Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1995 Aug;69(2):311–322. doi: 10.1016/S0006-3495(95)79936-2

Electronic structure of Q-A in reaction centers from Rhodobacter sphaeroides. I. Electron paramagnetic resonance in single crystals.

R A Isaacson 1, F Lendzian 1, E C Abresch 1, W Lubitz 1, G Feher 1
PMCID: PMC1236255  PMID: 8527644

Abstract

The magnitude and orientation of the electronic g-tensor of the primary electron acceptor quinone radical anion, Q-A, has been determined in single crystals of zinc-substituted reaction centers of Rhodobacter sphaeroides R-26 at 275 K and at 80 K. To obtain high spectral resolution, EPR experiments were performed at 35 GHz and the native ubiquinone-10 (UQ10) in the reaction center was replaced by fully deuterated UQ10. The principal values and the direction cosines of the g-tensor axes with respect to the crystal axes a, b, c were determined. Freezing of the single crystals resulted in only minor changes in magnitude and orientation of the g-tensor. The orientation of Q-A as determined by the g-tensor axes deviates only by a few degrees (< or = 8 degrees) from the orientation of the neutral QA obtained from an average of four different x-ray structures of Rb. sphaeroides reaction centers. This deviation lies within the accuracy of the x-ray structure determinations. The g-tensor values measured in single crystals agree well with those in frozen solutions. Variations in g-values between Q-A, Q-B, and UQ10 radical ion in frozen solutions were observed and attributed to different environments.

Full text

PDF
311

Images in this article

312FIGURE 1
on p.312
313FIGURE 2
on p.313
314FIGURE 3
on p.314
320FIGURE 9
on p.320

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allen J. P., Feher G., Yeates T. O., Komiya H., Rees D. C. Structure of the reaction center from Rhodobacter sphaeroides R-26: protein-cofactor (quinones and Fe2+) interactions. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8487–8491. doi: 10.1073/pnas.85.22.8487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Breton J., Boullais C., Burie J. R., Nabedryk E., Mioskowski C. Binding sites of quinones in photosynthetic bacterial reaction centers investigated by light-induced FTIR difference spectroscopy: assignment of the interactions of each carbonyl of QA in Rhodobacter sphaeroides using site-specific 13C-labeled ubiquinone. Biochemistry. 1994 Dec 6;33(48):14378–14386. doi: 10.1021/bi00252a002. [DOI] [PubMed] [Google Scholar]
  3. Breton J., Burie J. R., Berthomieu C., Berger G., Nabedryk E. The binding sites of quinones in photosynthetic bacterial reaction centers investigated by light-induced FTIR difference spectroscopy: assignment of the QA vibrations in Rhodobacter sphaeroides using 18O- or 13C-labeled ubiquinone and vitamin K1. Biochemistry. 1994 Apr 26;33(16):4953–4965. doi: 10.1021/bi00182a026. [DOI] [PubMed] [Google Scholar]
  4. Brudler R., de Groot H. J., van Liemt W. B., Steggerda W. F., Esmeijer R., Gast P., Hoff A. J., Lugtenburg J., Gerwert K. Asymmetric binding of the 1- and 4-C=O groups of QA in Rhodobacter sphaeroides R26 reaction centres monitored by Fourier transform infra-red spectroscopy using site-specific isotopically labelled ubiquinone-10. EMBO J. 1994 Dec 1;13(23):5523–5530. doi: 10.1002/j.1460-2075.1994.tb06889.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Buchanan S., Michel H., Gerwert K. Light-induced charge separation in Rhodopseudomonas viridis reaction centers monitored by Fourier-transform infrared difference spectroscopy: the quinone vibrations. Biochemistry. 1992 Feb 11;31(5):1314–1322. doi: 10.1021/bi00120a006. [DOI] [PubMed] [Google Scholar]
  6. Butler W. F., Calvo R., Fredkin D. R., Isaacson R. A., Okamura M. Y., Feher G. The electronic structure of Fe2+ in reaction centers from Rhodopseudomonas sphaeroides. III. EPR measurements of the reduced acceptor complex. Biophys J. 1984 May;45(5):947–973. doi: 10.1016/S0006-3495(84)84241-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chang C. H., el-Kabbani O., Tiede D., Norris J., Schiffer M. Structure of the membrane-bound protein photosynthetic reaction center from Rhodobacter sphaeroides. Biochemistry. 1991 Jun 4;30(22):5352–5360. doi: 10.1021/bi00236a005. [DOI] [PubMed] [Google Scholar]
  8. Chirino A. J., Lous E. J., Huber M., Allen J. P., Schenck C. C., Paddock M. L., Feher G., Rees D. C. Crystallographic analyses of site-directed mutants of the photosynthetic reaction center from Rhodobacter sphaeroides. Biochemistry. 1994 Apr 19;33(15):4584–4593. doi: 10.1021/bi00181a020. [DOI] [PubMed] [Google Scholar]
  9. Debus R. J., Feher G., Okamura M. Y. Iron-depleted reaction centers from Rhodopseudomonas sphaeroides R-26.1: characterization and reconstitution with Fe2+, Mn2+, Co2+, Ni2+, Cu2+, and Zn2+. Biochemistry. 1986 Apr 22;25(8):2276–2287. doi: 10.1021/bi00356a064. [DOI] [PubMed] [Google Scholar]
  10. Deisenhofer J., Michel H. Nobel lecture. The photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis. EMBO J. 1989 Aug;8(8):2149–2170. doi: 10.1002/j.1460-2075.1989.tb08338.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ermler U., Fritzsch G., Buchanan S. K., Michel H. Structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2.65 A resolution: cofactors and protein-cofactor interactions. Structure. 1994 Oct 15;2(10):925–936. doi: 10.1016/s0969-2126(94)00094-8. [DOI] [PubMed] [Google Scholar]
  12. Feher G., Okamura M. Y., McElroy J. D. Identification of an electron acceptor in reaction centers of Rhodopseudomonas spheroides by EPR spectroscopy. Biochim Biophys Acta. 1972 Apr 20;267(1):222–226. doi: 10.1016/0005-2728(72)90155-7. [DOI] [PubMed] [Google Scholar]
  13. Kirmaier C., Holten D., Debus R. J., Feher G., Okamura M. Y. Primary photochemistry of iron-depleted and zinc-reconstituted reaction centers from Rhodopseudomonas sphaeroides. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6407–6411. doi: 10.1073/pnas.83.17.6407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kleinfeld D., Okamura M. Y., Feher G. Electron-transfer kinetics in photosynthetic reaction centers cooled to cryogenic temperatures in the charge-separated state: evidence for light-induced structural changes. Biochemistry. 1984 Nov 20;23(24):5780–5786. doi: 10.1021/bi00319a017. [DOI] [PubMed] [Google Scholar]
  15. Loach P. A., Hall R. L. The question of the primary electron acceptor in bacterial photosynthesis. Proc Natl Acad Sci U S A. 1972 Apr;69(4):786–790. doi: 10.1073/pnas.69.4.786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lubitz W., Abresch E. C., Debus R. J., Isaacson R. A., Okamura M. Y., Feher G. Electron nuclear double resonance of semiquinones in reaction centers of Rhodopseudomonas sphaeroides. Biochim Biophys Acta. 1985 Aug 7;808(3):464–469. doi: 10.1016/0005-2728(85)90155-0. [DOI] [PubMed] [Google Scholar]
  17. Okamura M. Y., Feher G. Proton transfer in reaction centers from photosynthetic bacteria. Annu Rev Biochem. 1992;61:861–896. doi: 10.1146/annurev.bi.61.070192.004241. [DOI] [PubMed] [Google Scholar]
  18. Okamura M. Y., Isaacson R. A., Feher G. Primary acceptor in bacterial photosynthesis: obligatory role of ubiquinone in photoactive reaction centers of Rhodopseudomonas spheroides. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3491–3495. doi: 10.1073/pnas.72.9.3491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Stesmans A, De Vos G ESR observation of temperature-dependent g shifts in submetallic P-doped Si at low temperatures. Phys Rev B Condens Matter. 1986 Nov 1;34(9):6499–6502. doi: 10.1103/physrevb.34.6499. [DOI] [PubMed] [Google Scholar]
  20. Wraight C. A. Electron acceptors of bacterial photosynthetic reaction centers. II. H+ binding coupled to secondary electron transfer in the quinone acceptor complex. Biochim Biophys Acta. 1979 Nov 8;548(2):309–327. doi: 10.1016/0005-2728(79)90138-5. [DOI] [PubMed] [Google Scholar]
  21. van den Brink J. S., Spoyalov A. P., Gast P., van Liemt W. B., Raap J., Lugtenburg J., Hoff A. J. Asymmetric binding of the primary acceptor quinone in reaction centers of the photosynthetic bacterium Rhodobacter sphaeroides R26, probed with Q-band (35 GHz) EPR spectroscopy. FEBS Lett. 1994 Oct 24;353(3):273–276. doi: 10.1016/0014-5793(94)01047-1. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES