Skip to main content

Advertisement

SpringerLink
Log in

Structure and coordination of CuB in the Acidianus ambivalens aa 3 quinol oxidase heme–copper center

  • Original Article
  • Published:
JBIC Journal of Biological Inorganic Chemistry Aims and scope Submit manuscript

Abstract

The coordination environment of the CuB center of the quinol oxidase from Acidianus ambivalens, a type B heme–copper oxygen reductase, was investigated by Fourier transform (FT) IR and extended X-ray absorption fine structure (EXAFS) spectroscopy. The comparative structural chemistry of dinuclear Fe–Cu sites of the different types of oxygen reductases is of great interest. Fully reduced A. ambivalens quinol oxidase binds CO at the heme a 3 center, with ν(CO)=1,973 cm−1. On photolysis, the CO migrated to the CuB center, forming a Cu IB –CO complex with ν(CO)=2,047 cm−1. Raising the temperature of the samples to 25°C did not result in a total loss of signal in the FTIR difference spectrum although the intensity of these signals was reduced sevenfold. This observation is consistent with a large energy barrier against the geminate rebinding of CO to the heme iron from CuB, a restricted limited access at the active-site pocket for a second binding, and a kinetically stable CuB–CO complex in A. ambivalens aa 3. The CuB center was probed in a number of different states using EXAFS spectroscopy. The oxidized state was best simulated by three histidines and a solvent O scatterer. On reduction, the site became three-coordinate, but in contrast to the bo 3 enzyme, there was no evidence for heterogeneity of binding of the coordinated histidines. The CuB centers in both the oxidized and the reduced enzymes also appeared to contain substoichiometric amounts (0.2 mol equiv) of nonlabile chloride ion. EXAFS data of the reduced carbonylated enzyme showed no difference between dark and photolyzed forms. The spectra could be well fit by 2.5 imidazoles, 0.5 Cl− and 0.5 CO ligands. This arrangement of scatterers would be consistent with about half the sites remaining as unligated Cu(his)3 and half being converted to Cu(his)2Cl−CO, a 50/50 ratio of Cu(his)2Cl− and Cu(his)3CO, or some combination of these formulations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Abramson J, Riistama S, Larsson G, Jasaitis A, Svensson-Ek M, Laakkonen L, Puustinen A, Iwata S, Wikstrom M (2000) Nat Struct Biol 7:910–917

    Article  PubMed  CAS  Google Scholar 

  2. Iwata S, Ostermeier C, Ludwig B, Michel H (1995) Nature 376:660–669

    Article  PubMed  CAS  Google Scholar 

  3. Soulimane T, Buse G, Bourenkov GP, Bartunik HD, Huber R, Than ME (2000) EMBO J 19:1766–1776

    Article  PubMed  CAS  Google Scholar 

  4. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S (1995) Science 269:1069–1074

    Article  PubMed  CAS  Google Scholar 

  5. Svensson-Ek M, Abramson J, Larsson G, Tornroth S, Brzezinski P, Iwata S (2002) J Mol Biol 321:329–339

    Article  PubMed  CAS  Google Scholar 

  6. Pereira MM, Santana M, Teixeira M (2001) Biochim Biophys Acta 1505:185–208

    Article  PubMed  CAS  Google Scholar 

  7. Gomes CM, Backgren C, Teixeira M, Puustinen A, Verkhovskaya ML, Wikstrom M, Verkhovsky MI (2001) FEBS Lett 497:159–164

    Article  PubMed  CAS  Google Scholar 

  8. Bandeiras TM, Salgueiro C, Kletzin A, Gomes CM, Teixeira M (2002) FEBS Lett 531:273–277

    Article  PubMed  CAS  Google Scholar 

  9. Gomes CM, Lemos RS, Teixeira M, Kletzin A, Huber H, Stetter KO, Schafer G, Anemuller S (1999) Biochim Biophys Acta 1411:134–141

    Article  PubMed  CAS  Google Scholar 

  10. Lemos RS, Gomes CM, Teixeira M (2001) Biochem Biophys Res Commun 281:141–150

    Article  PubMed  CAS  Google Scholar 

  11. Anemüller S, Schmidt CL, Pacheco I, Schäfer G, Teixeira M (1994) FEMS Microbiol Lett 117:275–280

    Article  Google Scholar 

  12. Purschke WG, Schmidt CL, Petersen A, Schafer G (1977) Bacteriol J 179:1344–1353

    Google Scholar 

  13. Giuffre A, Gomes CM, Antonini G, D’Itri E, Teixeira M, Brunori M (1997) Eur J Biochem 250:383–388

    Article  PubMed  CAS  Google Scholar 

  14. Fann YC, Ahmed I, Blackburn NJ, Boswell JS, Verkhovskaya ML, Hoffman BM, Wikstrom M (1995) Biochemistry 34:10245–10255

    Article  PubMed  CAS  Google Scholar 

  15. Teixeira M, Batista R, Campos AP, Gomes C, Mendes J, Pacheco I, Anemuller S, Hagen WR (1995) Eur J Biochem 227:322–327

    Article  PubMed  CAS  Google Scholar 

  16. Blackburn NJ, Rhames FC, Ralle M, Jaron S (2000) J Biol Inorg Chem 5:341–353

    Article  PubMed  CAS  Google Scholar 

  17. Eisses JF, Stasser JP, Ralle M, Kaplan J, Blackburn NJ (2000) Biochemistry 39:7337–7342

    Article  PubMed  CAS  Google Scholar 

  18. George GN (1995) EXAFSPAK, Stanford Synchrotron Radiation Laboratory

  19. Binsted N, Gurman SJ, Campbell JW (1998) Daresbury Laboratory EXCURV98 Program

  20. Das TK, Gomes CM, Bandeiras TM, Pereira MM, Teixeira M, Rousseau DL (2004) Biochim Biophys Acta 1655:306–320

    Article  PubMed  CAS  Google Scholar 

  21. Pereira MM, Teixeira M (2004) Biochim Biophys Acta 1655:340–346

    Article  PubMed  CAS  Google Scholar 

  22. Einarsdottir O, Killough PM, Fee JA, Woodruff WH (1989) J Biol Chem 264:2405–2408

    PubMed  CAS  Google Scholar 

  23. Koutsoupakis K, Stavrakis S, Pinakoulaki E, Soulimane T, Varotsis C (2002) J Biol Chem 277:32860–32866

    Article  PubMed  CAS  Google Scholar 

  24. Aagaard A, Gilderson G, Gomes CM, Teixeira M, Brzezinski P (1990) Biochemistry 38:10032–10041

    Article  CAS  Google Scholar 

  25. Pasquali M, Floriani C (1984) In: Karlin KD, Zubieta J (eds) Copper coordination chemistry, biochemical and inorganic perspectives. Adenine, New York, pp 311–330

  26. Patch MG, Choi H, Chapman DR, Bau R, McKee V, Reed CA (1990) Inorg Chem 29:110–119

    Article  CAS  Google Scholar 

  27. Villacorta GM, Lippard SJ (1987) Inorg Chem 26:3672–3676

    Article  CAS  Google Scholar 

  28. Sorrell TN, Malachowski MR (1983) Inorg Chem 22:1883–1887

    Article  CAS  Google Scholar 

  29. Sorrell TN, Borovick AS (1987) J Am Chem Soc 109:4255–4260

    Article  CAS  Google Scholar 

  30. Ralle M, Verkovskaya ML, Morgan JE, Verkovsky MI, Wikstrom M, Blackburn NJ (1999) Biochemistry 38:7185–7194

    Article  PubMed  CAS  Google Scholar 

  31. Ostermeir C, Harrenga A, Ermler U, Michel H (1997) Proc Natl Acad Sci USA 94:10547–10533

    Article  PubMed  Google Scholar 

  32. Blackburn NJ, Barr ME, Woodruff WH, van der Oost J, de Vries S (1994) Biochemistry 33:10401–10407

    Article  PubMed  CAS  Google Scholar 

  33. Blackburn NJ, de Vries S, Barr ME, Houser RP, Tolman WB, Sanders D, Fee JA (1997) J Am Chem Soc 119:6135–6143

    Article  CAS  Google Scholar 

  34. Blackburn NJ, Ralle M, Gomez E, Hill MG, Patsuszyn A, Sanders D, Fee JA (1999) Biochemistry 38:7075–7084

    Article  PubMed  CAS  Google Scholar 

  35. Osbourne JP, Cosper NJ, Stälhandske CMV, Scott RA, Alben JO, Gennis RB (1999) Biochemisty 38:4526–4532

    Article  Google Scholar 

  36. Alben JO, Moh PP, Fiamingo FG, Altschuld RA (1981) Proc Natl Acad Sci USA 78:234–237

    Article  PubMed  CAS  Google Scholar 

  37. Dyer RB, Einarsdottir O, Killough PM, Lopez GJJ, Woodruff WH (1989) J Am Chem Soc 111:7657–7659

    Article  CAS  Google Scholar 

  38. Puustinen A, Bailey JA, D. R.B., Mecklenburg SL, Wikstrom M, Woodruff WH (1997) Biochemistry 36:13195–13200

    Article  PubMed  CAS  Google Scholar 

  39. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaona R, Yoshikawa S (1996) Science 272:1136–1144

    Article  PubMed  CAS  Google Scholar 

  40. Giuffre A, Forte E, Antonini G, D’Itri E, Brunori M, Soulimane T, Buse G (1999) Biochemistry 38:1057–1065

    Article  PubMed  CAS  Google Scholar 

  41. Moody AJ, Butler CS, Watmough NJ, Thomson AJ, Rich PR (1998) Biochem J 331:459–464

    PubMed  CAS  Google Scholar 

  42. Butler CS, Seward HE, Greenwood C, Thomson AJ (1997) Biochemistry 36:16259–16266

    Article  PubMed  CAS  Google Scholar 

  43. Kau LS, Spira-Solomon D, Penner-Hahn JE, Hodgson KO, Solomon EI (1987) J Am Chem Soc 109:6433–6422

    Article  CAS  Google Scholar 

  44. Pettingill TM, Strange RW, Blackburn NJ (1991) J Biol Chem 266:16996–17003

    PubMed  CAS  Google Scholar 

  45. Blackburn NJ, Strange RW, Reedijk J, Volbeda A, Farooq A, Karlin KD, Zubieta J (1989) Inorg Chem 28:1349–1357

    Article  CAS  Google Scholar 

  46. Yoshikawa S, Shinzawa-Itoh K, Nakashima R, Yaono R, Yamashita E, Inoue N, Yao M, Fei MJ, Libeu CP, Mizushima T, Yamaguchi H, Tomizaki T, Tsukihara T (1998) Science 280:1723–1729

    Article  PubMed  CAS  Google Scholar 

  47. Harrenga A, Michel H (1999) J Biol Chem 274:33296–33299

    Article  PubMed  CAS  Google Scholar 

  48. Wikstrom M (2000) Biochim Biophys Acta 1458:188–198

    Article  PubMed  CAS  Google Scholar 

  49. Popovic DM, Stuchebrukhov AA (2004) FEBS Lett 566:126–130

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The work was supported by a grant from the National Institutes of Health GM54803 to N.J.B. SSRL is supported by the National Institutes of Health Biomedical Research Technology Division, Division of Research Resources, and by the US Department of Energy, Basic Energy Sciences (BES), and Office of Biological and Environmental Research. The work was supported in part by a grant from FCT, project POCTI/BME/45122/2002. T.M.B. and M.M.P. are recipients of grants from the PRAXIS XXI program (BD/3133/00 and BPD/11621/2002). We acknowledge the contribution of C.M. Gomes (ITQB) at the early stages of this work.

Author information

Authors and Affiliations

  1. Instituto de Tecnologia Quìmica e Biológica, Universidade Nova de Lisboa, Av. da República (EAN), 2784-505, Oeiras, Portugal

    Tiago M. Bandeiras, Manuel M. Pereira & Miguel Teixeira

  2. Department of Environmental and Biomolecular Systems, OGI School of Science and Engineering at OHSU, 20000 NW Walker Rd., Beaverton, OR, 97006, USA

    Pierre Moenne-Loccoz & Ninian J. Blackburn

Authors
  1. Tiago M. Bandeiras
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manuel M. Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Miguel Teixeira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pierre Moenne-Loccoz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ninian J. Blackburn
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ninian J. Blackburn.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bandeiras, T.M., Pereira, M.M., Teixeira, M. et al. Structure and coordination of CuB in the Acidianus ambivalens aa 3 quinol oxidase heme–copper center. J Biol Inorg Chem 10, 625–635 (2005). https://doi.org/10.1007/s00775-005-0012-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00775-005-0012-6

Keywords

Search

Navigation