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:

The structure of Desulfovibrio vulgaris rubrerythrin reveals a unique combination of rubredoxin-like FeS4 and ferritin-like diiron domains

Nature Structural Biology volume 3, pages 539–546 (1996)Cite this article

Abstract

We have determined the structure of rubrerythrin, a non-haem iron protein from the anaerobic sulphate-reducing bacterium, Desulfovibrio vulgaris (Hildenborough), by X-ray crystallography. The structure reveals a tetramer of two-domain subunits. Each subunit contains a four-helix bundle surrounding a diiron-oxo site and a C-terminal rubredoxin-like FeS4 domain. The diiron-oxo site contains a larger number of carboxylate ligands and a higher degree of solvent exposure than do those in other diiron-oxo proteins. The four-helix bundle of rubrerythrin closely resembles those of the ferritin and bacterioferritin subunits, suggesting a relationship among these proteins—consistent with the recently demonstrated ferroxidase activity of rubrerythrin.

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. Moura, I., Tavares, P. & Ravi, N. Characterization of 3 proteins containing multiple iron sites - Rubrerythrin, desulforedoxin, and a protein containing a six-iron cluster. Meth. Enz. 243, 216–240 (1994).

    Article  CAS  Google Scholar 

  2. Dave, B.C., Czernuszewicz, R.S., Prickril, B.C. & Kurtz, D.M., Jr. Resonance raman spectroscopic evidence for the FeS4 and Fe-O-Fe sites in rubrerythrin from Desulfovibrio vulgaris. Biochemistry 33, 3572–3576 (1994).

    Article  CAS  Google Scholar 

  3. Ravi, N., Prickril, B.C., Kurtz, D.M., Jr & Huynh, B.H. Spectroscopic characterization of 57Fe-reconstituted rubrerythrin, a non-heme iron protein with structural analogies to ribonucleotide reductase. Biochemistry 32, 8487–8491 (1993).

    Article  CAS  Google Scholar 

  4. Pierik, A.J., Wolbert, R.B.G., Portier, G.L., Verhagen, M.F.J.M. & Hagen, W.R. Nigerythrin and rubrerythrin from Desulfovibrio vulgaris each contain 2 mononuclear iron centers and 2 dinuclear iron clusters. European Journal of Biochemistry 212, 237–245 (1993).

    Article  CAS  Google Scholar 

  5. Gupta, N. et al. Recombinant Desulfovibrio vulgaris rubrerythrin. Isolation and characterization of the diiron domain. Biochemistry 34, 3310–3318 (1995).

    Article  CAS  Google Scholar 

  6. Prickril, B.C., Kurtz, D.M., Jr. LeGall, J. & Voordouw, G. Cloning and sequencing of the gene for Rubrerythrin from Desulfovibrio vulgaris (Hildenborough). Biochemistry 30, 11118–11123 (1991).

    Article  CAS  Google Scholar 

  7. Kurtz, D.M., & Prickril, B.C. Intrapeptide sequence homology in rubrerythrin from Desulfovibrio vulgaris: Identification of potential ligands to the diiron site. Biochemical and Biophysical Research Communications 181, 337–341 (1991).

    Article  CAS  Google Scholar 

  8. Nordlund, P. & Eklund, H. Di-iron-carboxylate proteins. Current Opinion in Structural Biology 5, 758–766 (1995).

    Article  CAS  Google Scholar 

  9. Rosenzweig, A.C., Frederick, C.A., Lippard, S.J. & Nordlund, P. Crystal structure of a bacterial non-haem iron hydroxylase that catalyses the biological oxidation of methane. Nature 366, 537–543 (1993).

    Article  CAS  Google Scholar 

  10. Rosenzweig, A.C., Nordlund, P., Takahara, P.M., Frederick, C.A. & Lippard, S.J. Geometry of the soluble methane monooxygenase catalytic diiron center in two oxidation states. Chemistry & Biology 2, 409–418 (1995).

    Article  CAS  Google Scholar 

  11. Nordlund, P., Sjöberg, B.-M. & Eklund, H. Three dimensional structure of the free radical protein of ribonucleotide reductase. Nature 345, 593–598 (1990).

    Article  CAS  Google Scholar 

  12. Nordlund, P. & Eklund, H. Structure and function of the Escherichia coli ribonucleotide reductase protein R2. J. Mol. Biol. 231, 123–164 (1993).

    Article  Google Scholar 

  13. Widell, L.C. & Hansen, T.A. The dissimilatory sulphate-reducing and sulfur-reducing bacteria. in The Prokaryotes (eds. A. Balows, H.G. Dworkin, W. Harder, & K.H. Schleifer) 583–624 (Springer-Verlag, New York, 1992).

    Google Scholar 

  14. Liu, M.Y. & LeGall, J. Purification and characterization of two proteins with inorganic pyrophosphatase activity from Desulfovibrio vulgaris: Rubrerythrin and a new, highly active, enzyme. Biochem. Biophys. Res. Commun. 171, 316–318 (1990).

    Google Scholar 

  15. Feig, A.L. & Lippard, S.J. Reactions of non-heme iron (II)centers with dioxygen in biology and chemistry. Chemical Reviews 94, 759–805 (1994).

    Article  CAS  Google Scholar 

  16. Kurtz, D.M., Jr. Iron: Proteins with dinuclear active sites in Encyclopedia of Inorganic Chemistry (ed. King, R.B.) 1847–1859 (Wiley, Chichester, UK, 1994).

    Google Scholar 

  17. Stenkamp, R.E. Dioxygen and hemerythrin. Chemical Reviews 94, 715–726 (1994).

    Article  CAS  Google Scholar 

  18. Fox, B.C., Shanklin, J., Ai, J., Loehr, T.M. & Sanders-Loehr, J. Resonance Raman evidence for anFe-O-Fe center in stearoyl-ACP destaurase. Primary sequence identity with other diiron-oxo proteins. Biochemistry 33, 12776–12786 (1994).

    Article  CAS  Google Scholar 

  19. Harrison, P. & Lilley, T.H. Ferritin in Iron Carriers and Iron Proteins (ed. ^(eds. Loehr, T.M.) 123–237 (VCH Publishers, New York, 1989).

    Google Scholar 

  20. Hempstead, P.D. et al. Direct observation of the iron binding sites in a ferritin. FEBS Letters 350, 258–262 (1994).

    Article  CAS  Google Scholar 

  21. Frolow, F., Kalb(Gilboa), J. & Yariv, J. Structure of a unique two-fold symmetric haem-binding site. Nature Struct. Biology 1, 453–460 (1994).

    Article  CAS  Google Scholar 

  22. Bonomi, F., Kurtz Donald, M., Jr. & Cui, Xizoyuan. Ferroxidase activity of recombinant Desulfovibrio vulgaris rubrerythrin. J. Inorg. Biochem. 1, 69–72 (1996).

    Google Scholar 

  23. Sieker, L.C., Turley, S., Prickril, B.C. & LeGall, J. Crystallisation and preliminary X-ray diffraction study of a protein with a high potential rubredoxin center and a hemerythrin-type Fe center. Proteins: Struct., Funct. Genets 3, 184–186 (1988).

    Article  CAS  Google Scholar 

  24. Kurtz, D.M., Jr. Oxo- and hydroxo-bridged diiron complexes: A chemical perspective on a biological unit. Chemical Reviews 90, 585–606 (1990).

    Article  CAS  Google Scholar 

  25. Sieker, L.C., Stenkamp, R.E. & LeGall, J. Rubredoxin in Crystalline State in Meth Enzymol. 243, 203–216 (1994).

    Article  CAS  Google Scholar 

  26. Day, M.W. et al. X-ray crystal structures of the oxidized and reduced forms of rubredoxin from the marine hyperthermophilic archaebacterium Pyrococcus furiousus. Prot. Sci. 1, 1494–1507 (1992).

    Article  CAS  Google Scholar 

  27. Adman, E., Watenbaugh, K.D. & Jensen, L.H. NH⋯Hydrogen bonds in Peptococcus aerogenes ferredoxin, Clostridium pasteurianum rubredoxin, and Chromatium vinosum high potential iron protein. Proc. Nat. Acad. Sci. USA 72, 4854–4858 (1975).

    Article  CAS  Google Scholar 

  28. Holm, L. & Sander, C. Dali: A network tool for protein structure comparison. Trends in Biochemical Sciences 20, 478–480 (1995).

    Article  CAS  Google Scholar 

  29. Andrews, S.C., Smith, J.M.A., Yewdall, S.J., Guest, J.R. & Harrison, P.M. Bacterioferritins and ferritins are distantly related in evolution. FEBS Letters 293, 164–168 (1991).

    Article  CAS  Google Scholar 

  30. Lawson, D.M. et al. Identification of the ferroxidase centre in ferritin. FEBS Letters 254, 207–210 (1989).

    Article  CAS  Google Scholar 

  31. Bauminger, E.R. et al. lron(II)oxidation and early intermediates of iron-core formation in recombinant human H-chain ferritin. Biochem. J. 296, 709–719 (1993).

    Article  CAS  Google Scholar 

  32. Treffry, A., Zhao, Z., Quail, M.A., Guest, J.R. & Harrison, P.M. Iron(II) Oxidation by H chain ferritin: Evidence from site-directed mutagenesis that a transient blue species is formed at the dinuclear iron center. Biochemistry 34, 15204–15213 (1995).

    Article  CAS  Google Scholar 

  33. Chen-Barrett, Y. et al. Tyrosyl radical formation during the oxidative deposition if iron in human apoferritin. Biochemistry 34, 7847–7853 (1995).

    Article  CAS  Google Scholar 

  34. Yoshida, K. et al. A mutation in the ceruloplasmin gene is associated with systemic hemosiderosis in humans. Nature Genetics 9, 267–273 (1995).

    Article  CAS  Google Scholar 

  35. Kabsch, W.J. Automatic Processing of Rotation diffraction Data from Crystals of Initially Unknown Symmetry and Cell Constants. J. of Appl Crystallogr. 26, 795–800 (1993).

    Article  CAS  Google Scholar 

  36. Collaborative Computational Project, N.4. The CCP4 suite: Programs for protein crystallography. Acta Crystallographica D50, 760–763 (1994).

  37. Otwinowski, Z. in CCP4 Proceedings 80–88 (Daresbury Laboratories, Warrington, UK, 1991).

    Google Scholar 

  38. Brünger, T.A., Kuriyan, J. & Karplus, M. Crystallographic R Factor refinement by molecular dynamics. Science 235, 458–460 (1987).

    Article  Google Scholar 

  39. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard, M. Improved methods for the building of protein models in electron density maps and the location of errors in these models. Acta Crystallographica A47, 110–119 (1991).

    Article  CAS  Google Scholar 

  40. Lawson, D.M. et al. Solving the structure of human H ferritin by genetically engineered intermolecular crystal contacts. Nature 349, 541–544 (1991).

    Article  CAS  Google Scholar 

  41. Bernstein, F.C. et al. The protein data bank: a computer-based archival file for macromolecular structures. J. Mol. Biol. 112, 535–542 (1977).

    Article  CAS  Google Scholar 

  42. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. PROCHECK: A Program to Check the Stereochemical Quality of Protein Structures. Journal of Appl. Crystallogr. 26, 283–291 (1993).

    Article  CAS  Google Scholar 

  43. Kraulis, P.J. MOLSCRIPT: A Program to Produce Both Detailed and Schematic Plots of Protein Structures. J. of Appl. Crystallogr. 24, 946–950 (1991).

    Article  Google Scholar 

  44. Merritt, E.A. & Murphy, M.E.P. Raster3D Version 2.0: A Program for Photorealistic Molecular Graphics. Acta Crystallographica D50, 869–873 (1994).

    CAS  Google Scholar 

  45. Nicholls, A., Sharp, K.A. & Honig, B. Protein folding and association: Insights into the interracial and thermodynamic properties of hydrocarbons. PROTEINS 11, 281–296 (1991).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Biology, Stockholm University, 106 91, Stockholm, Sweden

    Fredrick deMaré & Pär Nordlund

  2. Department of Chemistry and Center for Metalloenzyme Studies, University of Georgia, Athens, Georgia, 30602, USA

    Donald M. Kurtz Jr

Authors
  1. Fredrick deMaré
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Donald M. Kurtz Jr
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pär Nordlund
    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

deMaré, F., Kurtz, D. & Nordlund, P. The structure of Desulfovibrio vulgaris rubrerythrin reveals a unique combination of rubredoxin-like FeS4 and ferritin-like diiron domains. Nat Struct Mol Biol 3, 539–546 (1996). https://doi.org/10.1038/nsb0696-539

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nsb0696-539

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