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Proton transport facilitating water-oxidation: the role of second sphere ligands surrounding the catalytic metal cluster

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Abstract

The ability of PSII to extract electrons from water, with molecular oxygen as a by-product, is a remarkable biochemical and evolutionary innovation. From an evolutionary perspective, the invention of PSII approximately 2.7 Ga led to the accelerated accumulation of biomass in the biosphere and the accumulation of oxygen in the atmosphere, a combination that allowed for the evolution of a much more complex and extensive biosphere than would otherwise have been possible. From the biochemical and enzymatic perspective, PSII is remarkable because of the thermodynamic and kinetic obstacles that needed to have been overcome to oxidize water as the ultimate photosynthetic electron donor. This article focuses on how proton release is an integral part of how these kinetic and thermodynamic obstacles have been overcome: the sequential removal of protons from the active site of H2O-oxidation facilitates the multistep oxidation of the substrate water at the Mn4CaO x , the catalytic heart of the H2O-oxidation reaction. As noted previously, the facilitated deprotonation of the Mn4CaO x cluster exerts a redox-leveling function preventing the accumulation of excess positive charge on the cluster, which might otherwise hinder the already energetically difficult oxidation of water. Using recent results, including the characteristics of site-directed mutants, the role of the second sphere of amino acid ligands and the associated network of water molecules surrounding the Mn4CaO x is discussed in relation to proton transport in other systems. In addition to the redox-leveling function, a trapping function is assigned to the proton release step occurring immediately prior to the dioxygen chemistry. This trapping appears to involve a yet-to-be clarified gating mechanism that facilitates to coordinated release of a proton from the neighborhood of the active site thereby insuring that the backward charge-recombination reaction does not out-compete the forward reaction of dioxygen chemistry during this final step of H2O-oxidation.

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References

  • Adir N, Zer H, Shochat S, Ohad I (2003) Photoinhibition: a historical perspective. Photosynth Res 76(1–3):343–370

    PubMed  CAS  Google Scholar 

  • Agmon N (1995) The Grotthuss mechanism. Chem Phys Lett 244 (5–6):456–462. doi:10.1016/0009-2614(95)00905-J

  • Ames W, Pantazis DA, Krewald V, Cox N, Messinger J, Lubitz W, Neese F (2011) Theoretical evaluation of structural models of the S2 state in the oxygen evolving complex of photosystem II: protonation states and magnetic interactions. J Am Chem Soc 133(49):19743–19757. doi:10.1021/ja2041805

    PubMed  CAS  Google Scholar 

  • Babcock GT, Barry BA, Debus RJ, Hoganson CW, Atamian M, McIntosh L, Sitole I, Yocum CF (1989) Water oxidation in photosystem II: from radical chemistry to multielectron chemistry. Biochemistry 28:9557–9565

    PubMed  CAS  Google Scholar 

  • Bondar AN, Dau H (2012) Extended protein/water H-bond networks in photosynthetic water oxidation. Biochim Biophys Acta 1817(8):1177–1190. doi:10.1016/j.bbabio.2012.03.031

    PubMed  CAS  Google Scholar 

  • Boussac A, Rutherford AW (2000) Comparative study of the g = 4.1 EPR signals in the S2 state of photosystem II. Biochim Biophys Acta 1457(3):145–156. doi:10.1016/S0005-2728(00)00073-6

    PubMed  CAS  Google Scholar 

  • Chrysina M, Zahariou G, Ioannidis N, Petrouleas V (2010) Conversion of the g = 4.1 EPR signal to the multiline conformation during the S2 to S3 transition of the oxygen evolving complex of photosystem II. Biochim Biophys Acta 1797(4):487–493. doi:10.1016/j.bbabio.2010.01.008

    PubMed  CAS  Google Scholar 

  • Chu HA, Nguyen AP, Debus RJ (1995) Amino acid residues that influence the binding of manganese or calcium to photosystem II. 1. The lumenal interhelical domains of the D1 polypeptide. Biochemistry 34:5839–5858

    PubMed  CAS  Google Scholar 

  • Clausen J, Debus RJ, Junge W (2004) Time-resolved oxygen production by PSII: chasing chemical intermediates. Biochim Biophys Acta 1655(1–3):184–194

    PubMed  CAS  Google Scholar 

  • Cox N, Messinger J (2013) Reflections on substrate water and dioxygen formation. Biochim Biophys Acta 1827(8–9):1020–1030. doi:10.1016/j.bbabio.2013.01.013

    PubMed  CAS  Google Scholar 

  • Damoder R, Dismukes GC (1984) pH dependence of the multiline, manganese EPR signal for the ‘S2’ state in PS II particles: absence of proton release during the S1 → S2 electron transfer step of the oxygen evolving system. FEBS Lett 174(1):157–161

    PubMed  CAS  Google Scholar 

  • Dau H, Haumann M (2006) Photosynthetic oxygen production: response. Science 312(5779):1471–1472

    CAS  Google Scholar 

  • 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(3):327–343. doi:10.1007/s11120-007-9141-9

    PubMed  CAS  Google Scholar 

  • 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(3–4):273–295. doi:10.1016/j.ccr.2007.09.001

    CAS  Google Scholar 

  • Dau H, Liebisch P, Haumann M (2003) X-ray absorption spectroscopy to analyze nuclear geometry and electronic structure of biological metal centers: potential and questions examined with special focus on the tetra-nuclear manganese complex of oxygenic photosynthesis. Anal Bioanal Chem 376(5):562–583

    PubMed  CAS  Google Scholar 

  • Day TJF, Schmitt UW, Voth GA (2000) The mechanism of hydrated proton transport in water. J Am Chem Soc 122(48):12027–12028. doi:10.1021/ja002506n

    CAS  Google Scholar 

  • De Grotthus C (1806) Sur la de′composition de l’eau et des corps qu’elle tient en dissolution a` l’aide de l’e′ lectricite′ galvanique. Ann Chim LVIII:54–74

    Google Scholar 

  • Decoursey TE (2003) Voltage-gated proton channels and other proton transfer pathways. Physiol Rev 83(2):475–579. doi:10.1152/physrev.00028.2002

    PubMed  CAS  Google Scholar 

  • Dekker JP, Ghanotakis DF, Plijter JJ, Van GHJ, Babcock GT (1984) Kinetics of the oxygen-evolving complex in salt-washed photosystem II preparations. Biochim Biophys Acta 767:515–523

    CAS  Google Scholar 

  • Dilbeck PL, Hwang HJ, Zaharieva I, Gerencser L, Dau H, Burnap RL (2012) The D1-D61N mutation in Synechocystis sp. PCC 6803 allows the observation of pH-sensitive intermediates in the formation and release of O2 from photosystem II. Biochemistry 51(6):1079–1091. doi:10.1021/Bi201659f

    PubMed  CAS  Google Scholar 

  • Diner BA, Rappaport F (2002) Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 53:551–580

    CAS  Google Scholar 

  • Diner BA, Force DA, Randall DW, Britt RD (1998) Hydrogen bonding, solvent exchange, and coupled proton and electron transfer in the oxidation and reduction of redox-active tyrosine Y(Z) in Mn-depleted core complexes of photosystem II. Biochemistry 37(51):17931–17943

    PubMed  CAS  Google Scholar 

  • Diner BA, Bautista JA, Nixon PJ, Berthomieu C, Hienerwadel R, Britt RD, Vermaas WFJ, Chisholm DA (2004) Coordination of proton and electron transfer from the redox-active tyrosine, Y–Z, of photosystem II and examination of the electrostatic influence of oxidized tyrosine, Y–D*(H+). Phys Chem Chem Phys 6(20):4844–4850

    CAS  Google Scholar 

  • Dismukes GC, Siderer Y (1981) Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water. Proc Natl Acad Sci USA 78(1):274–278. doi:10.1073/Pnas.78.1.274

    PubMed  CAS  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303(5665):1831–1838

    PubMed  CAS  Google Scholar 

  • Forbush B, Kok B, McGloin MP (1971) Cooperation of charges in photosynthetic O2 evolution: II damping of flash yield oscillation, deactivation. Photochem Photobiol 14:307–321

    CAS  Google Scholar 

  • Fowler CF (1977) Proton evolution from photosystem II stoichiometry and mechanistic considerations. Biochim Biophys Acta 462(2):414–421

    PubMed  CAS  Google Scholar 

  • Freier E, Wolf S, Gerwert K (2011) Proton transfer via a transient linear water-molecule chain in a membrane protein. Proc Natl Acad Sci USA 108(28):11435–11439

    PubMed  CAS  Google Scholar 

  • Gerencser L, Dau H (2010) Water oxidation by photosystem II: H2O–D2O exchange and the influence of pH support formation of an intermediate by removal of a proton before dioxygen creation. Biochemistry 49(47):10098–10106. doi:10.1021/bi101198n

    PubMed  CAS  Google Scholar 

  • Goussias C, Boussac A, Rutherford AW (2002) Photosystem II and photosynthetic oxidation of water: an overview. Philos Trans R Soc Lond B Biol Sci 357(1426):1369–1381

    PubMed  CAS  Google Scholar 

  • Gutman M, Nachliel E (1990) The dynamic aspects of proton-transfer processes. Biochim Biophys Acta 1015(3):391–414. doi:10.1016/0005-2728(90)90073-D

    CAS  Google Scholar 

  • Haddy A (2007) EPR spectroscopy of the manganese cluster of photosystem II. Photosynth Res 92(3):357–368

    PubMed  CAS  Google Scholar 

  • Haumann M, Junge W (1994) Extent and rate of proton release by photosynthetic water oxidation in thylakoids: electrostatic relaxation versus chemical production. Biochemistry 33(4):864–872

    PubMed  CAS  Google Scholar 

  • Haumann M, Hundelt M, Jahns P, Chroni S, Bogershausen O, Ghanotakis D, Junge W (1997) Proton release from water oxidation by photosystem II: similar stoichiometries are stabilized in thylakoids and PSII core particles by glycerol. FEBS Lett 410(2–3):243–248

    PubMed  CAS  Google Scholar 

  • Haumann M, Grabolle M, Neisius T, Dau H (2002) The first room-temperature X-ray absorption spectra of higher oxidation states of the tetra-manganese complex of photosystem II. FEBS Lett 512(1–3):116–120

    PubMed  CAS  Google Scholar 

  • Haumann M, Liebisch P, Muller C, Barra M, Grabolle M, Dau H (2005a) Photosynthetic O2 formation tracked by time-resolved X-ray experiments. Science 310(5750):1019–1021

    PubMed  CAS  Google Scholar 

  • Haumann M, Muller C, Liebisch P, Iuzzolino L, Dittmer J, Grabolle M, Neisius T, Meyer-Klaucke W, Dau H (2005b) Structural and oxidation state changes of the photosystem II manganese complex in four transitions of the water oxidation cycle (S0 → S1, S1 → S2, S2 → S3, and S3, S4 → S0) characterized by X-ray absorption spectroscopy at 20 K and room temperature. Biochemistry 44(6):1894–1908

    PubMed  CAS  Google Scholar 

  • Hillier W, Messinger J (2005) Mechanism of photosynthetic oxygen production. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light-driven water: plastoquinone oxidoreductase. Springer, Dordrecht, The Netherlands, pp 567–608

    Google Scholar 

  • Hillier W, Wydrzynski T (2008) O-18-water exchange in photosystem II: substrate binding and intermediates of the water splitting cycle. Coord Chem Rev 252(3–4):306–317. doi:10.1016/J.Ccr.2007.09.004

    CAS  Google Scholar 

  • Ho FM, Styring S (2008) Access channels and methanol binding site to the CaMn4 cluster in photosystem II based on solvent accessibility simulations, with implications for substrate water access. Biochim Biophys Acta 1777(2):140–153. doi:10.1016/j.bbabio.2007.08.009

    PubMed  CAS  Google Scholar 

  • Hoganson C, Lydakis-Simantiris N, Tang X, Tommos C, Warnke K, Babcock G, Diner B, McCraken J, Styring S (1995) A hydrogen atom abstraction model for the function of Yz in photosynthetic oxygen evolution. Photosynth Res 46:177–184

    CAS  Google Scholar 

  • Hundelt M, Hays AM, Debus RJ, Junge W (1998a) Oxygenic photosystem II: the mutation D1-D61N in Synechocystis sp. PCC 6803 retards S-state transitions without affecting electron transfer from YZ to P680+. Biochemistry 37(41):14450–14456

    PubMed  CAS  Google Scholar 

  • Hundelt M, Hays AMA, Debus RJ, Junge W (1998b) The mutation D1-D61N in PS II of Synechocystis: retardation of ET from OEC → Y oxz and no effect on Yz → P680+. In: Garab G (ed) Photosynthesis: mechanisms and effects, vol II. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 1387–1390

    Google Scholar 

  • Hwang HJ, Dilbeck P, Debus RJ, Burnap RL (2007) Mutation of arginine 357 of the CP43 protein of photosystem II severely impairs the catalytic S-state cycle of the H2O oxidation complex. Biochemistry 46(43):11987–11997

    PubMed  CAS  Google Scholar 

  • Hwang HJ, Nagarajan A, McLain A, Burnap RL (2008) Assembly and disassembly of the photosystem II manganese cluster reversibly alters the coupling of the reaction center with the light-harvesting phycobilisome. Biochemistry 47(37):9747–9755. doi:10.1021/bi800568p

    PubMed  CAS  Google Scholar 

  • Hynes JT (1999) Physical chemistry: the protean proton in water. Nature 397(6720):565. doi:10.1038/17487

    CAS  Google Scholar 

  • Ishikita H, Saenger W, Loll B, Biesiadka J, Knapp EW (2006) Energetics of a possible proton exit pathway for water oxidation in photosystem II. Biochemistry 45(7):2063–2071

    PubMed  CAS  Google Scholar 

  • Iuzzolino L, Dittmer J, Dorner W, Meyer-Klaucke W, Dau H (1998) X-ray absorption spectroscopy on layered photosystem II membrane particles suggests manganese-centered oxidation of the oxygen-evolving complex for the S0–S1, S1–S2, and S2–S3 transitions of the water oxidation cycle. Biochemistry 37(49):17112–17119

    PubMed  CAS  Google Scholar 

  • Jahns P, Lavergne J, Rappaport F, Junge W (1991) Stoichiometry of proton release during photosynthetic water oxidation a reinterpretation of the responses of neutral red leads to a non-integer pattern. Biochim Biophys Acta 1057(3):313–319

    CAS  Google Scholar 

  • Jenson DL, Barry BA (2009) Proton-coupled electron transfer in photosystem II: proton inventory of a redox active tyrosine. J Am Chem Soc 131(30):10567–10573. doi:10.1021/Ja902896e

    PubMed  CAS  Google Scholar 

  • Joliot P, Barbieri G, Chabaud R (1969) Un nouveau modele des centres photochimique du systeme II. Photochem Photobiol 10:309–329

    CAS  Google Scholar 

  • 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(1426):1407–1417

    PubMed  CAS  Google Scholar 

  • Kawakami K, Umena Y, Kamiya N, Shen JR (2011) Structure of the catalytic, inorganic core of oxygen-evolving photosystem II at 1.9 Å resolution. J Photochem Photobiol, B 104(1–2):9–18. doi:10.1016/j.jphotobiol.2011.03.017

    CAS  Google Scholar 

  • Klauss A, Haumann M, Dau H (2012) Alternating electron and proton transfer steps in photosynthetic water oxidation. Proc Natl Acad Sci USA 109(40):16035–16040. doi:10.1073/pnas.1206266109

    PubMed  CAS  Google Scholar 

  • Koike H, Inoue Y (1987) A low-temperature-sensitive intermediate state between S2 and S3 in photosynthetic water oxidation deduced by means of thermoluminescence measurements. Biochim Biophys Acta 894(3):573–577

    CAS  Google Scholar 

  • Koike H, Hanssum B, Inoue Y, Renger G (1987) Temperature dependence of the S-state transitions in a thermophilic cyanobacterium, Synechococcus vulcanus Copeland measured by absorption changes in the ultraviolet region. Biochim Biophys Acta 893:524

    CAS  Google Scholar 

  • Kok B, Forbush B, McGloin M (1970) Cooperation of charges in photosynthetic oxygen evolution: I. a linear four step mechanism. Photochem Photobiol 11:457–475

    PubMed  CAS  Google Scholar 

  • Krammer EM, Till MS, Sebban P, Ullmann GM (2009) Proton-transfer pathways in photosynthetic reaction centers analyzed by profile hidden markov models and network calculations. J Mol Biol 388(3):631–643. doi:10.1016/j.jmb.2009.03.020

    PubMed  CAS  Google Scholar 

  • Krishtalik LI (1986) Energetics of multielectron reactions: photosynthetic oxygen evolution. Biochim Biophys Acta 849(1):162–171

    CAS  Google Scholar 

  • Krishtalik LI (2000) The mechanism of the proton transfer: an outline. Biochim Biophys Acta 1458(1):6–27. doi:10.1016/S0005-2728(00)00057-8

    PubMed  CAS  Google Scholar 

  • Kuhne H, Brudvig GW (2002) Proton-coupled electron transfer involving tyrosine Z in photosystem II. J Phys Chem B 106(33):8189–8196. doi:10.1021/jp0206222

    Google Scholar 

  • Kusunoki M (2011) S1-state Mn4Ca complex of photosystem II exists in equilibrium between the two most-stable isomeric substrates: XRD and EXAFS evidence. J Photochem Photobiol, B 104(1–2):100–110. doi:10.1016/j.jphotobiol.2011.03.002

    CAS  Google Scholar 

  • Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438(7070):1040–1044

    PubMed  CAS  Google Scholar 

  • Lubbers K, Haumann M, Junge W (1993) Photosynthetic water oxidation under flashing light. Oxygen release, proton release, and absorption transients in the near ultraviolet: a comparison between thylakoids and a reaction center preparation. Biochim Biophys Acta 1183:210–214

    Google Scholar 

  • McEvoy JP, Brudvig GW (2004) Structure-based mechanism of photosynthetic water oxidation. Phys Chem Chem Phys 6(20):4754–4763. doi:10.1039/B407500e

    CAS  Google Scholar 

  • McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106(11):4455–4483

    PubMed  CAS  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767(6):414–421. doi:10.1016/j.bbabio.2006.11.019

    PubMed  CAS  Google Scholar 

  • Murray JW, Barber J (2007) Structural characteristics of channels and pathways in photosystem II including the identification of an oxygen channel. J Struct Biol 159(2):228–237. doi:10.1016/j.jsb.2007.01.016

    PubMed  CAS  Google Scholar 

  • Noguchi T, Suzuki H, Tsuno M, Sugiura M, Kato C (2012) Time-resolved infrared detection of the proton and protein dynamics during photosynthetic oxygen evolution. Biochemistry 51(15):3205–3214. doi:10.1021/bi300294n

    PubMed  CAS  Google Scholar 

  • Ono TA, Noguchi T, Inoue Y, Kusunoki M, Matsushita T, Oyanagi H (1992) X-ray detection of the period-four cycling of the manganese cluster in photosynthetic water oxidizing enzyme. Science 258(5086):1335–1337

    PubMed  CAS  Google Scholar 

  • Pecoraro VL, Baldwin MJ, Caudle MT, Hsieh W-Y, Law N (1998) A proposal for water oxidation in photosystem II. Pure Appl Chem 70:925–929

    CAS  Google Scholar 

  • Petrek M, Otyepka M, Banas P, Kosinova P, Koca J, Damborsky J (2006) CAVER: a new tool to explore routes from protein clefts, pockets and cavities. BMC Bioinformatics 7:316. doi:10.1186/1471-2105-7-316

    PubMed  Google Scholar 

  • Polander BC, Barry BA (2012) A hydrogen-bonding network plays a catalytic role in photosynthetic oxygen evolution. Proc Natl Acad Sci USA 109(16):6112–6117. doi:10.1073/pnas.1200093109

    PubMed  CAS  Google Scholar 

  • Polander BC, Barry BA (2013) Detection of an intermediary, protonated water cluster in photosynthetic oxygen evolution. Proc Natl Acad Sci USA 110(26):10634–10639. doi:10.1073/pnas.1306532110

    PubMed  CAS  Google Scholar 

  • Pushkar Y, Yano J, Sauer K, Boussac A, Yachandra VK (2008) Structural changes in the Mn4Ca cluster and the mechanism of photosynthetic water splitting. Proc Natl Acad Sci USA 105(6):1879–1884. doi:10.1073/pnas.0707092105

    PubMed  CAS  Google Scholar 

  • Rappaport F, Lavergne J (1991) Proton release during successive oxidation steps of the photosynthetic water oxidation process: stoichiometries and pH-dependence. Biochemistry 30(41):10004–10012

    PubMed  CAS  Google Scholar 

  • Rappaport F, Lavergne J, Blanchard-Desce M (1994) Kinetics of electron transfer and electrochromic change during the redox transitions of the photosynthetic oxygen-evolving complex. Biochim Biophys Acta 1184(2/3):178–192

    CAS  Google Scholar 

  • Razeghifard MR, Pace RJ (1999) EPR kinetic studies of oxygen release in thylakoids and PSII membranes: a kinetic intermediate in the S3 to S0 transition. Biochemistry 38(4):1252–1257. doi:10.1021/bi9811765

    PubMed  CAS  Google Scholar 

  • Rivalta I, Amin M, Luber S, Vassiliev S, Pokhrel R, Umena Y, Kawakami K, Shen JR, Kamiya N, Bruce D, Brudvig GW, Gunner MR, Batista VS (2011) Structural-functional role of chloride in photosystem II. Biochemistry 50(29):6312–6315. doi:10.1021/bi200685w

    PubMed  CAS  Google Scholar 

  • Robblee JH, Messinger J, Cinco RM, McFarlane KL, Fernandez C, Pizarro SA, Sauer K, Yachandra VK (2002) The Mn cluster in the S(0) state of the oxygen-evolving complex of photosystem II studied by EXAFS spectroscopy: are there three Di-μ-oxo-bridged Mn(2) moieties in the tetranuclear Mn complex? J Am Chem Soc 124(25):7459–7471

    PubMed  CAS  Google Scholar 

  • Rutherford AW, Boussac A, Faller P (2004) The stable tyrosyl radical in Photosystem II: why D? Biochim Biophys Acta 1655(1–3):222–230

    PubMed  CAS  Google Scholar 

  • Saito K, Shen J-R, Ishida T, Ishikita H (2011) Short hydrogen bond between redox-active tyrosine YZ and D1-His190 in the photosystem II crystal structure. Biochemistry 50(45):9836–9844. doi:10.1021/bi201366j

    PubMed  CAS  Google Scholar 

  • Sauer K, Yano J, Yachandra VK (2005) X-ray spectroscopy of the Mn4Ca cluster in the water-oxidation complex of photosystem II. Photosynth Res 85(1):73–86

    PubMed  CAS  Google Scholar 

  • Schlodder E, Witt HT (1999) Stoichiometry of proton release from the catalytic center in photosynthetic water oxidation. J Biol Chem 274(43):30387–30392. doi:10.1074/jbc.274.43.30387

    PubMed  CAS  Google Scholar 

  • Service RJ, Hillier W, Debus RJ (2010) Evidence from FTIR difference spectroscopy of an extensive network of hydrogen bonds near the oxygen-evolving Mn(4)Ca cluster of photosystem II involving D1-Glu65, D2-Glu312, and D1-Glu329. Biochemistry 49(31):6655–6669. doi:10.1021/bi100730d

    PubMed  CAS  Google Scholar 

  • Siegbahn PEM (2012) Mechanisms for proton release during water oxidation in the S2 to S3 and S3 to S4 transitions in photosystem II. Phys Chem Chem Phys 14(14):4849–4856. doi:10.1039/c2cp00034b

    PubMed  CAS  Google Scholar 

  • Siegbahn PEM, Blomberg MRA (2009) A combined picture from theory and experiments on water oxidation, oxygen reduction and proton pumping. Dalton Trans 30:5832–5840. doi:10.1039/B903007g

    PubMed  Google Scholar 

  • Sjoholm J, Havelius KGV, Mamedov F, Styring S (2010) Effects of pH on the S3 state of the oxygen evolving complex in photosystem II probed by EPR split signal induction. Biochemistry 49(45):9800–9808. doi:10.1021/Bi101364t

    PubMed  Google Scholar 

  • Sproviero EM, Gascon JA, McEvoy JP, Brudvig GW, Batista VS (2008) Quantum mechanics/molecular mechanics study of the catalytic cycle of water splitting in photosystem II. J Am Chem Soc 130(11):3428–3442. doi:10.1021/ja076130q

    PubMed  CAS  Google Scholar 

  • Styring S, Rutherford AW (1987) In the oxygen evolving complex of photosystem II the S0 state is oxidized to the S1-state by D+ (Signal II-Slow). Biochemistry 26(9):2401–2405. doi:10.1021/bi00383a001

    CAS  Google Scholar 

  • Suzuki H, Sugiura M, Noguchi T (2009) Monitoring proton release during photosynthetic water oxidation in photosystem II by means of isotope-edited infrared spectroscopy. J Am Chem Soc 131(22):7849–7857. doi:10.1021/Ja901696m

    PubMed  CAS  Google Scholar 

  • Takizawa K, Cruz JA, Kanazawa A, Kramer DM (2007) The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf. Biochim Biophys Acta 1767(10):1233–1244

    PubMed  CAS  Google Scholar 

  • Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473(7345):55–60. doi:10.1038/nature09913

    PubMed  CAS  Google Scholar 

  • Vass I, Cser K (2009) Janus-faced charge recombinations in photosystem II photoinhibition. Trends Plant Sci 14(4):200–205. doi:10.1016/J.Tplants.2009.01.009

    PubMed  CAS  Google Scholar 

  • Vassiliev S, Comte P, Mahboob A, Bruce D (2010) Tracking the flow of water through photosystem II using molecular dynamics and streamline tracing. Biochemistry 49(9):1873–1881. doi:10.1021/bi901900s

    PubMed  CAS  Google Scholar 

  • Vassiliev S, Zaraiskaya T, Bruce D (2012) Exploring the energetics of water permeation in photosystem II by multiple steered molecular dynamics simulations. Biochim Biophys Acta 1817(9):1671–1678. doi:10.1016/j.bbabio.2012.05.016

    PubMed  CAS  Google Scholar 

  • Visser H, Anxolabehere-Mallart E, Bergmann U, Glatzel P, Robblee JH, Cramer SP, Girerd JJ, Sauer K, Klein MP, Yachandra VK (2001) Mn K-edge XANES and Kbeta XES studies of two Mn-oxo binuclear complexes: investigation of three different oxidation states relevant to the oxygen-evolving complex of photosystem II. J Am Chem Soc 123(29):7031–7039

    PubMed  CAS  Google Scholar 

  • Vrettos JS, Limburg J, Brudvig GW (2001) Mechanism of photosynthetic water oxidation: combining biophysical studies of photosystem II with inorganic model chemistry. Biochim Biophys Acta 1503(1–2):229–245

    PubMed  CAS  Google Scholar 

  • Westphal KL, Tommos C, Cukier RI, Babcock GT (2000) Concerted hydrogen-atom abstraction in photosynthetic water oxidation. Curr Opin Plant Biol 3(3):236–242

    PubMed  CAS  Google Scholar 

  • Wincencjusz H, Yocum CF, van Gorkom HJ (1999) Activating anions that replace Cl- in the O2-evolving complex of photosystem II slow the kinetics of the terminal step in water oxidation and destabilize the S2 and S3 states. Biochemistry 38(12):3719–3725

    PubMed  CAS  Google Scholar 

  • Wolf S, Freier E, Potschies M, Hofmann E, Gerwert K (2010) Directional proton transfer in membrane proteins achieved through protonated protein-bound water molecules: a proton diode. Angew Chem Int Ed Engl 49(38):6889–6893

    PubMed  CAS  Google Scholar 

  • Wraight CA (2006) Chance and design: proton transfer in water, channels and bioenergetic proteins. Biochim Biophys Acta 1757(8):886–912. doi:10.1016/J.Bbabio.2006.06.017

    PubMed  CAS  Google Scholar 

  • Xu DY, Liu XW, Zhao J, Zhao JD (2005) FesM, a membrane iron–sulfur protein, is required for cyclic electron flow around photosystem I and photoheterotrophic growth of the cyanobacterium Synechococcus sp PCC 7002. Plant Physiol 138(3):1586–1595. doi:10.1104/Pp.105.061549

    PubMed  CAS  Google Scholar 

  • Yamashita T, Voth GA (2011) Insights into the mechanism of proton transport in cytochrome c oxidase. J Am Chem Soc 134(2):1147–1152. doi:10.1021/ja209176e

    Google Scholar 

  • Yano J, Yachandra VK (2007) Oxidation state changes of the Mn(4)Ca cluster in photosystem II. Photosynth Res 92(3):289–303. doi:10.1007/s11120-007-9153-5

    PubMed  CAS  Google Scholar 

  • Yano J, Kern J, Sauer K, Latimer MJ, Pushkar Y, Biesiadka J, Loll B, Saenger W, Messinger J, Zouni A, Yachandra VK (2006) Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster. Science 314(5800):821–825

    PubMed  CAS  Google Scholar 

  • Zaharieva I, Wichmann JM, Dau H (2011) Thermodynamic limitations of photosynthetic water oxidation at high proton concentrations. J Biol Chem 286(20):18222–18228. doi:10.1074/Jbc.M111.237941

    PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank Prof. Richard Debus for the many useful discussions and supplying the Synechocystis mutants. Funding by the National Science Foundation MCB 1244586 (to RLB). This work was funded by the National Science Foundation (MCB-1244586 to RLB).

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  1. Department of Microbiology and Molecular Genetics, Oklahoma State University, 307 Life Sciences East, Stillwater, OK, 74078, USA

    Han Bao, Preston L. Dilbeck & Robert L. Burnap

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  1. Han Bao
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  2. Preston L. Dilbeck
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  3. Robert L. Burnap
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Correspondence to Robert L. Burnap.

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For Special issues on Photosynthesis Education which will honor Professors Govindjee and Pierre Joliot on the occasion of their 80th birthdays.

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Bao, H., Dilbeck, P.L. & Burnap, R.L. Proton transport facilitating water-oxidation: the role of second sphere ligands surrounding the catalytic metal cluster. Photosynth Res 116, 215–229 (2013). https://doi.org/10.1007/s11120-013-9907-1

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  • DOI: https://doi.org/10.1007/s11120-013-9907-1

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