Skip to main content
Log in

13C−1H heteronuclear dipolar correlation studies of the hydrogen bonding of the quinones inRhodobacter sphaeroides R26 reaction centers

  • Published:
Applied Magnetic Resonance Aims and scope Submit manuscript

Abstract

The photosynthetic reaction center (RC) of the photosynthetic bacteriumRhodobacter sphaeroides R26 contains two quinones, QA and QB. Solid-state heteronuclear (1H−13C) dipolar correlation spectroscopy has been used to study the binding of the quinones in the ground state for RCs reconstituted with l-13C ubiquinone-10. Lee-Goldburg cross-polarization buildup curves are recorded to determine distancesr CH between the l-13C carbon labels and the protons involved in the polarization transfer. The l-13C of both QA and QB have intermolecular correlations with protons that resonate downfield, in the region of hydrogen-bonding protons. The distances between the carbon labels and the correlated protons are short, 0.21±0.01 nm. Hence the nuclear magnetic resonance provides evidence for strong hydrogen-bonding interactions at the l-C=O of both QA and QB for RCs in the ground state. The environment of the l-13C of the QB is structurally heterogeneous compared to that of the QA. The data can be reconciled with a strong H-bonding interaction of the l-C=O of QA with Ala M260 NH, and with complex hydrogen bonding involving NH of Ile-L224 and of Gly-L225, and possibly the Ser-L223 hydroxyl group of the l-C=O of the QB, in the proximal site.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Allen J.P., Feher G., Yeates T.O., Komiya H., Rees C.D.: Proc. Natl. Acad Sci. USA85, 8487–8491 (1988)

    Article  ADS  Google Scholar 

  2. Feher G., Allen J.P., Okamura M.Y., Rees D.C.: Nature339, 111–116 (1989)

    Article  ADS  Google Scholar 

  3. van Liemt W.B.S., Boender G.J., Gast P., Hoff A.J., Lugtenburg J., de Groot H.J.M.: Biochemistry34, 10229–10236 (1995)

    Article  Google Scholar 

  4. van Rossum B.J., van Liemt W.B.S., Boender G.J., Gast P., Hoff A.J., Lugtenburg J., de Groot H.J.M. in: Photosynthesis: From Light to Biosphere; Xth International Photosynthesis Congress, Montpellier, France, 1995. (Mathis P., ed.), vol. 1, p. 899. Dordrecht: Kluwer Academic 1995.

    Google Scholar 

  5. Feher G., Isaacson R.A., Okamura M.Y., Lubitz W. in: Antennas and Reaction Centers of Photosynthetic Bacteria (Michel-Beyerle M.E., ed.). Springer Series in Chemical Physics, vol. 42, p. 174. Berlin: Springer 1985.

    Google Scholar 

  6. Lubitz W., Abresch E.C., Debus R.J., Isaacson R.A., Okamura M.Y., Feher G.: Biochim. Biophys. Acta808, 464–469 (1985)

    Article  Google Scholar 

  7. van den Brink J., Spolyakov A., van Liemt W.B.S., Raap J., Lugtenburg J., Gast P., Hoff A.J.: FEBS Lett.353, 273–276 (1994)

    Article  Google Scholar 

  8. van den Brink J.S., Hulsebosch R.J., Gast P., Hore P.J., Hoff A.J.: Biochemistry33, 13668–13677 (1994)

    Article  Google Scholar 

  9. Isaacson R.A., Abresch E.C., Lendzian F., Boullais C., Paddock M.L., Mioskowski C., Lubitz W., Feher G.: Biophys. J.69, 311–322 (1995)

    Article  ADS  Google Scholar 

  10. Bosch M.K., Gast P., Hoff A.J., Spoyalov A.P., Tsvetkov Yu.D.: Chem. Phys. Lett.239, 306–312 (1995)

    Article  ADS  Google Scholar 

  11. Hulsebosch R.J.: Ph.D. thesis, Leiden University, Leiden, The Netherlands (1999)

  12. Rohrer M., Gast P., Möbius K., Prisner T.F.: Chem. Phys. Lett.259, 523–530 (1996)

    Article  ADS  Google Scholar 

  13. Brudler R., de Groot H.J.M., van Liemt W.B.S., Steggerda W.F., Esmeijer R., Gast P., Hoff A.J., Lugtenburg J., Gerwert K.: EMBO J.13, 5523–5530 (1994)

    Google Scholar 

  14. Breton J., Boullais C., Burie J.R., Nabedryk E., Mioskowski C.: Biochemistry33, 14378–14386 (1994)

    Article  Google Scholar 

  15. Brudler R., de Groot H.J.M., van Liemt W.B.S., Gast P., Hoff A.J., Lugtenburg J., Gerwert K.: FEBS Lett.370, 88–92 (1995)

    Article  Google Scholar 

  16. Breton J., Boullais C., Berger G., Mioskowski C., Nabedryk E.: Biochemistry34, 11606–11616 (1995)

    Article  Google Scholar 

  17. Kleinfeld D., Okamura M.Y., Feher G.: Biochemistry23, 5780–5786 (1984)

    Article  Google Scholar 

  18. Peloquin J.M., Williams J.C., Lin X., Alden R.G., Taguchi A.K.W., Allen J.P., Woodbury N.W.: Biochemistry33, 8089–8100 (1994)

    Article  Google Scholar 

  19. Holzwarth A.R., Müller M.G.: Biochemistry35, 11820–11831 (1996)

    Article  Google Scholar 

  20. Parson W.W., Chu Z.T., Warshel A.: Biophys. J.74, 182–191 (1998)

    Article  ADS  Google Scholar 

  21. cohen B.E., McAnaney T.B., Park E.S., Jan Y.N., Boxer S.G., Jan L.Y.: Science296, 1700–1703 (2002)

    Article  ADS  Google Scholar 

  22. Nagy L., Milano F., Dorogi M., Agostiano A., Laczko G., Szebenyi K., Varo G., Trotta M., Maroti P.: Biochemistry43, 12913–12923 (2004)

    Article  Google Scholar 

  23. Stowell M.B.H., McPhillips T.M., Rees D.C., Soltis S.M., Abresch E., Feher G.: Science276, 812–816 (1997)

    Article  Google Scholar 

  24. Graige M.S., Feher G., Okamura M.Y.: Proc. Natl. Acad. Sci. USA95, 11679–11684 (1998)

    Article  ADS  Google Scholar 

  25. Breton J., Boullais C., Mioskowski C., Sebban P., Baciou L., Nabedryk E.: Biochemistry41, 12921–12927 (2002)

    Article  Google Scholar 

  26. Nabedryk E., Paddock M.L., Okamura M.Y., Breton J.: Biochemistry44, 14519–14527 (2005)

    Article  Google Scholar 

  27. Breton J., Wakeham M.C., Fyfe P.K., Jones M.R., Nabedryk E.: Biochim. Biophys. Acta1656, 127–138 (2004)

    Article  Google Scholar 

  28. Breton J.: Biochemistry43, 3318–3326 (2004)

    Article  Google Scholar 

  29. Boers R.B., Gast P., Hoff A.J., de Groot H.J.M., Lugtenburg J.: Eur. J. Org. Chem.1, 189–202 (2002)

    Article  Google Scholar 

  30. Rossum B.J., de Groot C., de Groot H.J.M., Ladizhansky V., Vega S.: J. Am. Chem. Soc.122, 3465–3472 (2000).

    Article  Google Scholar 

  31. Feher G., Okamura M.Y. in: The Photosynthetic Bacteria (Clayton R.K., Sistrom W.R., eds.), pp. 349–386. New York: Plenum 1978.

    Google Scholar 

  32. Okamura M.Y., Isaacson R.A., Feher G.: Proc. Natl. Acad. Sci. USA72, 3491–3495 (1975)

    Article  ADS  Google Scholar 

  33. van Liemt W.B.S., Steggerda W.F., Esmeijer R., Lugtenburg J.: Rec. Trav. Chim. Pays-Bas113, 153–161 (1994)

    Google Scholar 

  34. de Groot H.J.M., Copié V., Smith S.O., Allen P.J., Winkel C., Lugtenburg J., Herzfeld J., Griffin R.G.: J. Magn. Reson.77, 251–257 (1988)

    Google Scholar 

  35. Bennet A.E., Rienstra C.M., Auger M., Lakshmi K.V., Griffin R.G.: J. Chem. Phys.103, 6951–6957 (1995)

    Article  ADS  Google Scholar 

  36. Fischer M.R., de Groot H.J.M., Raap J., Winkel C., Hoff A.J., Lugtenburg J.: Biochemistry31, 11038–11049 (1992)

    Article  Google Scholar 

  37. Schmidt-Rohr K., Spiess H.: Multidimensional Solid State NMR and Polymers. London: Academic Press 1994.

    Google Scholar 

  38. van Rossum B.J., Förster H., de Groot H.J.M.: J. Magn. Reson.124, 516–519 (1997)

    Article  ADS  Google Scholar 

  39. Chang C.H., El-Kabbani O., Tiede D., Norris J., Schiffer M.: Biochemistry30, 5352–5360 (1991)

    Article  Google Scholar 

  40. Chirino A.J., Lous E.J., Huber M., Allen J.P., Schenck C.C., Paddock M.L., Feher G., Rees D.: Biochemistry33, 4584–4593 (1994)

    Article  Google Scholar 

  41. Ermler U., Fritzsch G., Buchanan S.K., Michel H.: Structure2, 925–936 (1994)

    Article  Google Scholar 

  42. Arnoux B., Gaucher J.F., Ducruix A., Reiss-Husson F.: Acta Crystallogr. D51, 368–379 (1995)

    Article  Google Scholar 

  43. Arnoux B., Reiss-Husson F.: Eur. Biophys. J.24, 233–242 (1996)

    Article  Google Scholar 

  44. Limbach H.H., Manz J.: Ber. Bunsenges. Phys. Chem. Chem. Phys.102, 289–291 (1998)

    Google Scholar 

  45. Seavey B.R., Farr E.A., Westler W.M., Markley J.L.: J. Biomol. NMR1, 217–236 (1991)

    Article  Google Scholar 

  46. Muh F., Rautter J., Lubitz W.: Biochemistry36, 4155–4162 (1997)

    Article  Google Scholar 

  47. Nagy L., Fodor E., Tandori J., Rinyu L., Farkas T.: Aust. J. Plant Physiol.25, 465–473 (1999)

    Article  Google Scholar 

  48. Taly A., Baciou L., Sebban P.: FEBS Lett.532, 91–96 (2002)

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

van Rossum, B.J., van Liemt, W.B.S., Gast, P. et al. 13C−1H heteronuclear dipolar correlation studies of the hydrogen bonding of the quinones inRhodobacter sphaeroides R26 reaction centers. Appl. Magn. Reson. 31, 145–158 (2007). https://doi.org/10.1007/BF03166252

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03166252

Keywords

Navigation