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Distorted octahedral coordination of tungstate in a subfamily of specific binding proteins

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Abstract

Bacteria and archaea import molybdenum and tungsten from the environment in the form of the oxyanions molybdate (MoO4 2−) and tungstate (WO4 2−). These substrates are captured by an external, high-affinity binding protein, and delivered to ATP binding cassette transporters, which move them across the cell membrane. We have recently reported a crystal structure of the molybdate/tungstate binding protein ModA/WtpA from Archaeoglobus fulgidus, which revealed an octahedrally coordinated central metal atom. By contrast, the previously determined structures of three bacterial homologs showed tetracoordinate molybdenum and tungsten atoms in their binding pockets. Until then, coordination numbers above four had only been found for molybdenum/tungsten in metalloenzymes where these metal atoms are part of the catalytic cofactors and coordinated by mostly non-oxygen ligands. We now report a high-resolution structure of A. fulgidus ModA/WtpA, as well as crystal structures of four additional homologs, all bound to tungstate. These crystal structures match X-ray absorption spectroscopy measurements from soluble, tungstate-bound protein, and reveal the details of the distorted octahedral coordination. Our results demonstrate that the distorted octahedral geometry is not an exclusive feature of the A. fulgidus protein, and suggest distinct binding modes of the binding proteins from archaea and bacteria.

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Abbreviations

ABC:

ATP binding cassette

AfModA:

Archaeoglobus fulgidus ModA/WtpA

EXAFS:

Extended X-ray absorption fine structure

MaModA:

Methanosarcina acetivorans ModA/WtpA

MjModA:

Methanocaldococcus jannaschii ModA/WtpA

PEG:

Poly(ethylene glycol)

PfModA:

Pyrococcus furiosus ModA/WtpA

PhModA:

Pyrococcus horikoshii ModA/WtpA

Tris:

Tris(hydroxymethyl)aminomethane

References

  1. Hille R (2002) Trends Biochem Sci 27:360–367

    Article  PubMed  CAS  Google Scholar 

  2. Johnson MK, Rees DC, Adams MW (1996) Chem Rev 96:2817–2840

    Article  PubMed  CAS  Google Scholar 

  3. Holland IB, Cole SPC, Kuchler K, Higgins CF (eds) (2003) ABC proteins: from bacteria to man. Academic Press, London

    Google Scholar 

  4. Quiocho FA, Ledvina PS (1996) Mol Microbiol 20:17–25

    Article  PubMed  CAS  Google Scholar 

  5. Wilkinson AJ, Verschueren KHG (2003) In: Holland IB, Cole SPC, Kuchler K, Higgins CF (eds) ABC proteins: from bacteria to man. Academic Press, London, pp 187–207

  6. Hollenstein K, Frei DC, Locher KP (2007) Nature 446:213–216

    Article  PubMed  CAS  Google Scholar 

  7. Bevers LE, Hagedoorn PL, Krijger GC, Hagen WR (2006) J Bacteriol 188:6498–6505

    Article  PubMed  CAS  Google Scholar 

  8. Hu Y, Rech S, Gunsalus RP, Rees DC (1997) Nat Struct Biol 4:703–707

    Article  PubMed  CAS  Google Scholar 

  9. Lawson DM, Williams CE, Mitchenall LA, Pau RN (1998) Structure 6:1529–1539

    Article  PubMed  CAS  Google Scholar 

  10. Balan A, Santacruz-Perez C, Moutran A, Ferreira LC, Neshich G, Goncalves Barbosa JA (2008) Biochim Biophys Acta 1784:393–399

    PubMed  CAS  Google Scholar 

  11. Strange RW, Feiters MC (2008) Curr Opin Struct Biol 18:609–616

    Article  PubMed  CAS  Google Scholar 

  12. Otwinowski Z, Minor W, Carter CW Jr (1997) Methods Enzymol 276:307–326

    Article  CAS  Google Scholar 

  13. Kabsch W (1993) J Appl Crystallogr 26:795–800

    Article  CAS  Google Scholar 

  14. Sheldrick GM (2008) Acta Crystallogr A 64:112–122

    Article  PubMed  Google Scholar 

  15. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Acta Crystallogr D Biol Crystallogr 54:905–921

    Article  PubMed  CAS  Google Scholar 

  16. de La Fortelle E, Bricogne G, Charles CW Jr (1997) Methods Enzymol 276:472–494

    Article  CAS  Google Scholar 

  17. Cowtan KD, Main P (1996) Acta Crystallogr D Biol Crystallogr 52:43–48

    Article  PubMed  CAS  Google Scholar 

  18. Abrahams JP, Leslie AGW (1996) Acta Crystallogr D Biol Crystallogr 52:30–42

    Article  PubMed  CAS  Google Scholar 

  19. Jones TA, Zou JY, Cowan SW, Kjeldgaard M (1991) Acta Crystallogr A 47:110–119

    Article  PubMed  Google Scholar 

  20. Pettifer RF, Hermes C (1985) J Appl Crystallogr 18:404–412

    Article  CAS  Google Scholar 

  21. Korbas M, Marsa DF, Meyer-Klaucke W (2006) Rev Sci Instrum 77. doi:10.1063/1.2209954

  22. Gurman SJ, Binsted N, Ross I (1984) J Phys C Solid State Phys 17:143–151

    Article  CAS  Google Scholar 

  23. Gurman SJ, Binsted N, Ross I (1986) J Phys C Solid State Phys 19:1845–1861

    Article  Google Scholar 

  24. Binsted N, Strange RW, Hasnain SS (1992) Biochemistry 31:12117–12125

    Article  PubMed  CAS  Google Scholar 

  25. Stern EA (1993) Phys Rev B Condens Matter 48:9825–9827

    PubMed  CAS  Google Scholar 

  26. Cruickshank DW (1999) Acta Crystallogr D Biol Crystallogr 55:583–601

    Article  PubMed  CAS  Google Scholar 

  27. Blow DM (2002) Acta Crystallogr D Biol Crystallogr 58:792–797

    Article  PubMed  CAS  Google Scholar 

  28. Einsle O, Tezcan FA, Andrade SL, Schmid B, Yoshida M, Howard JB, Rees DC (2002) Science 297:1696–1700

    Article  PubMed  CAS  Google Scholar 

  29. Zhou ZH, Hou SY, Cao ZX, Wan HL, Ng SW (2004) J Inorg Biochem 98:1037–1044

    Article  PubMed  CAS  Google Scholar 

  30. Zhou ZH, Zhao H, Tsai KR (2004) J Inorg Biochem 98:1787–1794

    Article  PubMed  CAS  Google Scholar 

  31. Duhme AK, Meyer-Klaucke W, White DJ, Delarbre L, Mitchenall LA, Pau RN (1999) J Biol Inorg Chem 4:588–592

    Article  PubMed  CAS  Google Scholar 

  32. Ha SW, Korbas M, Klepsch M, Meyer-Klaucke W, Meyer O, Svetlitchnyi V (2007) J Biol Chem 282:10639–10646

    Article  PubMed  CAS  Google Scholar 

  33. Metselaar GA, Schwartz E, de Gelder R, Feiters MC, Nikitenko S, Smolentsev G, Yalovega GE, Soldatov AV, Cornelissen JJ, Rowan AE, Nolte RJ (2007) Chemphyschem 8:1850–1856

    Article  PubMed  CAS  Google Scholar 

  34. Rech S, Wolin C, Gunsalus RP (1996) J Biol Chem 271:2557–2562

    Article  PubMed  CAS  Google Scholar 

  35. Balan A, Santacruz CP, Moutran A, Ferreira RC, Medrano FJ, Perez CA, Ramos CH, Ferreira LC (2006) Protein Expr Purif 50:215–222

    Article  PubMed  CAS  Google Scholar 

  36. Fraústo da Silva JJR, Williams RJP (2005) The biological chemistry of the elements: the inorganic chemistry of life. Oxford University Press, Oxford

    Google Scholar 

  37. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) J Mol Biol 340:783–795

    Article  PubMed  Google Scholar 

  38. Holm L, Park J (2000) Bioinformatics 16:566–567

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the beamline staff at the Swiss Light Source for assistance with diffraction data collection, and D.C. Rees for discussions. This work was supported by the Roche Research Fund, the National Center for Competence in Research (NCCR) Structural Biology Zurich, the Swiss National Science Foundation, and the European Commission, Research Infrastructure Action under FP6 “Structuring the European Research Area Specific Programme,” contract no. RII3-CT-2004-506008 for supporting access to the EMBL. The coordinates and structure factors have been deposited in the Protein Data Bank under IDs 3CIJ (AfModA), 3CFX (MaModA), 3CG1 (PfModA), 3CFZ (MjModA), and 3CG3 (PhModA).

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Correspondence to Kaspar P. Locher.

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K. Hollenstein and M. Comellas-Bigler contributed equally to this work.

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Hollenstein, K., Comellas-Bigler, M., Bevers, L.E. et al. Distorted octahedral coordination of tungstate in a subfamily of specific binding proteins. J Biol Inorg Chem 14, 663–672 (2009). https://doi.org/10.1007/s00775-009-0479-7

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