Abstract
Old and very recent experiments on the extent and the rate of proton release during the four reaction steps of photosynthetic water oxidation are reviewed. Proton release is discussed in terms of three main sources, namely the chemical production upon electron abstraction from water, protolytic reactions of Mn-ligands (e.g. oxo-bridges), and electrostatic response of neighboring amino acids. The extent of proton release differs between the four oxidation steps and greatly varies as a function of pH both, but differently, in thylakoids and PS II-membranes. Contrastingly, it is about constant in PS II-core particles. In any preparation, and on most if not all reaction steps, a large portion of proton transfer can occur very rapidly (<20 μs) and before the oxidation of the Mn-cluster by Yz + is completed. By these electrostatically driven reactions the catalytic center accumulates bases. An additional slow phase is observed during the oxygen evolving step, S3⇒S4→S0. Depending on pH, this phase consists of a release or an uptake of protons which accounts for the balance between the number of preformed bases and the four chemically produced protons. These data are compatible with the hypothesis of concerted electron/proton-transfer to overcome the kinetic and energetic constraints of water oxidation.
Similar content being viewed by others
Abbreviations
- BBY-membranes:
-
Photosystem II-enriched membrane fragments prepared after Berthold, Babcock and Yocum (1981)
- BSA:
-
bovine serum albumin
- Chl:
-
chlorophyll
- CAB-protein:
-
chlorophyll a/b-binding protein
- core particles:
-
oxygen evolving reaction center core particles of Photosystem II
- Cyt:
-
cytochrome
- DCBQ:
-
2,5-dichloro-p-benzoquinone
- IML:
-
intermittent light
- P-680:
-
primary electron donor of Photosystem II
- PS II:
-
Photosystem II
- Yz :
-
tyrosine residue on the D1 polypeptide, electron carrier between manganese and P-680
- photochemical reaction:
-
⇒
References
Ausländer W and Junge W (1975) Neutral red, a rapid indicator for pH changes in the inner phase of thylakoids. FEBS Lett 59: 310–315
Berthold DA, Babcock GT and Yocum CF (1981) A highly resolved, oxygen-evolving Photosystem II preparation from spinach thylakoid membranes. FEBS Lett 134: 231–236
Bossek U, Weyhermueller T, Wieghardt K, Nuber B and Weiss J (1990) [L2Mn2(m-O)2(m-O2)](ClO4)2. The first binuclear (m-peroxo)dimanganese(IV) complex (L=1,4,7-trimethyl-1,4,7-triazacyclononane). A model for the S4-S0 transformation in the oxygen-evolving complex in photosynthesis. J Am Chem Soc 112: 6387–6388
Bowes JM and Crofts AR (1981) The role of pH and membrane potential in the reactions of Photosystem II as measured by effects on delayed fluorescence. Biochim Biophys Acta 637: 464–472
Brettel K, Schlodder E and Witt HT (1984) Nanosecond reduction kinetics of photooxidized chlorophyll-a II (P-680) in single flashes as a probe for the electron pathway, H+-release and charge accumulation in the O2-evolving complex. Biochim Biophys Acta 766: 403–415
Brudvig GW and De Paula JC (1987) On the mechanism of photosynthetic water oxidation. In: Biggins J (ed) Progress in Photosynthesis Research, pp 491–498. Martinus Nijhoff, Dordrecht
Buser CA, Diner BA and Brudvig GW (1992) Photooxidation of cytochrome b559 in oxygen evolving Photosystem II. Biochemistry 31: 11449–11459
Carroll JM and Norton JR (1992) Protonation of a bridging oxoligand is slow. J Am Chem Soc 114: 8744–8775
Conjeaud H and Mathis P (1986) Electron transfer in the photosynthesis membrane. Influence of pH and surface potential on the P 680 reduction kinetics. Biophys J 49: 1215–1221
Cooper SR and Calvin M (1977) Mixed valence interactions in di-μ-oxo bridged manganese clusters. J Am Chem Soc 99: 6623–6630
Debus RJ (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102: 269–352
Dekker JP, Plijter JJ, Ouwenand L and Van Gorkom HJ (1984a) Kinetics of manganese redox transitions in the oxygen evolving apparatus of photosynthesis. Biochim Biophys Acta 767: 176–179
Dekker JP, Van Gorkom HJ, Wensink J and Ouwehand L (1984b) Absorbance difference spectra of the successive redox states of the oxygen-evolving apparatus of photosynthesis. Biochim Biophys Acta 767: 1–9
Delosme R (1971) New results about chlorophyll fluorescence in vivo. In: Forti G, Avron M and Melandri A (eds) Proceedings of the IInd International Congress on Photosynthesis, pp 187–195. Dr. W. Junk, The Hague
Dilley RA (1991) Energy coupling in chloroplasts: A calciumgated switch controls proton fluxes between localized and delocalized proton gradients. Current Topics in Bioenergetics 16: 265–318
Eckert HJ and Renger G (1988) Temperature dependence of P680+ reduction in oxygen-evolving PS II membrane fragments at different redox states Si of the water oxidizing system. FEBS Lett 236: 425–431
Eigen M (1963) Protonenübertragung, Säure-Base-Katalyse und enzymatische Hydrolyse. Teil I: Elementarvorgänge. Angew Chem 12s: 489–588
Emrich HM, Junge W and Witt HT (1969) Further evidence for an optical response of chloroplast bulk pigments to a light-induced electrical field in photosynthesis. Z Naturforsch B 24: 1144–1146
Fowler CF (1977) Proton evolution from Photosystem II. Stoichiometry and mechanistic considerations. Biochim Biophys Acta 462: 414–421
Förster V, and Junge W (1984) Protolytic reactions at the donor side of PS II: Proton release in tris-washed chloroplasts with t1/2×100ms. Implications for the interpretation of the proton release pattern in untreated, oxygen-evolving chloroplasts. In: Sybesma C (ed) Advances in Photosynthetic Research, pp 305-ff. Martinus Nijhoff/Dr W. Junk, The Hague/Boston/Lancaster
Förster V and Junge W (1985) Stoichiometry and kinetics of proton release upon photosynthetic water oxidation. Photochem Photobiol 41: 183–190
Förster V, Hong YQ and Junge W (1981) Electron transfer and proton pumping under excitation of dark-adapted chloroplasts with flashes of light. Biochim Biophys Acta 638: 141–152
George GN, Prince RC and Cramer SP (1989) The manganese site of photosynthetic water-splitting enzyme. Science 234: 789–791
Gerwert K, Souvignier G and Hess B (1990) Simultaneous monitoring of light induced changes in protein side-group protonation, chromophore isomerization, and backbone motion of bacteriorhodopsin by time-resolved Fourier-transform infrared spectroscopy. Proc Natl Acad Sci USA 87: 9774–9778
Ghanotakis DF, Babcock GT and Yocum CF (1984) Structural and catalytic properties of the oxygen-evolving complex. Correlation of polypeptide and manganese release with the behavior of Z+ in chloroplasts and a highly resolved preparation of the PS II complex. Biochim Biophys Acta 765: 388–398
Ghanotakis DF, Waggoner CM, Bowlby NR, Demetriou DM, Babcock GT and Yocum CF (1987) Comparative structural and catalytic properties of oxygen-evolving Photosystem II preparations. Photosynth Res 14: 191–199
Gutman M and Nachliel E (1990) The dynamic aspects of proton transfer processes. Biochim Biophys Acta 1015: 391–414
Haag E, Irrgang KD, Boekema EJ and Renger G (1990) Functional and structural analysis of Photosystem II core complexes from spinach with high oxygen evolution capacity. Eur J Biochem 189: 47–53
Haumann M and Junge W (1993) Extent and role of proton release by photosynthetic water oxidation in thylakoids: Electrostatic relaxation versus chemical production. Biochemistry (in press)
Hong YQ and Junge W (1983) Localized or delocalized protons in photophosphorylation? On the accessibility of the thylakoid lumen for ions and buffers. Biochim Biophys Acta 722: 197–208
Hong YQ, Förster V and Junge W (1981) A cyclic protolytic reaction around Photosystem II at the inside of the thylakoid membrane in DCMU-poisoned chloroplasts. FEBS Lett 132: 247–251
Hope AB and Morland A (1979) Proton translocation in isolated spinach chloroplasts after single-turnover actinic flashes. Aust J Plant Physiol 6: 1–16
Jahns P and Junge W (1989) The protonic shortcircuit by DCCD in Photosystem II. A common feature of all redox transitions of water oxidation. FEBS Lett 253: 33–37
Jahns P and Junge W (1990) Dicyclohexylcarbodiimide-binding proteins related to the short circuit of the proton-pumping activity of Photosystem II. Identified as light-harvesting chlorophyll a/b-binding proteins. Eur J Biochem 193: 731–736
Jahns P and Junge W (1992a) Thylakoids from pea seedlings grown under intermittent light: Biochemical and flashspectrophotometric properties. Biochemistry 31: 7390–7397
Jahns P and Junge W (1992b) Proton release during the four steps of photosynthetic water oxidation: Induction of 1:1:1:1 pattern due to lack of chlorophyll a/b binding proteins. Biochemistry 31: 7398–7403
Jahns P and Junge W (1993) Another role of chlorophyll a/b binding proteins of higher plants: They modulate protolytic reactions associated with Photosystem II. Photochem Photobiol 57: 120–124
Jahns P, Polle A and Junge W (1988) The photosynthetic water oxidase: Its proton pumping activity is short-circuited within the protein by DCCD. EMBO J 7: 589–594
Jahns P, Lavergne J, Rappaport F and Junge W (1991) Stoichiometry of proton release during photosynthetic water oxidation: A reinterpretation of the response of neutral red leads to a non-integer pattern. Biochim Biophys Acta 1057: 313–319
Jahns P, Haumann M, Bögershausen O and Junge W (1992) Water oxidation: 1:1:1:1 proton-over-electron stoichiometry in CAB-protein depleted thylakoids and PS II core particles. In: Murata N (ed) Research in Photosynthesis II, pp 333–336. Kluwer Academic Publishers, Dordrecht
Joliot P and Kok B (1975) Oxygen evolution in photosynthesis. In: Govindjee (ed) Bioenergetics of Photosynthesis, pp 387–412. Academic Press, New York
Joliot P, Joliot A, Bouges B and Barbieri G (1971) Studies of System II photocenters by comparative measurements of luminescence, fluorescence and oxygen emission. Photochem Photobiol 14: 287–305
Junge W and Polle A (1986) Theory of proton flow along appressed thylakoid membranes under both non-stationary and stationary conditions. Biochim Biophys Acta 848: 265–273
Junge W and Witt HT (1968) On the ion transport system of photosynthesis: Investigation on a molecular level. Z Naturforsch 23b: 244–254
Junge W, Ausländer W, McGeer AJ and Runge T (1979) The buffering capacity of the internal phase of thylakoids and the magnitude of the pH changes inside under flashing light. Biochim Biophys Acta 546: 121–141
Junge W, Schönknecht G and Förster V (1986) Neutral red as an indicator of pH transients in the lumen of thylakoids: Some answers to criticism. Biochim Biophys Acta 852: 93–99
Kirilovsky DL, Boussac A, Van Mieghem FJE, Ducruet JM, Sétif P, Yu J, Vermaas WFJ and Rutherford AW (1992) Oxygen-evolving Photosystem II preparation from wild type and Photosystem II mutants of Synechocystis sp. PCC 6803. Biochemistry 31: 2099–2107
Kok B, Forbush B and McGloin M (1970) Cooperation of charges in photosynthetic O2 evolution: I. A linear four-step mechanism. Photochem Photobiol 11: 457–475
Krishtalik LI (1986) Energetics of multielectron reactions. Photosynthetic oxygen evolution. Biochim Biophys Acta 849: 162–171
Krishtalik LI (1990) Activation energy of photosynthetic oxygen evolution: an attempt at theoretical analysis. Bioelectrochem Bioenerg 23: 249–263
Lavergne J (1987) Optical-difference spectra of the S-state transitions in the photosynthetic oxygen-evolving complex. Biochim Biophys Acta 894: 91–107
Lavergne J (1991) Improved UV-visible spectra of the Stransitions in the photosynthetic oxygen-evolving system. Biochim Biophys Acta 1060: 175–188
Lavergne J and Rappaport F (1990) On the stoichiometry of proton release by the oxygen-evolving system. In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol I, pp 873–876. Kluwer Academic Publishers, Dordrecht
Lavergne J, Blanchard-Desce M and Rappaport F (1992) Oxidation and deprotonation reactions in the Kok cycle. In: Murata N (ed) Research in Photosynthesis, pp 273–280. Kluwer Academic Publishers, Dordrecht
Lübbers K and Junge W (1990) Is the proton release due to water oxidation directly coupled to events at the manganese centre?. In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol I, pp 877–880. Kluwer Academic Publishers, Dordrecht
Lübbers K, Haumann M and Junge W (1993) Photosynthetic water oxidation under flashing light: Oxygen release, proton release and absorption transients in the near UV. A comparison between thylakoids and a reaction center core preparation. Biochim Biophys Acta (in press)
Machanda R, Thorp HH, Brudvig GW and Crabtree RH (1991) Proton coupled electron transfer in high-valent oxomanganese dimers: Role of the ancillary ligands. Inorg Chem 30: 494–497
Machanda R, Thorp HH, Brudvig GW and Crabtree RH (1992) An unusual example of multiple proton-coupled electron transfer in a high-valent oxomanganese dimer [(phen)2 Mn(III) (O)2 Mn(IV) (phen)2](Clo4)3; (phen=1,10-Phenathrolin). Inorg Chem 31: 4040–4041
Maróti P and Wraight CA (1988) Flash-induced H+-binding by bacterial photosynthesis reaction centers: Influences of the redox states of the acceptor quinones and primary donor. Biochim Biophys Acta 934: 329–347
McPherson PH, Okamura MY and Feher G (1988) Light induced proton uptake by photosynthetic reaction centers from Rhodobacter sphaeroides R-26. I. Protonation of the one-electron-states. Biochim Biophys Acta 934: 348–368
Meyer B, Schlodder E, Dekker JP and Witt HT (1989) O2 evolution and Chl a II +(P-680+) nanosecond reduction kinetics in single flashes as a function of pH. Biochim Biophys Acta 974: 36–43
Nanba O and Satoh K (1987) Isolation of a Photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci USA 84: 109–112
Okamura MY and Feher G (1992) Proton transfer in reaction centers from photosynthetic bacteria. Annu Rev Biochem 61: 861–896
Pecoraro VL (1988) Structural proposals for the manganese centers of the oxygen evolving complex: An inorganic chemist's prospective. Photochem Photobiol 48: 249–264
Penner-Hahn JE, Fronko RM, Waldo GS, Yocum CF, Bowlby NR and Betts SD (1990) X-ray absorption spectroscopy of the photosynthetic oxygen evolving complex. In: Baltscheffsky M (ed) Current Research in Photosynthesis, pp 797–800. Kluwer Academic Publishers, Dordrecht
Philouze C, Blondin G, Menage S, Auger N, Girerd JJ, Vigner D, Lance M and Nierlich M (1992) A novel manganeseoxygen cluster type with a chain Mn4 unit: Relation to the reaction center of Photosystem II. Angew Chem 104: 1634–1636
Polle A and Junge W (1986a) Transient and intramembrane trapping of pumped protons in thylakoids. The domains are delocalized and redox-sensitive. FEBS Lett 198: 263–267
Polle A and Junge W (1986b) The slow rise of the flash-light-induced alkalization by Photosystem II of the suspending medium of thylakoids is reversibly related to thylakoid stacking. Biochim Biophys Acta 848: 257–264
Polle A and Junge W (1989) Proton diffusion along the membrane surface of thylakoids is not enhanced over that in bulk water. Biophys J 56: 27–31
Rappaport F and Lavergne J (1991) Proton release during successive oxidation steps of the photosynthetic water oxidation process: Stoichiometries and pH dependence. Biochemistry 30: 10004–10012
Renger G (1988) On the mechanism of photosynthetic water oxidation to dioxygen. In: Vänngard T (ed) Chemica Scripta 28A, pp 105–109. Cambridge University Press, Cambridge
Renger G and Hanssum B (1992) Studies on the reaction coordinates of the water oxidase in PS II membrane fragments from spinach. FEBS Lett 299: 28–32
Renger G and Voelker M (1982) Studies on the proton release pattern of the donor side of system II: Correlation between oxidation and deprotonization of donor D1 in Tris-washed inside-out thylakoids. FEBS Lett 149: 203–207
Rögner M, Dekker JP, Boekema EJ and Witt HT (1987) Size, shape and mass of the oxygen-evolving Photosystem II complex from the thermophilic cyanobacterium Synechococcus sp. FEBS Lett 219: 207–211
Saphon S and Crofts AR (1977) Protolytic reactions in Photosystem II: A new model for the release of protons accompanying the photooxidation of water. Z Naturforsch, C: Biosci 32C: 617–626
Sauer K, Vittal K, Yachandra WK, Britt RD and Klein MP (1992) The photosynthetic water oxidation complex studied by EPR and X-ray absorption spectroscopy. In: Pecoraro VL (ed) Manganese Redox Enzymes, pp 141–175, VCH, New York
Saygin Ö and Witt HT (1985) Evidence for the electrochromic identification of the change of charges in the four oxidation steps of the photoinduced water cleavage in photosynthesis. FEBS Lett 187: 224–226
Schatz G and Van Gorkom HJ (1985) Absorbance difference spectra upon charge transfer to secondary donors and acceptors in Photosystem II. Biochim Biophys Acta 810: 283–294
Takahashi E, Maróti P and Wraight CA (1992) Coupled proton and electron transfer pathways in the acceptor quinone complex of reaction centers from Rhodobacter sphaeroides. In: Müller A, Diemann E, Junge W and Ratajczak H (eds) Electron and Proton Transfer in Chemistry and Biology, pp 219–236. Elsevier, Amsterdam
Theg SM and Homann PH (1982) Light-, pH- and uncouplerdependent association of chloride with chloroplast thylakoids. Biochim Biophys Acta 679: 221–234
Theg SM and Junge W (1983) The effect of low concentrations of uncouplers on the detectability of proton deposition in thylakoids. Evidence for subcompartmentation and preexisting pH differences in the dark. Biochim Biophys Acta 723: 294–307
Thorp H, Sasneskhi JE, Brudvig GW and Crabtree RH (1989) Proton coupled electrons transfer in [(bpy)2Mn(O) 2Mn(bpy)2]3+. J Am Chem Soc 3: 9249–9250
Van Leeuwen PJ, Nieveen MC, van de Meent EJ, Dekker JP and Van Gorkom HJ (1991) Rapid and simple isolation of pure Photosystem II core and reaction center particles from spinach. Photosynth Res 28: 149–153
Van Leeuwen PJ, Heimann C, Dekker JP, Gast JP and van Gorkom HJ (1992a) Redox changes of the oxygen evolving complex in Photosystem II core particles as studied by UV spectroscopy. In: Murata N (ed) Research in Photosynthesis, pp 325–326. Kluwer Academic Publishers, Dordrecht
Van Leeuwen PJ, Heimann C, Kleinherenbrink FAM and van Gorkom HJ (1992b) Kinetics of electron transport on the donor side of spinach photosystem core particles. In: Murata N (ed) Research in Photosynthesis, pp 341–344. Kluwer Academic Publishers, Dordrecht
Velthuys B (1981) Spectrophotometric studies on the S-state transition of Photosystem II and of the interactions of its charged donor chains with lipid soluble anions. In: Akoyunoglou G (ed) Photosynthesis II. Electron Transport and Photophosphorylation, pp 75–85. Balaban International Science Services, Philadelphia
Velthuys BR (1988) Spectroscopic characterization of the acceptor state QA - and the donor state S2 of Photosystem II of spinach in the blue, red and near-infrared. Biochim Biophys Acta 933: 249–257
Wacker U, Haag E and Renger G (1990) Investigation of pH-change-patterns of photosystem-II membrane fragments from spinach. In: Baltscheffsky M (ed) Current Research in Photosynthesis, pp 869–872. Kluwer Academic Publishers, Dordrecht
Webber AN and Gray JC (1989) Detection of calcium binding by Photosystem II polypeptides immobilized onto nitrocellulose membrane. FEBS Lett 249: 79–82
Wille B and Lavergne J (1982) Measurement of proton translocation in the thylakoids under flashing light using a spin-labeled amine. Photobiochem Photobiophys 4: 131–144
Yachandra VK, Guiles RD, McDermott AE, Britt RD, Dexheimer SL, Sauer K and Klein MP (1986) The state of manganese in the photosynthetic apparatus. 4. Structure of the manganese complex in Photosystem II studied using EXAFS spectroscopy. The S1 state of the oxygen-evolving Photosystem II complex from spinach. Biochim Biophys Acta 850: 324–332
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lavergne, J., Junge, W. Proton release during the redox cycle of the water oxidase. Photosynth Res 38, 279–296 (1993). https://doi.org/10.1007/BF00046752
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00046752