Alternating electron and proton transfer steps in photosynthetic water oxidation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 40, 2012, Pages 16035-16040

  Klauss, André ^a   Haumann, Michael ^a   Dau, Holger ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MANGANESE; SULFUR; WATER;

ARTICLE; CHEMICAL MODEL; CHEMICAL REACTION KINETICS; ELECTRON TRANSPORT; MOLECULAR MODEL; NONHUMAN; PHASE TRANSITION; PHOTOOXIDATION; PHOTOSYNTHESIS; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTON TRANSPORT; SURFACE CHARGE;

BIOLOGICAL TRANSPORT; ELECTRON TRANSPORT; KINETICS; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PROTONS; SPECTRUM ANALYSIS; SPINACIA OLERACEA; WATER;

ALGAE; CYANOBACTERIA;

EID: 84867049701     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1206266109     Document Type: Article

References (66)

1. McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106:4455-4483. (Pubitemid 44816649)
2. Dau H, Haumann M (2008) The manganese complex of photosystem II in its reaction cycle: Basic framework and possible realization at the atomic level. Coord Chem Rev 252:273-295.
3. Barber J (2009) Photosynthetic energy conversion: Natural and artificial. Chem Soc Rev 38:185-196.
4. Blankenship RE (2002) Molecular Mechanisms of Photosynthesis (Blackwell Science, Oxford).
5. Rutherford AW, Moore TA (2008) Mimicking photosynthesis, but just the best bits. Nature 453:449. (Pubitemid 351733297)
6. Magnuson A, et al. (2009) Biomimetic and microbial approaches to solar fuel generation. Acc Chem Res 42:1899-1909.
7. Dau H, et al. (2010) The mechanism of water oxidation: From electrolysis via homogeneous to biological catalysis. ChemCatChem 2:724-761.
8. 2: Design principles of photosystem II and hydrogenases. Energy Environ Sci 1:15-31.
9. Dau H, Zaharieva I (2009) Principles, efficiency, and blueprint character of solar-energy conversion in photosynthetic water oxidation. Acc Chem Res 42:1861-1870.
10. Barry BA, Babcock GT (1987) Tyrosine radicals are involved in the photosynthetic oxygen-evolving system. Proc Natl Acad Sci USA 84:7099-7103.
11. Styring S, Sjöholm J, Mamedov F (2012) Two tyrosines that changed the world: Interfacing the oxidizing power of photochemistry to water splitting in photosystem II. Biochim Biophys Acta 1817:76-87.
12. 4Ca cluster and to the evolution of molecular oxygen in photosystem II. Coord Chem Rev 252:259-272.
13. Zouni A, et al. (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739-743. (Pubitemid 32144521)
14. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831-1838. (Pubitemid 38374869)
15. Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55-60.
16. 2 evolution, I. A linear four-step mechanism. Photochem Photobiol 11:457 -475.
17. Dau H, Haumann M (2007) Time-resolved X-ray spectroscopy leads to an extension of the classical S-state cycle model of photosynthetic oxygen evolution. Photosynth Res 92:327-343. (Pubitemid 47248571)
18. Lavergne J, Junge W (1993) Proton release during the redox cycle of the water oxidase. Photosynth Res 38:279-296.
19. Junge W, Haumann M, Ahlbrink R, Mulkidjanian A, Clausen J (2002) Electrostatics and proton transfer in photosynthetic water oxidation. Philos Trans R Soc Lond B Biol Sci 357:1407-1418. (Pubitemid 35293780)
20. Rappaport F, Lavergne J (1991) Proton release during successive oxidation steps of the photosynthetic water oxidation process: Stoichiometries and pH dependence. Biochemistry 30:10004-10012.
21. Ho FM (2008) Uncovering channels in photosystem II by computer modelling: Current progress, future prospects, andlessons fromanalogous systems. Photosynth Res 98:503-522.
22. 2 formation tracked by time-resolved X-ray experiments. Science 310:1019-1021.
23. Hoganson CW, Babcock GT (1997) A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277:1953-1956. (Pubitemid 27449129)
24. Dau H, Haumann M (2007) Eight steps preceding O-O bond formation in oxygenic photosynthesis: A basic reaction cycle of the photosystem II manganese complex. Biochim Biophys Acta 1767:472-483. (Pubitemid 46860310)
25. Meyer TJ, Huynh MHV, Thorp HH (2007) The possible role of proton-coupled electron transfer (PCET) in water oxidation by photosystem II. Angew Chem Int Ed 46:5284-5304. (Pubitemid 47086254)
26. 2O exchange and the influence of pH support formation of an intermediate by removal of a proton before dioxygen creation. Biochemistry 49:10098-10106.
27. Haumann M, Bögershausen O, Cherepanov D, Ahlbrink R, Junge W (1997) Photosynthetic oxygen evolution: H/D isotope effects and the coupling between electron and proton transfer during the redox reactions at the oxidizing side of photosystem II. Photosynth Res 51:193-208. (Pubitemid 27275238)
28. Renger G, Hanssum B (1992) Studies on the reaction coordinates of the water oxidase in PS II membrane fragments from spinach. FEBS Lett 299:28-32.
29. Dekker JP, Plijter JJ, Ouwehand L, van Gorkom HJ (1984) Kinetics of manganese redox transitions in the oxygen evolving apparatus of photosynthesis. Biochim Biophys Acta 767:176-179.
30. Haumann M, Junge W (1994) Extent and rate of proton release by photosynthetic water oxidation in thylakoids: Electrostatic relaxation versus chemical production. Biochemistry 33:864-872. (Pubitemid 24058423)
31. Schlodder E, Witt HT (1999) Stoichiometry of proton release from the catalytic center in photosynthetic water oxidation. Reexamination by a glass electrode study at ph 5.5-7. J Biol Chem 274:30387-30392.
32. Rappaport F, Blanchard-Desce M, Lavergne J (1994) Kinetics of electron transfer and electrochromic change during the redox transition of the photosynthetic oxygen-evolving complex. Biochim Biophys Acta 1184:178-192. (Pubitemid 24080783)
33. Dau H, Haumann M (2006) Reaction cycle of photosynthetic water oxidation in plants and cyanobacteria (response letter). Science 312:1471-1472.
34. Braslavsky SE, Heibel GE (1992) Time-resolved photothermal and photoacoustic methods applied to photoinduced processes in solution. Chem Rev 92:1381-1410.
35. Falvey DE (1997) Photothermal beam deflection calorimetry in solution photochemistry: Recent progress and future prospects. Photochem Photobiol 65:4-9. (Pubitemid 27084354)
36. Gensch T, Viappiani C (2003) Time-resolved photothermal methods: Accessing time-resolved thermodynamics of photoinduced processes in chemistry and biology. Photochem Photobiol Sci 2:699-721. (Pubitemid 41662956)
37. Krivanek R, Dau H, Haumann M (2008) Enthalpy changes during photosynthetic water oxidation tracked by time-resolved calorimetry using a photothermal beam deflection technique. Biophys J 94:1890-1903.
38. Klauss A, Krivanek R, Dau H, Haumann M (2009) Energetics and kinetics of photosynthetic water oxidation studied by photothermal beam deflection (PBD) experiments. Photosynth Res 102:499-509.
39. Feitelson J, Mauzerall D (2002) Enthalpy and electrostriction in the electron-transfer reaction between triplet zinc uroporphyrin and ferricyanide. J Phys Chem B 106:9674-9678. (Pubitemid 35382781)
40. Rizzi AC, et al. (2008) Entropic changes control the charge separation process in triads mimicking photosynthetic charge separation. J Phys Chem A 112:4215-4223. (Pubitemid 351704615)
41. Hou HJM, Mauzerall D (2011) Listening to PS II: Enthalpy, entropy, and volume changes. J Photochem Photobiol B 104:357-365.
42. Mauzerall D, Hou JM, Boichenko VA (2002) Volume changes and electrostriction in the primary photoreactions of various photosynthetic systems: Estimation of dielectric coefficient in bacterial reaction centers and of the observed volume changes with the Drude-Nernst equation. Photosynth Res 74:173-180. (Pubitemid 35409517)
43. Hou JM, Boichenko VA, Diner BA, Mauzerall D (2001) Thermodynamics of electron transfer in oxygenic photosynthetic reaction centers: Volume change, enthalpy, and entropy of electron-transfer reactions in manganese-depleted photosystem II core complexes. Biochemistry 40:7117-7125. (Pubitemid 32554034)
44. 0) characterized by X-ray absorption spectroscopy at 20 K and room temperature. Biochemistry 44:1894-1908.
45. Noguchi T (2008) Fourier transform infrared analysis of the photosynthetic oxygen-evolving center. Coord Chem Rev 252:336-346.
46. Buchta J, Grabolle M, Dau H (2007) Photosynthetic dioxygen formation studied by time-resolved delayed fluorescence measurements: Method, rationale, and results on the activation energy of dioxygen formation. Biochim Biophys Acta 1767:565-574. (Pubitemid 46860312)
47. Karge M, Irrgang KD, Renger G (1997) Analysis of the reaction coordinate of photosynthetic water oxidation by kinetic measurements of 355 nm absorption changes at different temperatures in photosystem II preparations suspended in either H2O or D2O. Biochemistry 36:8904-8913. (Pubitemid 27342537)
48. Razeghifard MR, Klughammer C, Pace RJ (1997) Electron paramagnetic resonance kinetic studies of the S states in spinach thylakoids. Biochemistry 36:86-92. (Pubitemid 27024681)
49. Hatcher E, Soudackov A, Hammes-Schiffer S (2005) Comparison of dynamical aspects of nonadiabatic electron, proton, and proton-coupled electron transfer reactions. Chem Phys 319:93-100. (Pubitemid 41750476)
50. Krishtalik LI (2000) The mechanism of the proton transfer: An outline. Biochim Biophys Acta 1458:6-27.
51. Garczarek F, Gerwert K (2006) Functional waters in intraprotein proton transfer monitored by FTIR difference spectroscopy. Nature 439:109-112. (Pubitemid 43053638)
52. Barry BA, et al. (2006) Time-resolved vibrational spectroscopy detects protein-based intermediates in the photosynthetic oxygen-evolving cycle. Proc Natl Acad Sci USA 103:7288-7291. (Pubitemid 43727825)
53. 2+ determines the entropy changes associated with the formation of transition states during water oxidation by photosystem II. Energy Environ Sci 4:2520-2524.
54. 0 transition. Biochemistry 38:1252-1257.
55. Dau H, Iuzzolino L, Dittmer J (2001) The tetra-manganese complex of photosystem II during its redox cycle: X-ray absorption results and mechanistic implications. Biochim Biophys Acta 1503:24-39.
56. 2 moieties in the tetranuclear Mn complex? J Am Chem Soc 124:7459-7471.
57. Zaharieva I, Wichmann JM, Dau H (2011) Thermodynamic limitations of photosynthetic water oxidation at high proton concentrations. J Biol Chem 286:18222-18228.
58. Teutloff C, et al. (2009) Electronic structure of the tyrosine D radical and the water-splitting complex from pulsed ENDOR spectroscopy on photosystem II single crystals. Phys Chem Chem Phys 11:6715-6726.
59. Siegbahn PE (2008) A structure-consistent mechanism for dioxygen formation in photosystem II. Chem Eur J 14:8290-8302.
60. 2 state in the oxygen evolving complex of photosystem II: Protonation states and magnetic interactions. J Am Chem Soc 133:19743-19757.
61. Hundelt M, Hays AM, Debus RJ, Junge W (1998) Oxygenic photosystem II: The mutation D1-D61N in Synechocystis sp. PCC 6803 retards S-state transitions without affecting electron transfer from YZ to P 680+. Biochemistry 37:14450-14456. (Pubitemid 28489051)
62. 2 from photosystem II. Biochemistry 51:1079-1091.
63. McEvoy JP, Brudvig GW (2004) Structure-based mechanism of photosynthetic water oxidation. Phys Chem Chem Phys 6:4754-4763.
64. 2 formation. Biochemistry 40:7937-7945.
65. Bondar AN, Dau H (2012) Extended protein/water H-bond networks in photosynthetic water oxidation. Biochim Biophys Acta 1817:1177-1190.
66. 0 transitions monitored by delayed chlorophyll fluorescence. Proceedings of the Fifteenth International Conference on Photosynthesis, in press.