Skip to main content
NCBI home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2002 Oct 29;357(1426):1407–1420. doi: 10.1098/rstb.2002.1137

Electrostatics and proton transfer in photosynthetic water oxidation.

Wolfgang Junge 1, Michael Haumann 1, Ralf Ahlbrink 1, Armen Mulkidjanian 1, Jürgen Clausen 1
PMCID: PMC1693046  PMID: 12437879

Abstract

Photosystem II (PSII) oxidizes two water molecules to yield dioxygen plus four protons. Dioxygen is released during the last out of four sequential oxidation steps of the catalytic centre (S(0) --> S(1), S(1) --> S(2), S(2) --> S(3), S(3) --> S(4) --> S(0)). The release of the chemically produced protons is blurred by transient, highly variable and electrostatically triggered proton transfer at the periphery (Bohr effect). The extent of the latter transiently amounts to more than one H(+)/e(-) under certain conditions and this is understood in terms of electrostatics. By kinetic analyses of electron-proton transfer and electrochromism, we discriminated between Bohr-effect and chemically produced protons and arrived at a distribution of the latter over the oxidation steps of 1 : 0 : 1 : 2. During the oxidation of tyr-161 on subunit D1 (Y(Z)), its phenolic proton is not normally released into the bulk. Instead, it is shared with and confined in a hydrogen-bonded cluster. This notion is difficult to reconcile with proposed mechanisms where Y(Z) acts as a hydrogen acceptor for bound water. Only in manganese (Mn) depleted PSII is the proton released into the bulk and this changes the rate of electron transfer between Y(Z) and the primary donor of PSII P(+)(680) from electron to proton controlled. D1-His190, the proposed centre of the hydrogen-bonded cluster around Y(Z), is probably further remote from Y(Z) than previously thought, because substitution of D1-Glu189, its direct neighbour, by Gln, Arg or Lys is without effect on the electron transfer from Y(Z) to P(+)(680) (in nanoseconds) and from the Mn cluster to Y(ox)(Z).

Full Text

The Full Text of this article is available as a PDF (277.9 KB).

Selected References

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

  1. Ahlbrink R., Haumann M., Cherepanov D., Bögershausen O., Mulkidjanian A., Junge W. Function of tyrosine Z in water oxidation by photosystem II: electrostatical promotor instead of hydrogen abstractor. Biochemistry. 1998 Jan 27;37(4):1131–1142. doi: 10.1021/bi9719152. [DOI] [PubMed] [Google Scholar]
  2. Beroza P., Fredkin D. R., Okamura M. Y., Feher G. Electrostatic calculations of amino acid titration and electron transfer, Q-AQB-->QAQ-B, in the reaction center. Biophys J. 1995 Jun;68(6):2233–2250. doi: 10.1016/S0006-3495(95)80406-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beroza P., Fredkin D. R., Okamura M. Y., Feher G. Protonation of interacting residues in a protein by a Monte Carlo method: application to lysozyme and the photosynthetic reaction center of Rhodobacter sphaeroides. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5804–5808. doi: 10.1073/pnas.88.13.5804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boussac A., Etienne A. L. Oxido-reduction kinetics of Signal II slow in tris-washed chloroplasts. Biochem Biophys Res Commun. 1982 Dec 31;109(4):1200–1205. doi: 10.1016/0006-291x(82)91904-0. [DOI] [PubMed] [Google Scholar]
  5. Chu H. A., Hillier W., Law N. A., Babcock G. T. Vibrational spectroscopy of the oxygen-evolving complex and of manganese model compounds. Biochim Biophys Acta. 2001 Jan 5;1503(1-2):69–82. doi: 10.1016/s0005-2728(00)00216-4. [DOI] [PubMed] [Google Scholar]
  6. Clausen J., Winkler S., Hays A. M., Hundelt M., Debus R. J., Junge W. Photosynthetic water oxidation in Synechocystis sp. PCC6803: mutations D1-E189K, R and Q are without influence on electron transfer at the donor side of photosystem II. Biochim Biophys Acta. 2001 Nov 1;1506(3):224–235. doi: 10.1016/s0005-2728(01)00217-1. [DOI] [PubMed] [Google Scholar]
  7. Dau H., Iuzzolino L., Dittmer J. The tetra-manganese complex of photosystem II during its redox cycle - X-ray absorption results and mechanistic implications. Biochim Biophys Acta. 2001 Jan 5;1503(1-2):24–39. doi: 10.1016/s0005-2728(00)00230-9. [DOI] [PubMed] [Google Scholar]
  8. Debus R. J., Campbell K. A., Pham D. P., Hays A. M., Britt R. D. Glutamate 189 of the D1 polypeptide modulates the magnetic and redox properties of the manganese cluster and tyrosine Y(Z) in photosystem II. Biochemistry. 2000 May 30;39(21):6275–6287. doi: 10.1021/bi992749w. [DOI] [PubMed] [Google Scholar]
  9. Drachev L. A., Semenov AYu, Skulachev V. P., Smirnova I. A., Chamorovsky S. K., Kononenko A. A., Rubin A. B., Uspenskaya NYa Fast stages of photoelectric processes in biological membranes. III. Bacterial photosynthetic redox system. Eur J Biochem. 1981 Jul;117(3):483–489. doi: 10.1111/j.1432-1033.1981.tb06363.x. [DOI] [PubMed] [Google Scholar]
  10. Fromme Petra, Kern Jan, Loll Bernhard, Biesiadka Jaceck, Saenger Wolfram, Witt Horst T., Krauss Norbert, Zouni Athina. Functional implications on the mechanism of the function of photosystem II including water oxidation based on the structure of photosystem II. Philos Trans R Soc Lond B Biol Sci. 2002 Oct 29;357(1426):1337-44; discussion 1344-5, 1367. doi: 10.1098/rstb.2002.1143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Haumann M., Bögershausen O., Junge W. Photosynthetic oxygen evolution: net charge transients as inferred from electrochromic bandshifts are independent of proton release into the medium. FEBS Lett. 1994 Nov 21;355(1):101–105. doi: 10.1016/0014-5793(94)01181-8. [DOI] [PubMed] [Google Scholar]
  12. Haumann M., Hundelt M., Jahns P., Chroni S., Bögershausen O., Ghanotakis D., Junge W. Proton release from water oxidation by photosystem II: similar stoichiometries are stabilized in thylakoids and PSII core particles by glycerol. FEBS Lett. 1997 Jun 30;410(2-3):243–248. doi: 10.1016/s0014-5793(97)00596-6. [DOI] [PubMed] [Google Scholar]
  13. Haumann M., Junge W. Extent and rate of proton release by photosynthetic water oxidation in thylakoids: electrostatic relaxation versus chemical production. Biochemistry. 1994 Feb 1;33(4):864–872. doi: 10.1021/bi00170a003. [DOI] [PubMed] [Google Scholar]
  14. Haumann M., Junge W. The rates of proton uptake and electron transfer at the reducing side of photosystem II in thylakoids. FEBS Lett. 1994 Jun 20;347(1):45–50. doi: 10.1016/0014-5793(94)00495-1. [DOI] [PubMed] [Google Scholar]
  15. Haumann M., Mulkidjanian A., Junge W. Electrogenicity of electron and proton transfer at the oxidizing side of photosystem II. Biochemistry. 1997 Aug 5;36(31):9304–9315. doi: 10.1021/bi963114p. [DOI] [PubMed] [Google Scholar]
  16. Haumann M, Junge W. Evidence for impaired hydrogen-bonding of tyrosine YZ in calcium-depleted photosystem II . Biochim Biophys Acta. 1999 Apr 21;1411(1):121–133. doi: 10.1016/s0005-2728(99)00045-6. [DOI] [PubMed] [Google Scholar]
  17. Haumann M, Junge W. Photosynthetic water oxidation: a simplex-scheme of its partial reactions . Biochim Biophys Acta. 1999 Apr 21;1411(1):86–91. doi: 10.1016/s0005-2728(99)00042-0. [DOI] [PubMed] [Google Scholar]
  18. Hillier W., Wydrzynski T. Oxygen ligand exchange at metal sites - implications for the O2 evolving mechanism of photosystem II. Biochim Biophys Acta. 2001 Jan 5;1503(1-2):197–209. doi: 10.1016/s0005-2728(00)00225-5. [DOI] [PubMed] [Google Scholar]
  19. Hoganson C. W., Babcock G. T. A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science. 1997 Sep 26;277(5334):1953–1956. doi: 10.1126/science.277.5334.1953. [DOI] [PubMed] [Google Scholar]
  20. Hoganson C. W., Babcock G. T. Mechanistic aspects of the tyrosyl radical-manganese complex in photosynthetic water oxidation. Met Ions Biol Syst. 2000;37:613–656. [PubMed] [Google Scholar]
  21. Junge W., Ausländer W., McGeer A. J., Runge T. The buffering capacity of the internal phase of thylakoids and the magnitude of the pH changes inside under flashing light. Biochim Biophys Acta. 1979 Apr 11;546(1):121–141. doi: 10.1016/0005-2728(79)90175-0. [DOI] [PubMed] [Google Scholar]
  22. Junge W., Witt H. T. On the ion transport system of photosynthesis--investigations on a molecular level. Z Naturforsch B. 1968 Feb;23(2):244–254. doi: 10.1515/znb-1968-0222. [DOI] [PubMed] [Google Scholar]
  23. Messinger J., Robblee J. H., Bergmann U., Fernandez C., Glatzel P., Visser H., Cinco R. M., McFarlane K. L., Bellacchio E., Pizarro S. A. Absence of Mn-centered oxidation in the S(2) --> S(3) transition: implications for the mechanism of photosynthetic water oxidation. J Am Chem Soc. 2001 Aug 15;123(32):7804–7820. doi: 10.1021/ja004307+. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Messinger J. Towards understanding the chemistry of photosynthetic oxygen evolution: dynamic structural changes, redox states and substrate water binding of the Mn cluster in photosystem II. Biochim Biophys Acta. 2000 Aug 15;1459(2-3):481–488. doi: 10.1016/s0005-2728(00)00187-0. [DOI] [PubMed] [Google Scholar]
  25. Metz J. G., Nixon P. J., Rögner M., Brudvig G. W., Diner B. A. Directed alteration of the D1 polypeptide of photosystem II: evidence that tyrosine-161 is the redox component, Z, connecting the oxygen-evolving complex to the primary electron donor, P680. Biochemistry. 1989 Aug 22;28(17):6960–6969. doi: 10.1021/bi00443a028. [DOI] [PubMed] [Google Scholar]
  26. Mulkidjanian A. Y., Cherepanov D. A., Haumann M., Junge W. Photosystem II of green plants: topology of core pigments and redox cofactors as inferred from electrochromic difference spectra. Biochemistry. 1996 Mar 5;35(9):3093–3107. doi: 10.1021/bi9513057. [DOI] [PubMed] [Google Scholar]
  27. Mulkidjanian A. Y. Conformationally controlled pK-switching in membrane proteins: one more mechanism specific to the enzyme catalysis? FEBS Lett. 1999 Dec 17;463(3):199–204. doi: 10.1016/s0014-5793(99)01536-7. [DOI] [PubMed] [Google Scholar]
  28. Mulkidjanian AY. Photosystem II of green plants: on the possible role of retarded protonic relaxation in water oxidation1 . Biochim Biophys Acta. 1999 Jan 27;1410(1):1–6. doi: 10.1016/s0005-2728(98)00174-1. [DOI] [PubMed] [Google Scholar]
  29. Nugent J. H., Rich A. M., Evans M. C. Photosynthetic water oxidation: towards a mechanism. Biochim Biophys Acta. 2001 Jan 5;1503(1-2):138–146. doi: 10.1016/s0005-2728(00)00223-1. [DOI] [PubMed] [Google Scholar]
  30. Renger G. Photosynthetic water oxidation to molecular oxygen: apparatus and mechanism. Biochim Biophys Acta. 2001 Jan 5;1503(1-2):210–228. doi: 10.1016/s0005-2728(00)00227-9. [DOI] [PubMed] [Google Scholar]
  31. Robblee J. H., Cinco R. M., Yachandra V. K. X-ray spectroscopy-based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution. Biochim Biophys Acta. 2001 Jan 5;1503(1-2):7–23. doi: 10.1016/s0005-2728(00)00217-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Siegbahn P. E. Theoretical models for the oxygen radical mechanism of water oxidation and of the water oxidizing complex of photosystem II. Inorg Chem. 2000 Jun 26;39(13):2923–2935. doi: 10.1021/ic9911872. [DOI] [PubMed] [Google Scholar]
  33. Tommos C., Babcock G. T. Proton and hydrogen currents in photosynthetic water oxidation. Biochim Biophys Acta. 2000 May 12;1458(1):199–219. doi: 10.1016/s0005-2728(00)00069-4. [DOI] [PubMed] [Google Scholar]
  34. Tommos C., Hoganson C. W., Valentin M. D., Lydakis-Simantiris N., Dorlet P., Westphal K., Chu H. A., McCracken J., Babcock G. T. Manganese and tyrosyl radical function in photosynthetic oxygen evolution. Curr Opin Chem Biol. 1998 Apr;2(2):244–252. doi: 10.1016/s1367-5931(98)80066-5. [DOI] [PubMed] [Google Scholar]
  35. Vass I., Styring S. pH-dependent charge equilibria between tyrosine-D and the S states in photosystem II. Estimation of relative midpoint redox potentials. Biochemistry. 1991 Jan 22;30(3):830–839. doi: 10.1021/bi00217a037. [DOI] [PubMed] [Google Scholar]
  36. Vrettos J. S., Limburg J., Brudvig G. W. Mechanism of photosynthetic water oxidation: combining biophysical studies of photosystem II with inorganic model chemistry. Biochim Biophys Acta. 2001 Jan 5;1503(1-2):229–245. doi: 10.1016/s0005-2728(00)00214-0. [DOI] [PubMed] [Google Scholar]
  37. Yachandra Vittal K. Structure of the manganese complex in photosystem II: insights from X-ray spectroscopy. Philos Trans R Soc Lond B Biol Sci. 2002 Oct 29;357(1426):1347-57; discussion 1357-8, 1367. doi: 10.1098/rstb.2002.1133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Zouni A., Witt H. T., Kern J., Fromme P., Krauss N., Saenger W., Orth P. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 A resolution. Nature. 2001 Feb 8;409(6821):739–743. doi: 10.1038/35055589. [DOI] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES