300 (1995).

    Article  CAS  Google Scholar 

  20. Bozzi, M. et al . Anovel non-heme iron-binding ferritin related to the DNA-binding proteins of the Dps family in Listeria innocua. J. Biol. Chem. 272, 3259–3265 (1997).

    Article  CAS  Google Scholar 

  21. Wai, S. N., Nakayama, K., Takade, A. & Amako, K. Overproduction of Campylobacter ferritin in E. coli and induction of paracrystalline inclusion by ferrous compound. Microbiol. Immunol. 41, 461–467 (1997).

    Article  CAS  Google Scholar 

  22. Robinow, C. & Kellenberger, E. The bacterial nucleoid revisited. Microbiol. Rev. 58, 211–232 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from the Consortium of the German Chemical Association. We thank S. Levin-Zidman and E. Shimoni for their help in the electron microscopy studies, and H. Salman for his assistance in the DIC and fluorescence experiments.

Author information

Authors and Affiliations

  1. Departments of Organic Chemistry The Weizmann Institute of Science, Rehovot, 76100, Israel

    Sharon G. Wolf, Daphna Frenkiel, Abraham Minsky & Abraham Minsky

  2. Departments of Structural Biology, The Weizmann Institute of Science, Rehovot, 76100, Israel

    Talmon Arad

  3. Department of Microbiology and Molecular Genetics, Harvard Medical School, 200 Longwood Avenue, Boston, 02115, Massachusetts, USA

    Steven E. Finkel & Roberto Kolter

Authors
  1. Sharon G. Wolf
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daphna Frenkiel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Talmon Arad
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Steven E. Finkel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Roberto Kolter
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Abraham Minsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abraham Minsky.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wolf, S., Frenkiel, D., Arad, T. et al. DNA protection by stress-induced biocrystallization. Nature 400, 83–85 (1999). https://doi.org/10.1038/21918

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/21918

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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