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Mechanism of Photosynthetic Production and Respiratory Reduction of Molecular Dioxygen: A Biophysical and Biochemical Comparison

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Bioenergetic Processes of Cyanobacteria

Abstract

This chapter describes the role of the redox couple H2O/O2 as the cornerstone of biological Gibbs free energy transformation in all higher forms of life on earth.

After a short introduction into basic thermodynamic principles, a short description summarizes the general functional pattern of the two processes that perform these activities: (1) solar energy exploitation via photosynthetic water splitting and (2) Gibbs free energy extraction from food through oxygenic respiration. These reactions take place in multimeric protein complexes, which are anisotropically incorporated into specialized membrane systems, thus giving rise to transient “storage” of Gibbs free energy in form of a transmembrane electrochemical potential difference of protons that provides the driving force for ATP synthesis. Of key relevance in the overall processes are the reaction sequences of the redox couple H2O/O2 either in the forward (O2-formation) or in the backward (O2-consumption) direction taking place within two “molecular machines”: (1) Photosystem II (PS II) which acts as light driven plastoquinone-water:oxido-reductase and (2) cytochrome c oxidase (COX) acting as cytochrome c-oxygen:oxido-reductase.

In this chapter our current knowledge on the structural and functional properties of these two systems is described. Oxidative water splitting into molecular oxygen and four protons requires. the formation of a strongly oxidizing species and the cooperation of four electron abstraction steps from two water molecules. The former goal is achieved through functionalizing of chlorophyll a by a special protein matrix and the second task performed at manganese containing catalytic metal cluster. In COX the Gibbs free energy available from exergonic dioxygen reduction to water is transformed into a protein motive force by a special mechanism of proton pumping.

Open questions on the mechanism of both system (e.g. O–O bond formation in PS II and proton pumping in COX) are outlined and future perspectives discussed.

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Notes

  1. 1.

    The Gibbs free energy is defined as G = H – TS, where H and S are the enthalpy and entropy, respectively, and T is the absolute temperature (see Atkins 2001).

  2. 2.

    A X-ray diffraction crystallographic (XRDC) structure model of 1.9 Å resolution was reported by J.-R. Shen et al. (2010) at the 15th International Congress of Photosynthesis in Beijing (poster PS 6.5).

  3. 3.

    Alternative (Shelaev et al. 2008) and complementary (Romeo et al. 2010) pathways with PD1 as primary electron donor have also been discussed.

  4. 4.

    A theoretical analysis of EPR, ENDOR and ESEEM data led to the alternative conclusion that MnC rather than MnA attains the state Mn(III) in S2 (Schinzel et al. 2010).

References

  • Aartsma TJ, Matysik J (eds) (2008) Biophysical techniques in photosynthesis, Volume II. Advances in photosynthesis and respiration, Vol. 26, Springer, Dordrecht

    Book  Google Scholar 

  • Allakhverdiev SI, Tomo T, Shimada Y, Kindo H, Nagao R, Klimov VV and Mimuro M (2010) Redox potential of pheophytin a in Photosystem II of two cyanobacteria having the different special pair chlorophylls. Proc Natl Acad Sci 107: 3924–3929

    Article  PubMed  CAS  Google Scholar 

  • Amunts A, Drory O and Nelson N (2007) The structure of a plant Photosystem I supercomplex at 3.4 Å resolution. Nature 447: 58–63

    Article  PubMed  CAS  Google Scholar 

  • Anderson JM (2001) Does functional Photosystem II complex have an oxygen channel? FEBS Lett 488: 1–4

    Article  PubMed  CAS  Google Scholar 

  • Anderson AB and Albu TV (1999) Ab initio determination of reversible potentials and activation energies for outer-sphere oxygen reduction to water and the reverse oxidation reaction. J Am Chem Soc 121: 11855–11863

    Article  CAS  Google Scholar 

  • Aoyama H, Muramoto K, Shinzawa-Itoh K, Hirata K, Yamashita E, Tsukihara T, Ogura T and Yoshikawa S (2009) A peroxide bridge between Fe and Cu ions in the O2 reduction site of fully oxidized cytochrome c oxidase could suppress the proton pump. Proc Natl Acad Sci U S A 106: 2165–2169

    Article  PubMed  CAS  Google Scholar 

  • Atkins PW (2001) Physical Chemistry, Oxford University Press, Oxford

    Google Scholar 

  • Bader KP, Renger G and Schmidt GH (1993) A mass spectroscopic analysis of the water-splitting reaction. Photosynth Res 38: 355–361

    Article  CAS  Google Scholar 

  • Baker SC, Ferguson SJ, Ludwig B, Page MD, Richter O-MH and van Spanning RJM (1998) Molecular genetics of the genus Paracoccus—metabolically versatile bacteria with bioenergetic flexibility. Microbiol Mol Biol Rev 62: 1046–1078

    PubMed  CAS  Google Scholar 

  • Belevich I and Verkhovsky MI (2008) Molecular mechanism of proton translocation by cytochrome c oxidase. Antioxid Redox Sign 10: 1–29

    Article  CAS  Google Scholar 

  • Belevich I, Verkhovsky MI and Wikström M (2006) Proton-coupled electron transfer drives the proton pump of cytochrome c oxidase. Nature 440: 829–832

    Article  PubMed  CAS  Google Scholar 

  • Belevich I, Bloch DA, Belevich N, Wikström M and Verkhovsky MI (2007) Exploring the proton pump mechanism of cytochrome c oxidase in real time. Proc Natl Acad Sci U S A 104: 2685–2690

    Article  PubMed  CAS  Google Scholar 

  • Belevich I, Gorbikova E, Belevich NP, Rauhamäki V, Wikström M and Verkhovsky MI (2010) Initiation of the proton pump of cytochrome c oxidase. Proc Natl Acad Sci U S A 107: 18469–18474

    Article  PubMed  CAS  Google Scholar 

  • Benson AA (2002) Following the path of carbon in photosynthesis: A personal story. Photosynth Res 73: 29–49

    Article  PubMed  CAS  Google Scholar 

  • Bernarding J, Eckert H-J, Eichler H-J, Napiwotzki A and Renger G (1994) Kinetic studies on the stabilization of the primary radical pair P680+Pheo− in different Photosystem II preparations from higher plants. Photochm Photobiol 59: 566–573

    Article  CAS  Google Scholar 

  • Bertini I, Cavallaro G and Rosato A (2005) A structural model for the adduct between cytochrome c and cytochrome c oxidase. J Biol Inorg Chem 10: 613–624

    Article  PubMed  CAS  Google Scholar 

  • Bisson R, Steffens GCM, Capaldi RA and Buse G (1982) Mapping of the cytochrome c binding site on cytochrome c oxidase. FEBS Lett 144: 359–363

    Article  PubMed  CAS  Google Scholar 

  • Boltzmann L (1905) Der zweite Hauptsatz der mechanischen Wärmetheorie. In: Populäre Schriften, J. A. Barth, Leipzig (in German)

    Google Scholar 

  • Brand SE, Rajagukguk S, Ganesan K, Geren L, Fabian M, Han D, Gennis RB, Durham B and Millett F (2007) A new ruthenium complex to study single-electron reduction of the pulsed O(H) state of detergent-solubilized cytochrome oxidase. Biochemistry 46: 14610–14618

    Article  PubMed  CAS  Google Scholar 

  • Bränden G, Pawate AS, Gennis RB and Brzezinski P (2006) Controlled uncoupling and recoupling of proton pumping in cytochrome c oxidase. Proc Natl Acad Sci U S A 103: 317–322

    Article  PubMed  CAS  Google Scholar 

  • Bratton MR, Pressler MA and Hosler JP (1999) Suicide inactivation of cytochrome c oxidase: Catalytic turnover in the absence of subunit III alters the active site. Biochemistry 38: 16236–16245

    Article  PubMed  CAS  Google Scholar 

  • Brzezinski P and Gennis RB (2008) Cytochrome c oxidase: Exciting progress and remaining mysteries. J Bioenerg Biomembr 40: 521–531

    Article  PubMed  CAS  Google Scholar 

  • Budiman K, Kannt A, Lyubenova S, Richter O-MH, Ludwig B, Michel H and MacMillan F (2004) Tyrosine-167: The origin of the radical species observed in the reaction of cytochrome c oxidase with hydrogen peroxide in Paracoccus denitrificans. Biochemistry 43: 11709–11716

    Article  PubMed  CAS  Google Scholar 

  • Buick R (1992) The antiquity of oxygenic photosynthesis; evidence from stromatolites in sulphate-deficient Archaen lakes. Science 255: 74–77

    Article  PubMed  CAS  Google Scholar 

  • Bundschuh FA, Hoffmeier K and Ludwig B (2008) Two variants of the assembly factor Surf1 target specific terminal oxidases in Paracoccus denitrificans. Biochim Biophys Acta 1777: 1336–1343

    Article  PubMed  CAS  Google Scholar 

  • Burda K, Bader KP and Schmid GH (2001) An estimation of the size of the water cluster present at the cleavage site of the water splitting enzyme. FEBS Lett 491: 81–84

    Article  PubMed  CAS  Google Scholar 

  • Buse G, Soulimane T, Dewor M, Meyer HE and Blüggel M (1990) Evidence for a copper-coordinated histidine-tyrosine cross-link in the active site of cytochrome oxidase. Protein Sci 8: 985–990

    Article  Google Scholar 

  • Calvin M (1989) Forty years of photosynthesis and related activities. Photosynth Res 21: 3–16

    Google Scholar 

  • Castelfranco PA, Lu Y-K and Stemler AJ (2007) Hypothesis: The peroxydicarbonic acid cycle in photosynthetic oxygen evolution. Photosynth Res 94: 235–246

    Article  PubMed  CAS  Google Scholar 

  • Chakrabarty S, Namslauer I, Brzezinski P and Warshel A (2011) Exploration of the cytochrome c oxidase pathway puzzle and examination of the origin of elusive mutational effects. Biochim Biophys Acta 1807: 413–426

    Google Scholar 

  • Chow WS and Aro EM (2005) Photoinactivation and mechanism of recovery In: Wydrzynski T and Satoh K (eds) Photosystem II: The water/plastoquinone oxido-reductase in photosynthesis, advances in photosynthesis and respiration, Vol. 22, Springer, Dordrecht, pp 627–648

    Google Scholar 

  • Clausen J and Junge W (2004) Detection of an intermediate of photosynthetic water oxidation. Nature 430: 480–483

    Article  PubMed  CAS  Google Scholar 

  • Clausen J, Debus RJ and Junge W (2004) Time-resolved oxygen production by PS II: Chasing chemical intermediates. Biochim Biophys Acta 1655: 184–194

    Article  PubMed  CAS  Google Scholar 

  • Clausen J, Beckmann K, Junge W and Messinger J (2005) Evidence that bicarbonate is not the substrate in photosynthetic oxygen evolution. Plant Physiol 139: 1444–1450

    Article  PubMed  CAS  Google Scholar 

  • Cukier RI (2002) A theory that connects proton-coupled electron-transfer and hydrogen-atom transfer reactions. J Phys Chem B 106: 1746–1757

    Article  CAS  Google Scholar 

  • Cukier RI (2004) Quantum molecular dynamics simulation of proton transfer in cytochrome c oxidase. Biochim Biophys Acta 1656: 189–202

    Article  PubMed  CAS  Google Scholar 

  • Danielsson R, Suorsa M, Paakkarinen V, Albertsson P-Å, Styring S, Aro E-M, and Mamedov F (2006) Dimeric and monomeric organization of Photosystem II. Distribution of five distinct complexes in the different domains of the thylakoids membrane. J Biol Chem 281: 14241–14249

    Article  PubMed  CAS  Google Scholar 

  • de Grotthuss CJT (2006) Memoir on the decomposition of water and of the bodies that it holds in solution by means of galvanic electricity. Biochim Biophys Acta 1757: 871–875

    Article  PubMed  CAS  Google Scholar 

  • de Marais DJ (2000) Evolution. When did photosynthesis emerge on Earth? Science 289: 1703–1705

    PubMed  CAS  Google Scholar 

  • de Wijn R and van Gorkom HJ (2001) Kinetics of electron transfer from QA to QB in Photosystem II. Biochemistry 40: 11912–11922

    Article  PubMed  CAS  Google Scholar 

  • Drosou V, Malatesta F and Ludwig B (2002a) Mutations in the docking site for cytochrome c on the Paracoccus heme aa 3 oxidase: Electron entry and kinetic phases of the reaction. Eur J Biochem 269: 2980–2988

    Article  CAS  Google Scholar 

  • Drosou V, Reincke B, Schneider M and Ludwig B (2002b) Specificity of interaction between the Paracoccus denitrificans oxidase and its substrate cytochrome c: Comparing the mitochondrial to the homologous bacterial cytochrome c 552, and its truncated and site-directed mutants. Biochemistry 41: 10629–10634

    Article  CAS  Google Scholar 

  • Dürr K, Koepke J, Hellwig P, Müller H, Angerer H, Peng G, Olkova E, Richter O-MH, Ludwig B and Michel H (2008) A D-pathway mutation decouples the Paracoccus denitrificans cytochrome c oxidase by altering the side chain orientation of a distant, conserved glutamate. J Mol Biol 384: 865–877

    Article  PubMed  CAS  Google Scholar 

  • Fabian M and Palmer G (1995) The interaction of cytochrome oxidase with hydrogen peroxide: The relationship of compounds P and F. Biochemistry 34: 13802–13810

    Article  PubMed  CAS  Google Scholar 

  • Fadda E, Yu CH and Pomès R (2008) Electrostatic control of proton pumping in cytochrome c oxidase. Biochim Biophys Acta 1777: 277–284

    Article  PubMed  CAS  Google Scholar 

  • Farver O, Grell E, Ludwig B, Michel H and Pecht I (2006) Rates and equilibrium of CuA to heme a electron transfer in Paracoccus denitrificans cytochrome c oxidase. Biophys J 90: 2131–2137

    Article  PubMed  CAS  Google Scholar 

  • Faxen K, Gilderson G, Ädelroth P and Brzezinski P (2005) A mechanistic principle for proton pumping by cytochrome c oxidase. Nature 437: 286–289

    Article  PubMed  CAS  Google Scholar 

  • Fee JA, Case DA and Noodleman L (2008) Toward a chemical mechanism of proton pumping by the B-Type cytochrome c oxidases: Application of density functional theory to cytochrome ba 3 of Thermus thermophilus. J Am Chem Soc 130: 15002–15021

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Flöck D and Helms V (2002) Protein–protein docking of electron transfer complexes: Cytochrome c oxidase and cytochrome c. Proteins 47: 75–85

    Article  PubMed  CAS  Google Scholar 

  • Florens L, Schmidt B, McCracken J and Ferguson-Miller S (2001) Fast deuterium access to the buried magnesium/manganese site in cytochrome c oxidase. Biochemistry 40: 7491–7497

    Article  PubMed  CAS  Google Scholar 

  • Fontanesi F, Soto IC, Horn D and Barrientos A (2006) Assembly of mitochondrial cytochrome c-oxidase, a complicated and highly regulated cellular process. Am J Physiol Cell Physiol 291: 1129–1147

    Article  CAS  Google Scholar 

  • Fromme R, Grotjohann I and Fromme P (2008) Structure and function of photosystem I. In: Renger G (ed) Primary processes of photosynthesis: Principles and apparatus, Part II reaction centers/photosystems, electron transport chains, photophosphorylation and evolution, Royal Society Chemistry, Cambridge, pp 111–146

    Google Scholar 

  • Fufezan C, Gross CM, Sjödin M, Rutherford AW, Krieger-Liszkay A and Kirilovsky D (2007) Influence of the redox potential of the primary quinone electron acceptor on photoinhibition in Photosystem II. J Biol Chem 282: 12492–12502

    Article  PubMed  CAS  Google Scholar 

  • Fukuda R, Zhang H, Kim, J, Shimoda L, Dang CV and Semenza GL (2007) HIF-1 Regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 129: 111–122

    Article  PubMed  CAS  Google Scholar 

  • Gabdulkhakov A, Guskov A, Broser M, Kern J, Müh F, Saenger W and Zouni A (2009) Probing the accessibility of the Mn4Ca cluster in Photosystem II: Channels calculation, noble gas derivatization, and cocrystallization with DMSO. Structure 17: 1223–1234

    Article  PubMed  CAS  Google Scholar 

  • Genova ML, Baracca A, Biondi A, Casalena G, Faccioli M, Falasca AI, Formiggini G, Sgarbi G, Solaini G and Lenaz G (2008) Is supercomplex organization of the respiratory chain required for optimal electron transfer activity? Biochim Biophys Acta 1777: 740–774

    Article  PubMed  CAS  Google Scholar 

  • Gibasiewicz K, Dobek A, Breton J and Leibl W (2001) Modulation of primary radical pair kinetics and energetics in Photosystem II by the redox state of the quinone electron acceptor QA. Biophys J 80: 1617–1630

    Article  PubMed  CAS  Google Scholar 

  • Gilbert DL (ed) (1981) Oxygen and living processes: An interdisciplinary approach, Springer, New York

    Book  Google Scholar 

  • Giuffrè A, Forte E, Antonini A, D’Itri E, Brunori M, Soulimane T and Buse G (1999) Kinetic properties of ba 3 oxidase from thermus thermophilus: Effect of temperature. Biochemistry 38: 1057–1065

    Article  PubMed  Google Scholar 

  • Glatzel P, Bergmann U, Yano J, Visser H, Robblee JH, Gu WW, de Groot FMF, Christou G, Pecoraro VL, Cramer SP and Yachandra VK (2004) The electronic structure of Mn in oxides, coordination complexes, and the oxygen-evolving complex of Photosystem II studied by resonant inelastic X-ray scattering. J Am Chem Soc 126: 9946–9959

    Article  PubMed  CAS  Google Scholar 

  • Gorbikova EA, Belevich I, Wikström M and Verkhovsky MI (2008a) The proton donor for O–O bond scission by cytochrome c oxidase. Proc Natl Acad Sci U S A 105: 10733–10737

    Article  CAS  Google Scholar 

  • Gorbikova EA, Wikström M and Verkhovsky MI (2008b) The protonation state of the cross-linked tyrosine during the catalytic cycle of cytochrome c oxidase. J Biol Chem 283: 34907–34912

    Article  CAS  Google Scholar 

  • Govindjee, Beatty JT, Gest H and Allen JF (eds) (2005) Discoveries in photosynthesis. Advances in photosynthesis and respiration, Vol. 20, Springer, Dordrecht

    Google Scholar 

  • Greiner P, Hannappel A, Werner C and Ludwig B (2008) Biogenesis of cytochrome c oxidase—bacterial approaches to study cofactor insertion into subunit I. Biochim Biophys Acta 1777: 904–911

    Article  PubMed  CAS  Google Scholar 

  • Groot ML, Pawlowicz NP, van Wilderen LJGW, Breton J, van Stokkum IHM and van Grondelle R (2005) Initial electron donor and acceptor in isolated photosystem II reaction centers identified with femtosecond mid-IR spectroscopy. Proc Natl Acad Sci U S A 102: 13087–13092

    Article  PubMed  CAS  Google Scholar 

  • Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A and Saenger W (2009) Cyanobacterial Photosystem II at 2.9 Å resolution and the role of quinones, lipids, channels and chloride. Nature Struct Mol Biol 16: 334–342

    Article  CAS  Google Scholar 

  • Haltia T, Saraste M and Wikström M (1991) Subunit III of cytochrome c oxidase is not involved in proton translocation: A site-directed mutagenesis study. EMBO J 10: 2015–2021

    PubMed  CAS  Google Scholar 

  • Hamza I and Gitlin JD (2002) Copper chaperones for cytochrome c oxidase and human disease. J Bioenerg Biomembr 34: 381–388

    Article  PubMed  CAS  Google Scholar 

  • Hammes-Schiffer S (2006) Hydrogen tunneling and protein motion in enzyme reactions. Acc Chem Res 39: 93–100

    Article  PubMed  CAS  Google Scholar 

  • Hansson Ö, Andreasson LE and Vänngard T (1986) Oxygen from water is coordinated to manganese in the S2 state of Photosystem II. FEBS Lett 195: 151–154

    Article  CAS  Google Scholar 

  • Harrenga A, Reincke B, Rüterjans H, Ludwig B and Michel H (2000) Structure of the soluble domain of cytochrome c 552 from Paracoccus denitrificans in the oxidized and reduced states. J Mol Biol 295: 667–678

    Article  PubMed  CAS  Google Scholar 

  • Hasegawa K and Noguchi T (2005) Density functional theory calculations on the dielectric-constant dependence of the oxidation potential of chlorophyll: Implication for the high potential of P680 in Photosystem II. Biochemistry 44: 8865–8872

    Article  PubMed  CAS  Google Scholar 

  • Hellwig P, Behr J, Ostermeier C, Richter O-MH, Pfitzner U, Odenwald A, Ludwig B, Michel H and Mäntele W (1998) Involvement of Glutamic Acid 278 in the Redox Reaction of the Cytochrome c Oxidase from Paracoccus denitrificans investigated by FTIR Spectroscopy. Biochemistry 37: 7390–7399

    Article  PubMed  CAS  Google Scholar 

  • Hendler RW, Pardhasaradhi K, Reynafarje B and Ludwig B (1991) Comparison of energy-transducing capabilities of the two- and three-subunit cytochromes aa 3 from Paracoccus denitrificans and the 13-subunit beef heart enzyme. Biophys J 60: 415–423

    Article  CAS  Google Scholar 

  • Hill BC (1994) Modeling the sequence of electron transfer reactions in the single turnover of reduced, mammalian cytochrome c oxidase with oxygen. J Biol Chem 269: 2419–2425

    PubMed  CAS  Google Scholar 

  • Hillier W and Messinger J (2005) Mechanism of photosynthetic oxygen production In: Wydrzynski T and Satoh K (eds) Photosystem II. The light-driven water: Plastoquinone oxidoredutase, Advances in photosynthesis and respiration, Vol. 22, Springer, Dordrecht, pp 567–608

    Google Scholar 

  • Hillier W, McConnell I, Badger MR, Boussac A, Klimov VV, Dismukes GC and Wydrzynski T (2006) Quantitative assessment of intrinsic carbonic anhydrase activity and the capacity for bicarbonate oxidation in Photosystem II. Biochemistry 45: 2094–2102

    Article  PubMed  CAS  Google Scholar 

  • Hillier W and Wydrzynski T (2008) 18O-water exchange in Photosystem II: Substrate binding and intermediates of the water splitting cycle. Coord Chem Rev 252: 306–317

    Article  CAS  Google Scholar 

  • Hiser L, Di Valentin M, Hamer AG and Hosler JP (2000) Cox11p is required for stable formation of the CuB and magnesium centers of cytochrome c oxidase. J Biol Chem 275: 619–623

    Article  PubMed  CAS  Google Scholar 

  • Ho FM and 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: 140–153

    Article  PubMed  CAS  Google Scholar 

  • Holzwarth AR, Müller MG, Reus M, Nowaczyk M, Sander J and Rögner M (2006) Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: Pheophytin is the primary electron donor. Proc Natl Acad Sci U S A 103: 6895–6900

    Article  PubMed  CAS  Google Scholar 

  • Hosler JP, Ferguson-Miller S, Calhoun MW, Thomas JW, Hill J, Lemieux L, Ma J, Georgiou C, Fetter J, Shapleigh J, Tecklenburg MMJ, Babcock GT and Gennis RB (1993) Insight into the active site structure and function of cytochrome oxidase by analysis of site-directed mutants of bacterial cytochrome aa 3 and cytochrome bo. J Bioenerg Biomembr 25: 121–136

    Article  PubMed  CAS  Google Scholar 

  • Hosler JP, Ferguson-Miller S and Mills DA (2006) Energy Transduction: Proton transfer through the respiratory complexes. Ann Rev Biochem 75: 165–187

    Article  PubMed  CAS  Google Scholar 

  • Hunter CN, Daldal F, Thurnauer MC and Beatty JT (eds) (2008) The purple phototrophic bacteria. Advances in photosynthesis and respiration, Vol. 28, Springer, Dordrecht

    Google Scholar 

  • Huynh MHV and Meyer TJ (2007) Proton-coupled electron transfer. Chem Rev 107: 5004–5064

    Article  PubMed  CAS  Google Scholar 

  • Ishida N, Sugiura M, Rappaport F, Lai T-L, Rutherford AW and Boussac A (2008) Biosynthetic exchange of bromide for chloride and strontium for calcium in the Photosystem II oxygen-evolving enzymes. J Biol Chem 283: 13330—13340

    Article  PubMed  CAS  Google Scholar 

  • Ishikita H, Knapp E-W (2005) Control of quinone redox potentials in Photosystem II: Electron transfer and photoprotection. J Am Chem Soc 127: 14714–14720

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Iwata S, Ostermeier C, Ludwig B and Michel H (1995) Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376: 660–669

    Article  PubMed  CAS  Google Scholar 

  • Janzon J, Ludwig B and Malatesta F (2007) Electron transfer kinetics of soluble fragments indicate a direct interaction between complex III and the caa 3 oxidase in Thermus thermophilus. IUBMB Life 59: 563–569

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Junge W (2008) Evolution of photosynthesis. In: Renger G (ed) Primary processes of photosynthesis: Priniciples and apparatus, Part II reaction centers/photosystems, electron transport chains, photophosphorylation and evolution, Royal Society Chemistry, Cambridge, pp 447–487

    Google Scholar 

  • Kaila VRI, Verkhovsky M, Hummer G and Wikström M (2008a) Prevention of leak in the proton pump of cytochrome c oxidase. Biochim Biophys Acta 1777: 890–892

    Article  CAS  Google Scholar 

  • Kaila VRI, Verkhovsky M, Hummer G and Wikström M (2008b) Glutamic acid 242 is a valve in the proton pump of cytochrome c oxidase. Proc Natl Acad Sci U S A 105: 6255–6259

    Article  CAS  Google Scholar 

  • Kaila VRI, Johansson MP, Sundholm D, Laakkonen L and Wikström M (2009) The chemistry of the CuB site in cytochrome c oxidase and the importance of its unique His–Tyr bond. Biochim Biophys Acta 1787: 223–233

    Google Scholar 

  • Kaila VR, Verkhovsky MI and Wikström M (2010) Proton-coupled electron transfer in cytochrome oxidase. Chem Rev 110: 7062–7081

    Article  PubMed  CAS  Google Scholar 

  • Kaminskaya O, Shuvalov VA and Renger G (2007) Evidence for a novel quinone binding site in the Photosystem II (PS II) complex which regulates the redox potential of Cyt b559. Biochemistry 46: 1091–1105

    Article  PubMed  CAS  Google Scholar 

  • Kamiya N and Shen J-R (2003) Crystal structure of oxygen-evolving Photosystem II from Thermosynechococcus vulcanus at 3.7 Å resolution. Proc Natl Acad Sci U S A 100: 98–103

    Article  PubMed  CAS  Google Scholar 

  • Kannt A, Soulimane T, Buse G, Becker A, Bamberg E and Michel H (1998) Electrical current generation and proton pumping catalyzed by the ba 3-type cytochrome c oxidase from Thermus thermophilus. FEBS Lett 434: 17–22

    Article  PubMed  CAS  Google Scholar 

  • Karge M, Irrgang K-D and 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

    Article  PubMed  CAS  Google Scholar 

  • Karpefors M, Ädelroth P and Brzezinski P (2000) Localized control of proton transfer through the D-pathway in cytochrome c oxidase: application of the proton-inventory technique. Biochemistry 39: 6850–6856

    Article  PubMed  CAS  Google Scholar 

  • Kasting JF and Seifert JF (2002) Life and the evolution of earth’s atmosphere. Science 296: 1066–1067

    Article  PubMed  CAS  Google Scholar 

  • Käß H, MacMillan F, Ludwig B and Prisner TF (2000) Investigation of the Mn binding site in cytochrome c oxidase from Paracoccus denitrificans by high-frequency EPR. J Phys Chem 104: 5362–5371

    Google Scholar 

  • Kato Y, Sugiura M, Oda A and Watanabe T (2009) Spectroelectrochemical determination of the redox potential of pheophytin a, the primary electron acceptor in Photosystem II. Proc Natl Acad Sci U S A 106: 17365–17370

    Article  CAS  Google Scholar 

  • Kern J and Renger G (2007) Photosystem II: structure and mechanism of the water:plastoquinone oxidoreductase. Photosynth Res 94: 183–202

    Article  PubMed  CAS  Google Scholar 

  • Khalimonchuk O and Winge DR (2008) Function and redox state of mitochondrial localized cysteine-rich proteins important in the assembly of cytochrome c oxidase. Biochim Biophys Acta 1783: 618–628

    Article  PubMed  CAS  Google Scholar 

  • Kirichenko AV, Pfitzner U, Ludwig B, Soares CM, Vygodina TV and Konstantinov AA (2005) Cytochrome c oxidase as a calcium binding protein. Studies on the role of a conserved aspartate in helices XI–XII cytoplasmic loop in cation binding. Biochemistry 44: 12391–12401

    Article  PubMed  CAS  Google Scholar 

  • Klimov VV, Allakhverdiev SI, Demeter S and Krasnovsky AA (1979) Photoreduction of pheophytin in Photosystem II of chloroplasts as a function of redox potential of the medium. Dokl Adad Nauk SSSR 249: 227–230

    CAS  Google Scholar 

  • Kobayashi M, Ohashi S, Iwamoto K, Shiraiwa Y, Kato Y and Watanabe T (2007) Redox potential of chlorophyll d in vitro. Biochim Biophys Acta 1767: 596–602

    Article  PubMed  CAS  Google Scholar 

  • Koepke J, Olkhova E, Angerer H, Müller H, Peng G and Michel H (2009) High resolution crystal structure of Paracoccus dentrificans cytochrome c oxidase: New insights into the active site and the proton transfer pathways. Biochim Biophys Acta 1787(6): 635–645

    Article  PubMed  CAS  Google Scholar 

  • Koike H, Hanssum B, Inoue Y and 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: 524–533

    Article  CAS  Google Scholar 

  • Kok B, Forbush B and McGloin M (1970) Cooperation of charges in photosynthetic O2 evolution. Photochem Photobiol 11: 457–476

    Article  PubMed  CAS  Google Scholar 

  • Kolling DRJ, Brown TS, Ananyev G and Dismukes GC (2009) Photosynthetic oxygen evolution is not reversed at high oxygen pressures: Mechanistic consequences for the water-oxidizing complex. Biochemistry 48: 1381–1389

    Article  PubMed  CAS  Google Scholar 

  • Konstantinov AA, Siletsky S, Mitchell D, Kaulen A and Gennis RB (1997) The roles of the two proton input channels in cytochrome c oxidase from Rhodobacter sphaeroides probed by the effects of site-directed mutations on time-resolved electrogenic intraprotein proton transfer. Proc Natl Acad Sci U S A 94: 9085–9090

    Article  PubMed  CAS  Google Scholar 

  • Krause F, Reifschneider NH, Vocke D, Seelert H, Rexroth S and Dencher NA (2004) “Respirasome”-like supercomplexes in green leaf mitochondria of spinach. J Biol Chem 279: 48369–48375

    Article  PubMed  CAS  Google Scholar 

  • Krieger-Liszkay A and Rutherford AW (1998) Influence of herbicide binding on the redox potential of teh quinone acceptor in photosystem II: Relevance to photodamage and phototoxicity. Biochemistry 37: 17339–17344

    Article  PubMed  CAS  Google Scholar 

  • Krieger A, Rutherford AW and Johnson GN (1995) On the determination of redox midpoint potential of the primary quinone electron-acceptor, Q(a), in Photosystem II. Biochim Biophys Acta 1229: 193–201

    Article  Google Scholar 

  • Kühn P, Eckert H-J, Eichler H-J and Renger G (2004) Analysis of the P680+• reduction pattern and its temperature dependence in oxygen-evolving PS II core complexes from thermophilic cyanobacteria and higher plants. Phys Chem Chem Phys 6: 4838–4843

    Article  CAS  Google Scholar 

  • Kulik LV, Epel B, Lubitz W and Messinger J (2007) Electronic structure of the Mn4OXCa cluster in the S0 and S2 states of the oxygen-evolving complex of Photosystem II based on pulse 55Mn-ENDOR and EPR spectroscopy. J Am Chem Soc 129: 13421–13435

    Article  PubMed  CAS  Google Scholar 

  • Lancaster R (2008) Structures of reaction centers in anoxygenic bacteria. In: Renger G (ed) Primary processes of photosynthesis: Priniciples and apparatus, Part II reaction centers/photosystems, electron transport chains, photophosphorylation and evolution, Royal Society Chemistry, Cambridge, pp 5–56

    Google Scholar 

  • Lane N (2002) Oxygen—the molecule that made the World. Oxford University Press, Oxford

    Google Scholar 

  • Larkum AWD (2008) The evolution of photosynthesis. In: Renger G (ed) Primary processes of photosynthesis: Priniciples and apparatus, Part II reaction centers/photosystems, electron transport chains, photophosphorylation and evolution, Royal Society Chemistry, Cambridge, pp 491–521

    Google Scholar 

  • Lee A, Kirichenko L, Vygodina T, Siletsky SA, Das TK, Rousseau DL, Gennis R and Konstantinov AA (2002) Ca(2+)-binding site in Rhodobacter sphaeroides cytochrome C oxidase. Biochemistry 41: 8886–8898

    Article  PubMed  CAS  Google Scholar 

  • Lee H, Das TK, Rousseau DL, Mills D, Ferguson-Miller S and Gennis RB (2000) Mutations in the putative H-channel in the cytochrome c oxidase from Rhodobacter sphaeroides show that this channel is not important for proton conduction but reveal modulation of the properties of heme a. Biochemistry 39: 2989–2996

    Article  PubMed  CAS  Google Scholar 

  • Lepp H, Salomonsson L, Zhu JP, Gennis RB and Brzezinski P (2008a) Impaired proton pumping in cytochrome c oxidase upon structural alteration of the D pathway. Biochim Biophys Acta 1777: 897–903

    Article  CAS  Google Scholar 

  • Lepp H, Svahn E, Faxén K and Brzezinski P (2008b) Charge transfer in the K proton pathway linked to electron transfer to the catalytic site in cytochrome c oxidase. Biochemistry 47: 4929–4935

    Article  CAS  Google Scholar 

  • Liang W, Roelofs TA, Cinco RM, Rompel A, Latimer MJ, Yu WO, Sauer K, Klein MP and Yachandra VK (2000) Structural change of the Mn cluster during the S2 to S3 state transition of the oxygen evolving complex of Photosystem II. Does it reflect the onset of water/substrate oxidation? Determination by Mn x-ray absorption spectroscopy. J Am Chem Soc 122: 3399–3412

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ludwig B and Gibson QH (1981) Reacton of oxygen with cytochrome c oxidase from Paracoccus denitrificans. J Biol Chem 256: 10092–10098

    PubMed  CAS  Google Scholar 

  • Ludwig B and Schatz G (1980) A Two-Subunit Cytochrome c Oxidase (Cytochrome aa 3) from Paracoccus denitrificans. Proc Natl Acad Sci USA 77: 196–200

    Article  PubMed  CAS  Google Scholar 

  • Luna VM, Chen Y, Fee JA and Stout CD (2008) Crystallographic studies of Xe and Kr binding within the large internal cavity of cytochrome ba 3 from Thermus thermophilus: structural analysis and role of oxygen transport channels in the heme-Cu oxidases. Biochemistry 47: 4657–4665

    Article  PubMed  CAS  Google Scholar 

  • Lyubenova S, Siddiqui K, Penning de Vries M, Ludwig B and Prisner TF (2007) Protein-protein interactions studied by EPR relaxation measurements: cytochrome c and cytochrome c oxidase. J Phys Chem B 111: 3839–3846

    Article  PubMed  CAS  Google Scholar 

  • MacMillan F, Kannt A, Behr J, Prisner T and Michel H (1999) Direct evidence for a tyrosine radical in the reaction of cytochrome c oxidase with hydrogen peroxide. Biochemistry 38: 9179–9184

    Article  PubMed  CAS  Google Scholar 

  • MacMillan F, Budiman K, Angerer H and Michel H (2006) The role of tryptophan 272 in the Paracoccus denitrificans cytochrome c oxidase. FEBS Lett 580: 1345–1349

    Article  PubMed  CAS  Google Scholar 

  • Maneg O, Ludwig B and Malatesta F (2003) Different interaction modes of two cytochrome c oxidase soluble CuA fragments with their substrates. J Biol Chem 278: 46734–46740

    Article  PubMed  CAS  Google Scholar 

  • Maneg O, Malatesta F, Ludwig B and Drosou V (2004) Interaction of cytochrome c with cytochrome oxidase: Two different docking scenarios. Biochim Biophys Acta 1655: 274–281

    Article  PubMed  CAS  Google Scholar 

  • Marcus RA and Sutin N (1985) Electron transport in chemistry and biology. Biochim Biophys Acta 811: 265–322

    Article  CAS  Google Scholar 

  • Margoliash E and Bosshard HR (1983) Guided by electrostatics, a textbook protein comes of age. Trends Biochem Sci 8: 316–320

    Article  CAS  Google Scholar 

  • Mather MW, Springer P, Hensel S, Buse G, and Fee JA (1993) Cytochrome oxidase genes from Thermus thermophilus. Nucleotide sequence of the fused gene and analysis of the deduced primary structures for subunits I and III of cytochrome caa 3. J Biol Chem 268: 5395–5408

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Messinger J and Renger G (2008) Photosynthetic water splitting. In: Renger G (ed) Primary processes of photosynthesis: Basic priniciples and apparatus, Volume II: Reaction centers/photosystems, electron transport chains, photophosphorylation and evolution, Royal Society Chemistry, Cambridge, pp 291–349

    Google Scholar 

  • Messinger J, Wacker U and Renger G (1991) Unusual low reactivity of the water oxidase in redox state S3 toward exogenous reductants. Analysis of the NH2OH and NH2NH2-induced modifications of flash-induced oxygen evolution in isolated spinach thylakoids. Biochemistry 30: 7852–7862

    Article  PubMed  CAS  Google Scholar 

  • Meyer TJ, Hang M, Huynh V and Thorp HH (2007) The role of proton coupled electron transfer (PCET) in water oxidation by photosystem II. Wiring for protons. Angew Chem Int Ed 46: 5284–5304

    Article  CAS  Google Scholar 

  • Michel H (1999) Cytochrome c oxidase: Catalytic cycle and mechanisms of proton pumping—A discussion. Biochemistry 38: 15129–15140

    Article  PubMed  CAS  Google Scholar 

  • Miloslavina Y, Szczepaniak M, Müller MG, Sander J, Nowaczyk M, Rögner M and Holzwarth AR (2006) Charge separation kinetics in intact photosystem II core particles is trap-limited. A picosecond fluorescence study. Biochemistry 45: 2436–2442

    Article  PubMed  CAS  Google Scholar 

  • Miqyass M, Marosvölgyi MA, Nagel Z, Yocum CF and van Gorkom HJ (2008) S-State dependence of the calcium requirement and binding characteristics in the oxygen-evolving complex of photosystem II. Biochemistry 47: 7915–7924

    Article  PubMed  CAS  Google Scholar 

  • Mitchell P (1961) Coupling of photophosphorylation to electron and hydrogen transfer by a chemiosmotic type of mechanism. Nature 191: 144–148

    Article  PubMed  CAS  Google Scholar 

  • Morowitz HJ (1978) Foundations of bioenergetics, Academic Press, New York, p 344

    Google Scholar 

  • Moser CC, Farid TA, Chobot SE and Dutton PL (2006) Electron tunneling chains of mitochondria. Biochim Biophys Acta 1757: 1096–1109

    Article  PubMed  CAS  Google Scholar 

  • Moser CC, Chobot SE, Page CC and Dutton PL (2008) Distance metrics for heme protein electron tunneling. Biochim Biophys Acta 1777: 1032–1037

    Article  PubMed  CAS  Google Scholar 

  • Muramoto K, Hirata K, Shinzawa-Itoh K, Yoko-o S, Yamashita E, Aoyama H, Tsukihara T and Yoshikawa S (2007) A histidine residue acting as a controlling site for dioxygen reduction and proton pumping by cytochrome c oxidase. Proc Natl Acad Sci U S A 104: 7881–7886

    Article  PubMed  CAS  Google Scholar 

  • Muresanu L, Pristovšek P, Löhr F, Maneg O, Mukrasch MD, Rüterjans H, Ludwig B and Lücke C (2006) The electron transfer complex between cytochrome c 552 and the CuA domain of the Thermus thermophilus ba 3 oxidase—a combined NMR and computational approach. J Biol Chem 281: 14503–14513

    Article  PubMed  CAS  Google Scholar 

  • Müh F and Zouni A (2011) Light-induced water oxidation in Photosystem II. Front Biosci (in press)

    Google Scholar 

  • Murray JW and Barber J (2007) Structural characteristics of channels and pathways in photosystem II including the identification of an oxygen channel. J Struct Biol 159: 228–237

    Article  PubMed  CAS  Google Scholar 

  • Namslauer A, Lepp H, Brändén M, Jasaitis A, Verkhovsky MI and Brzezinski P (2007) Plasticity of proton pathway structure and water coordination in cytochrome c oxidase. J Biol Chem 282: 15148–15158

    Article  PubMed  CAS  Google Scholar 

  • Neupert W and Herrmann JM (2007) Translocation of proteins into mitochondria. Annu Rev Biochem 76: 723–749

    Article  PubMed  CAS  Google Scholar 

  • Nicholls DG and Fergusson SJ (1982) Bioenergetics, vol. 2, Academic Press, London, pp 215–218

    Google Scholar 

  • Nicolls G, Prigogine I (1977) Self organization in nonequilibrium systems, Wiley, New York

    Google Scholar 

  • Noguchi T (2008) FTIR detection of water reactions in the oxygen-evolving centre of photosystem II. Phil Trans R Soc B 363: 1189–1195

    Article  PubMed  CAS  Google Scholar 

  • Noguchi T and Sugiura M (2002) Flash-induced FTIR difference spectra of the water oxidizing complex in moderately hydrated Photosystem II core films: Effect of hydration extent on S-state transitions. Biochemistry 41: 2322–2330

    Article  PubMed  CAS  Google Scholar 

  • Olesen K and Andréasson L-E (2003) The function of the chloride ion in photosynthetic oxygen evolution. Biochemistry 42: 2025–2035

    Article  PubMed  CAS  Google Scholar 

  • Olsson MHM, Siegbahn PEM, Blomberg MRA and Warshel A (2007) Exploring pathways and barriers for coupled ET/PT in cytochrome c oxidase: A general framework for examining energetics and mechanistic alternatives. Biochim Biophys Acta 1767: 244–260

    Article  PubMed  CAS  Google Scholar 

  • Orio M, Pantazis DA and Neese F (2009) Density functional theory. Photosynth Res 102(2–3): 443–453

    Article  PubMed  CAS  Google Scholar 

  • Ostermeier C, Harrenga A, Ermler U and Michel H (1997) Structure at 2.7 Å resolution of the Paracoccus denitrificans two-subunit cytochrome c oxidase complexed with an antibody Fv fragment. Proc Natl Acad Sci U S A 94: 10547–10553

    Article  PubMed  CAS  Google Scholar 

  • Otten MF, van der Oost J, Reijnders WNM, Westerhoff HV, Ludwig B and van Spanning RJM (2001) Cytochromes c 550, c 552 and c 1 in the electron transport network of Paracoccus denitrificans: Redundant or subtly different in function? J Bacteriol 183: 7017–7026

    Article  PubMed  CAS  Google Scholar 

  • Page CC, Moser CC, Chen X and Dutton PL (1999) Natural engineering principles of electron tunneling in biological oxidation-reduction. Nature 402: 47–52

    Article  PubMed  CAS  Google Scholar 

  • Parson WW (2008) Functional patterns of reaction centers in anoxygenic photosynthetic bacteria. In: Renger G (ed) Primary processes of photosynthesis: Priniciples and apparatus, Part II reaction centers/photosystems, electron transport chains, photophosphorylation and evolution, Royal Society Chemistry, Cambridge, pp 57–109

    Google Scholar 

  • Paumann M, Regelsberger G, Obinger C and Peschek GA (2005) The bioenergetic role of dioxygen and the terminal oxidase(s) in cyanobacteria. Biochim Biophys Acta 1777: 231–253

    Google Scholar 

  • Pereira MM, Sousa FL, Verissimo AF and Teixiera M (2008) Looking for the minimum common denominator in haem–copper oxygen reductases: Towards a unified catalytic mechanism. Biochim Biophys Acta 1777: 929–934

    Article  PubMed  CAS  Google Scholar 

  • Peschek G (2008) Electron transport chains in oxygenic cyanobacteria. In: Renger G (ed) Primary processes of photosynthesis: Priniciples and apparatus, Part II reaction centers/photosystems, electron transport chains, photophosphorylation and evolution, Royal Society Chemistry, Cambridge, pp 383–415

    Google Scholar 

  • Petrouleas V and Crofts AR (2005) The iron-quinone acceptor complex. In: Wydrzynski T and Satoh K (eds) Photosystem II: The water/plastoquinone oxido-reductase in photosynthesis, Springer, Dordrecht, pp 177–206

    Chapter  Google Scholar 

  • Pfitzner U, Odenwald A, Ostermann T, Weingard L, Ludwig B and Richter O-MH (1998) Cytochrome c oxidase (heme aa 3) from Paracoccus denitrificans: analysis of mutations in putative proton channels of subunit I. J Bioenerg Biomembr 30: 89–97

    Article  PubMed  CAS  Google Scholar 

  • Pfitzner U, Kirichenko AV, Konstantinov AA, Mertens M, Wittershagen A, Kolbesen BO, Steffens GCM, Harrenga A, Michel H and Ludwig B (1999) Mutations in the Ca2+ binding site of the Paracoccus denitrificans cytochrome c oxidase. FEBS Lett 456: 365–369

    Article  PubMed  CAS  Google Scholar 

  • Pfitzner U, Hoffmeier K, Harrenga A, Kannt A, Michel H, Bamberg E, Richter O-MH and Ludwig B (2000) Tracing the D-pathway in reconstituted site-directed mutants of cytochrome c oxidase from Paracoccus denitrificans. Biochemistry 39: 6756–6762

    Article  PubMed  CAS  Google Scholar 

  • Pieper J and Renger G (2009) Protein dynamics investigated by neutron scattering. Photosynth Res 102: 281–293

    Article  PubMed  CAS  Google Scholar 

  • Pilet E, Jasaitis A, Liebl U and Vos MH (2004) Electron transfer between hemes in mammalian cytochrome c oxidase. Proc Natl Acad Sci U S A 101: 16198–16203

    Article  PubMed  CAS  Google Scholar 

  • Pinakoulaki E, Pfitzner U, Ludwig B and Varotsis C (2002) The role of the cross-link his-tyr in the functional properties of the binuclear center in cytochrome c oxidase. J Biol Chem 277: 13563–13568

    Article  PubMed  CAS  Google Scholar 

  • Pisliakov AV et al (2008) Electrostatic basis for the unidirectionality of the primary proton transfer in cytochrome c oxidase. Proc Natl Acad Sci U S A 105: 7726–7731

    Article  PubMed  CAS  Google Scholar 

  • Pogson JB, Rissler HM and Frank HA (2005) The role of carotenoids in energy quenching. In: Wydrzynski T and Satoh K (eds) Photosystem II: The water/plastoquinone oxido-reductase in photosynthesis, Springer, Dordrecht, pp 515–537

    Chapter  Google Scholar 

  • Proshlyakov DE, Pressler MA and Babcock GT (1998) Dioxygen activation and bond cleavage by mixed-valence cytochrome c oxidase. Proc Natl Acad Sci U S A 95: 8020–8025

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Rappaport F and Diner BA (2008) Primary photochemistry and energetics leading to the oxidation of the (Mn)4Ca cluster and to the evolution of molecular oxygen in Photosystem II. Coord Chem Rev 252: 259–272

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Rappaport F, Cuni A, Xiong L, Sayre R and Lavergne J (2005) Charge recombination and thermoluminescence in photosystem II. Biophys J 88: 1948–1958

    Article  PubMed  CAS  Google Scholar 

  • Raszewski G, Diner BA, Schlodder E and Renger T (2008) Spectroscopic properties of reaction center pigments in photosystem II core complexes: Revision of the multimer model. Biophys J 95(1): 105–119, doi: 10.1529/biophysj.107.123935

    Article  PubMed  CAS  Google Scholar 

  • Raymond J and Blankenship RE (2004) The evolutionary development of the protein complement of Photosystem II. Biochim Biophys Acta 1655: 133–139

    Article  PubMed  CAS  Google Scholar 

  • Razeghifard MR and Pace RJ (1999) EPR kinetic studies of oxygen release in thylakoids in PS II membranes: A kinetic intermediate in the S3 to S0 transition. Biochemistry 38: 1252–1257

    Article  PubMed  CAS  Google Scholar 

  • Reincke B, Thöny-Meyer L, Dannehl C, Odenwald A, Aidim M, Witt H, Rüterjans H and Ludwig B (1999) Heterologous expression of soluble fragments of cytochrome c 552 acting as electron donor to the Paracoccus denitrificans cytochrome c oxidase. Biochim Biophys Acta 1411: 114–120

    Article  PubMed  CAS  Google Scholar 

  • Reincke B, Pérez C, Pristovsek P, Lücke C, Ludwig C, Löhr F, Rogov VV, Ludwig B and Rüterjans H (2001) Solution structure and dynamics of the functional domain of Paracoccus denitrificans c 552 in both redox states. Biochemistry 40: 12312–12320

    Article  PubMed  CAS  Google Scholar 

  • Renger G (1978) Theoretical studies about the functional and structural organization of the photosynthetic oxygen evolution. In: Metzner H (ed) Photosynthetic oxygen evolution, Academic Press, London, pp 229–248

    Google Scholar 

  • Renger G (1983) Biological energy conservation. In: Hoppe W, Lohmann W, Markl H and Ziegler H (eds), Biophysics, Springer, Berlin, pp 347–371

    Google Scholar 

  • Renger G (1999) Molecular mechanism of water oxidation. In: Singhal GS, Renger G, Govindjee, Irrgang KD and Sopory SK (eds) Concepts in photobiology: Photosynthesis and photomorphogenesis, Kluwer Academic Publishers (now Springer), Dordrecht and Narosa Publishing Co., Delhi, pp 292–329

    Google Scholar 

  • Renger G (2001) Photosynthetic water oxidation to molecular oxygen: Apparatus and mechanism. Biochim Biophys Acta 1503: 210–228

    Article  PubMed  CAS  Google Scholar 

  • Renger G (2004) Coupling of electron and proton transfer in oxidative water cleavage in photosynthesis. Biochim Biophys Acta 1655: 195–204

    Article  PubMed  CAS  Google Scholar 

  • Renger G (2007) Oxidative photosynthetic water splitting: Energetics, kinetics and mechanism. Photosynth Res 92: 407–425

    Article  PubMed  CAS  Google Scholar 

  • Renger G (2008) Functional pattern of Photosystem II in Oxygen Evolving Organisms. In: Renger G (ed) Primary processes of photosynthesis: principles and apparatus, Part II reaction centers/photosystems, electron transport chains, photophosphorylation and evolution. Royal Society Chemistry, Cambridge, pp 237–290

    Google Scholar 

  • Renger G (2011) Light induced oxidative water splitting in photosynthesis: energetics, kinetics and mechanism. Photobiochem Photobiophys B: Biol, doi: 10.1016/j.jphotobiol.2011.01.023

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Renger G and Holzwarth AR (2005) Primary electron transfer In: Wydrzynski T and Satoh K (eds) Photosystem II: The water: Plastoquinone oxido-reductase in photosynthesis, Springer, Dordrecht, pp 139–175

    Google Scholar 

  • Renger G and Kühn P (2007) Reaction pattern and mechanism of light induced oxidative water splitting in photosynthesis. Biochim Biophys Acta 1767: 458–471

    Article  PubMed  CAS  Google Scholar 

  • Renger G and Renger T (2008) Photosystem II: The machinery of photosynthetic water splitting. Photosynth Res 98: 53–80

    Article  PubMed  CAS  Google Scholar 

  • Renger G and Völker M (1982) Studies on the proton release 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

    Article  CAS  Google Scholar 

  • Renger G and Weiss W (1982) The detection of intrinsic 320 nm absorption changes reflecting the turnover of the water splitting enzyme system Y which leads to oxygen formation in trypsinized chloroplats. FEBS Lett 137: 217–221

    Article  CAS  Google Scholar 

  • Renger G, Eckert HJ and Völker M (1989) Studies on the electron transfer from Tyr-161 of polypeptide D-1 to P680+ in PS II membrane fragments from spinach. Photosynth Res 22: 247–256

    Article  CAS  Google Scholar 

  • Renger G, Eckert H-J, Bergmann A, Bernarding J, Liu B, Napiwotzki A, Reifarth F, and Eichler JH (1995) Fluorescence and spectroscopic studies on exciton trapping and electron transfer in Photosystem II of higher plants. Austr J Plant Physiol 22: 167–181

    Article  CAS  Google Scholar 

  • Renger G, Christen G, Karge M, Eckert H-J and Irrgang K-D (1998) Application of the Marcus theory for analysis of the temperature dependence of the reactions leading to photosynthetic water oxidation—results and implications. J Bioinorg Chem 3: 360–366

    CAS  Google Scholar 

  • Rich PR (1995) Towards an understanding of the chemistry of oxygen reduction and proton translocation in the iron-copper respiratory oxidases. Aust J Plant Physiol 22: 479–486

    Article  CAS  Google Scholar 

  • Riistama S, Puustinen A, García-Horsman A, Iwata S, Michel H and Wikström M (1996) Channelling of dioxygen into the respiratory enzyme. Biochim Biophys Acta 1275: 1–4

    Article  PubMed  Google Scholar 

  • Riistama S, Puustinen A, Verkhovsky MI, Morgan JE and Wikström M (2000) Binding of O2 and its reduction are both retarded by replacement of valine 279 by isoleucine in cytochrome c oxidase from Paracoccus denitrificans. Biochemistry 39: 6365–6372

    Article  PubMed  CAS  Google Scholar 

  • Robblee JH, Messinger J, Cinco RM, McFarlane KL, Fernandez C, Pizarro SA, Sauer K and Yachandra VK (2002) The Mn cluster in the S0 state of the oxygen evolving complex of Photosystem II studied by EXAFS spectroscopy: are there three di-µ-oxo-bridged Mn2 moieties in the tetranuclear Mn complex? J Am Chem Soc 124: 7459–7471

    Article  PubMed  CAS  Google Scholar 

  • Roberts VA and Pique ME (1999) Definition of the interaction domain for cytochrome c on cytochrome c oxidase—III. Prediction of the docked complex by a complete, systematic search. J Biol Chem 274: 38051–38060

    Article  PubMed  CAS  Google Scholar 

  • Romain S, Bozoglian F, Sala X and Llobet A (2009) Oxygen−oxygen bond formation by the Ru-Hbpp water oxidation catalyst occurs solely via an intramolecular reaction pathway. J Am Chem Soc 131: 2768–2769

    Article  PubMed  CAS  Google Scholar 

  • Romero E, van Stokkum IHM, Novoderezhkin VI, Dekker JP and van Grondelle R (2010) Two different charge separation pathways in Photosystem II. Biochemistry 49: 4300–4307

    Article  CAS  Google Scholar 

  • Ruitenberg M, Kannt A, Bamberg E, Michel H, Ludwig B and Fendler K (2000) Single-electron reduction of the oxidized state is coupled to proton uptake via the K-pathway in Paracoccus denitrificans cytochrome c oxidase. Proc Natl Acad Sci U S A 97: 4632–4636

    Article  PubMed  CAS  Google Scholar 

  • Ruitenberg M, Kannt A, Bamberg E, Fendler K and Michel H (2002) Reduction of cytochrome c oxidase by a second electron leads to proton translocation. Nature 417: 99–102

    PubMed  CAS  Google Scholar 

  • Sacconi S, Salviati L, Sue CM, Shanske S, Davidson MM, Bonilla E, Naini AB, De Vivo DC and DiMauro S (2003) Mutation screening in patients with isolated cytochrome c oxidase deficiency. Pediatr Res 53: 224–230

    Article  PubMed  CAS  Google Scholar 

  • Salje J, Ludwig B and Richter O-MH (2005) Is a third proton-conducting pathway operative in bacterial cytochrome c oxidases? Biochem Soc Trans 33: 829–831

    Article  PubMed  CAS  Google Scholar 

  • Saraste M and Castresana J (1994) Cytochrome oxidase evolved by tinkering with denitrification enzymes. FEBS Lett 341: 1–4

    Article  PubMed  CAS  Google Scholar 

  • Sauer K, Yano J and Yachandra VK (2008) X-ray spectroscopy of the photosynthetic oxygen-evolving complex. Coord Chem Rev 252: 318–335

    Article  PubMed  CAS  Google Scholar 

  • Schägger H and Pfeiffer K (2001) The ratio of oxidative phosphorylation complexes I–V in bovine heart mitochondria and the composition of respiratory chain supercomplexes. J Biol Chem 276: 37861–37867

    PubMed  Google Scholar 

  • Schinzel S, Schraut J, Arbuznikov AV, Siegbahn PEM and Kaipp M (2010) Density functional calculations of 55Mn, 14N and 13C electron paramagnetic resonance parameters support an energetically feasible model system for the S2 state of the oxygen-evolving complex of Photosystem II. Chem Eur J 16:10424–10438

    Article  PubMed  CAS  Google Scholar 

  • Schlodder E, Renger T, Raszewski G, Coleman WJ, Nixon PJ, Cohen RO and Diner B (2008) Site-directed mutations at D1-Thr179 of Photosystem II in Synechocystis sp. PCC 6803 modify the spectroscopic properties of the accessory chlorophyll in the D1-branch of the reaction center. Biochemistry 47: 3143–3154

    Article  PubMed  CAS  Google Scholar 

  • Seelig A, Ludwig B, Seelig J and Schatz G (1981) Copper and Manganese Electron Spin Resonance Studies of Cytochrome c Oxidase from Paracoccus denitrificans. Biochim Biophys Acta 636: 162–167

    Article  PubMed  CAS  Google Scholar 

  • Sharpe MA and Ferguson-Miller S (2008) A chemically explicit model for the mechanism of proton pumping in heme–copper oxidases. J Bioenerg Biomembr 40: 541–549

    Article  PubMed  CAS  Google Scholar 

  • Sharpe MA, Krzyaniak MD, Xu S, McCracken J and Ferguson-Miller S (2009) EPR Evidence of Cyanide Binding to the Mn(Mg) Center of Cytochrome c Oxidase: Support for CuA -Mg Involvement in Proton Pumping. Biochemistry 48: 328–335

    Article  PubMed  CAS  Google Scholar 

  • Shelaev IV, Gostev FE, Nadtochenko VA, Shkuropatov AY, Zabelin AA, Mamedov MD, Semenov AY, Sarkisov OM and Shuvalov VA (2008) Primary light-energy conversion in tetrameric chlorophyll structure of Photosystem II and bacterial reaction centers: II. Femto- and picosecond charge separation in PS II D1/D2/Cyt b559 complex. Photosynth Res 98: 95–103

    Article  PubMed  CAS  Google Scholar 

  • Sheleva D, Su J-H, Klimov V and Messinger J (2008) Hydrogencarbonate is not a tightly bound constituent of the water oxidizing complex in Photosystem II. Biochim Biophys Acta 1777: 532–539

    Article  CAS  Google Scholar 

  • Sheleva D, Beckmann K, Clausen J, Junge W and Messinger J (2011) Photosynthetic oxygen-evolution at elevated oxygen pressure: direct detection by membrane inlet mass spectrometry. Proc Natl Acad Sci 108: 3602–3607

    Google Scholar 

  • Shi L-X and Schröder WP (2004) The low molecular mass subunits of the photosynthetic supracomplex, Photosystem II. Biochim Biophys Acta 1608: 75–96

    Article  PubMed  CAS  Google Scholar 

  • Shibamoto T, Kato Y, Sugiura M and Watanabe T (2009) Redox potential of the primary plastoquinone electron acceptor QA in Photosystem II from Thermosynechococcus elongatus determined by spectroelectrochemistry. Biochemistry 48: 10682–10684

    Article  PubMed  CAS  Google Scholar 

  • Shimokata K, Katayama Y, Murayama H, Suematsu M, Tsukihara T, Muramoto K, Aoyama H, Yoshikawa S and Shimada H (2007) The proton pumping pathway of bovine heart cytochrome c oxidase. Proc Natl Acad Sci U S A 104: 4200–4205

    Article  PubMed  CAS  Google Scholar 

  • Shutova T, Irrgang K-D, Shubin V, Klimov VV and Renger G (1997) Analysis of pH-induced structural changes of the isolated extrinsic 33 kDa protein of Photosystem II. Biochemistry 36: 6350–6358

    Article  PubMed  CAS  Google Scholar 

  • Shutova T, Klimov VV, Andersson B and Samuelsson G (2007) A cluster of carboxylic groups in PsbO protein is involved in proton transfer from the water oxidizing complex of Photosystem II. Biochim Biohys Acta 1767: 434–440

    Article  CAS  Google Scholar 

  • Siegbahn PEM (2008) Theoretical studies of O–O bond formation in Photosystem II. Inorg Chem 47: 1779–1786

    Article  PubMed  CAS  Google Scholar 

  • Siegbahn PEM (2009) Structures and energetics for O2 formation in Photosystem II. Acc Chem Res 42: 1871–1880

    Article  PubMed  CAS  Google Scholar 

  • Siegbahn PEM and Blomberg MRA (2008) Proton pumping mechanism in cytochrome c oxidase. J Phys Chem A 112: 12772–12780

    Article  PubMed  CAS  Google Scholar 

  • Sjödin M, Styring S, Åkermark B, Sun L and Hammarström L (2002) The mechanism for proton coupled electron transfer from tyrosine in a model complex and comparison with tyrosine Z oxidation in Photosystem II. Phil Trans B 357: 1471–1478

    Article  CAS  Google Scholar 

  • Smirnova IA, Zaslavsky D, Fee JA, Gennis RB and Brzezinski (2008) Electron and proton transfer in the ba 3 oxidase from Thermus thermophilus. J Bioenerg Biomembr 40: 281–287

    Google Scholar 

  • Smith D, Gray J, Mitchell L, Antholine WE and Hosler JP (2005) Assembly of cytochrome-c oxidase in the absence of assembly protein Surf1p leads to loss of the active site heme, J Biol Chem 280: 17652–17656

    Article  PubMed  CAS  Google Scholar 

  • Soulimane T, Buse G, Bourenkov GP, Bartunik HD, Huber R, and Than ME (2000) Structure and mechanism of the aberrant ba(3)-cytochrome c oxidase from Thermus thermophilus. EMBO J 19: 1766–1776

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Steinrücke P, Steffens GCM, Panskus G, Buse G and Ludwig B (1987) Subunit II of cytochrome c oxidase from Paracoccus denitrificans: DNA sequence, gene expression, and the protein. Eur J Biochem 167: 431–439

    Article  PubMed  Google Scholar 

  • Stroh A, Anderka O, Pfeiffer K, Yagi T, Finel M, Ludwig B and Schägger H (2004) Assembly of respiratory complexes I, III, and IV into NADH oxidase supercomplex stabilizes complex I in Paracoccus denitrificans. J Biol Chem 279: 5000–5007

    Article  PubMed  CAS  Google Scholar 

  • Strzalka K, Walczak T, Sarna T and Swartz HM (1990) Measurement of time-resolved oxygen concentration changes in photosynthetic systems by nitroxide-based EPR oximetry. Arch Biochem Biophys 281: 312–318

    Article  PubMed  CAS  Google Scholar 

  • Sugiura M, Rappaport F, Hillier W, Dorlet P, Ohno Y, Hayashi H and Boussac A (2009) Evidence that D1-His332 in Photosystem II from Thermosynechococcus elongatus interacts with the S3-State and not with the S2-State. Biochemistry 48: 7856–7866

    Article  PubMed  CAS  Google Scholar 

  • Suzuki H, Nagasaka M, Sugiura M and Noguchi T (2005) Fourier transform infrared spectrum of the secondary quinone electron Acceptor QB in Photosystem II. Biochemistry 44: 11323–11328

    Article  PubMed  CAS  Google Scholar 

  • Than ME, Hof P, Huber R, Bourenkov GP, Bartunik HD, Buse G and Soulimane T (1997) Thermus thermophilus Cytochrome-c552: A new highly thermostable Cytochrome-c structure obtained by MAD Phasing. J Mol Biol 271: 629–644

    Article  PubMed  CAS  Google Scholar 

  • Thomas JW, Lemieux LJ, Alben JO and Gennis RB (1993) Site-directed mutagenesis of highly conserved residues in helix VIII of subunit I of the cytochrome bo ubiquinol oxidase from Escherichia coli: an amphipathic transmembrane helix that may be important in conveying protons to the binuclear center. Biochemistry 32: 11173–11180

    Article  PubMed  CAS  Google Scholar 

  • Tiede DM, Vashishta AC and Gunner MR (1993) Electron-transfer kinetics and electrostatic properties of the Rhodobacter sphaeroides reaction center and soluble c-cytochromes. Biochemistry 32: 4515–4531

    Article  PubMed  CAS  Google Scholar 

  • Tommos C and Babcock GT (2000) Proton and hydrogen currents in photosynthetic water oxidation. Biochim Biophys Acta 1458: 199–299

    Article  PubMed  CAS  Google Scholar 

  • Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R and Yoshikawa S (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 272: 1136–1144

    Article  PubMed  CAS  Google Scholar 

  • Turba A, Jetzek M and Ludwig B (1995) Purification of the cytochrome c 552 of Paracoccus denitrificans and sequence analysis of the gene. Eur J Biochem 231: 259–265

    PubMed  CAS  Google Scholar 

  • Tuukkanen A, Kaila VRI, Laakkonen L, Hummer G and Wikström M (2007) Dynamics of the glutamic acid 242 side chain in cytochrome c oxidase. Biochim Biophys Acta 1767: 1102–1110

    Article  PubMed  CAS  Google Scholar 

  • Tuukkanen A, Verkhovsky MI, Laakkonen L and Wikström M (2006) The K-pathway revisited: A computational study on cytochrome c oxidase. Biochim Biophys Acta 1757: 1117–1121

    Article  PubMed  CAS  Google Scholar 

  • Ulas G, Olack G, Brudvig GW (2008) Evidence against bicarbonate bound in the O2-evolving complex of Photosystem II. Biochemistry 47: 3073–3075

    Article  PubMed  CAS  Google Scholar 

  • Vakkasoglu AS, Morgan JE, Han D, Pawatea AS and Gennis RB (2006) Mutations which decouple the proton pump of the cytochrome c oxidase from Rhodobacter sphaeroides perturb the environment of glutamate 286. FEBS Lett 580: 4613–4617

    Article  PubMed  CAS  Google Scholar 

  • Van Eps N, Szundi I and Einarsdottir Ó (2000) A new approach for studying fast biological reactions involving dioxygen: The reaction of fully reduced cytochrome c oxidase with O2. Biochemistry 39: 14576–14582

    Article  PubMed  CAS  Google Scholar 

  • van Leeuwen PJ, Heimann C, Gast P, Dekker JP and Gorkom HJ (1993) Flash-induced redox changes in oxygen-evolving spinach Photosystem II core particles. Photosynth Res 38: 169–176

    Article  CAS  Google Scholar 

  • van Niel CB (1941) The bacterial photosynthesis and their importance of the general problem of photosynthesis. Act Enzymol 1: 263–328

    CAS  Google Scholar 

  • Vass I and Aro EM (2008) Photoinhibition of photosynthetic electron transport. In: Renger G (ed) Primary processes of photosynthesis: Basic priniciples and apparatus, Part I photophysical principles, pigments and light harvesting/adaptation/stress, Royal Society Chemistry, Cambridge, pp 393–425

    Google Scholar 

  • Velthuys B (1981) Spectroscopis studies of the S-state transitions of Photosystem II and of the interacxtion of its charged donorchains with lipid-soluble anions. In: Akoyunoglou G (ed) Photosynthesis II. Electron transport and photophosphorylation. Balaban, Philadelphia, pp 75–85

    Google Scholar 

  • Vermeglio A (2008) Electron transport chain and phosphorylation. In: Renger G (ed) Primary processes of photosynthesis: Priniciples and apparatus, Part II reaction centers/photosystems, electron transport chains, photophosphorylation and evolution, Royal Society Chemistry, Cambridge, pp 353–382

    Google Scholar 

  • Vogt S, Riehl A, Koch V and Kadenbach B (2007) Regulation of oxidative phosphorylation by inhibition of its enzyme complexes via reversible phosphorylation. Curr Enzyme Inhib 3: 189–206

    Article  CAS  Google Scholar 

  • Vonck J and Schäfer E (2009) Supramolecular organization of protein complexes in the mitochondrial innermembrane. Biochim Biophys Acta 1793: 117–124

    Article  PubMed  CAS  Google Scholar 

  • Wagner BK, Kitami T, Gilbert TJ, Peck D, Ramanathan A, Schreiber SL, Golub TR and Mootha VK (2008) Large-scale chemical dissection of mitochondrial function. Nat Biotech 26: 343–351

    Article  CAS  Google Scholar 

  • Wickner W and Schekman R (2005) Protein translocation across biological membranes. Science 310: 1452–1456

    Article  PubMed  CAS  Google Scholar 

  • Wienk H, Maneg O, Lücke C, Pristovsek P, Löhr F, Ludwig B and Rüterjans H (2003) Interaction of cytochrome c with cytochrome c oxidase: An NMR study on two soluble fragments derived from Paracoccus denitrificans. Biochemistry 42: 6005–6012

    Article  PubMed  CAS  Google Scholar 

  • Wiertz FGM, Richter O-MH, Cherepanov AV, MacMillan F, Ludwig B and de Vries S (2004) An oxo-ferryl tryptophan radical catalytic intermediate in cytochrome c and quinol oxidases trapped by microsecond freeze-hyperquenching (MHQ). FEBS Lett 575: 127–130

    Article  PubMed  CAS  Google Scholar 

  • Wiertz FGM, Richter O-MH, Ludwig B and de Vries S (2007) Kinetic resolution of a tryptophan-radical intermediate in the reaction of Paracoccus denitrificans cytochrome c oxidase. J Biol Chem 282: 31580–31591

    Article  PubMed  CAS  Google Scholar 

  • Wikström M (2004) Cytochrome c oxidase: 25 years of the elusive proton pump. Biochim Biophys Acta 1655: 241–247

    Article  PubMed  CAS  Google Scholar 

  • Wikström M and Verkhovsky MI (2007) Mechanism and energetics of proton translocation by the respiratory heme-copper oxidases. Biochim Biophys Acta 1767: 1200–1214

    Article  PubMed  CAS  Google Scholar 

  • Wikström M, Verkhovsky MI and Hummer G (2003) Water-gated mechanism of proton translocation by cytochrome c oxidase. Biochim Biophys Acta 1604: 61–65

    Article  PubMed  CAS  Google Scholar 

  • Williams PA, Fülöp V, Leung YC, Chan C, Moir JW, Howlett G, Ferguson SJ, Radford SE and Hajdu J (2005) Pseudospecific docking surfaces on electron transfer proteins as illustrated by pseudoazurin, cytochrome c 550 and cytochrome cd 1 nitrite reductase. Nat Struct Biol 2: 975–982

    Article  Google Scholar 

  • Witt H, Zickermann V and Ludwig B (1995) Site-directed mutagenesis of cytochrome c oxidase reveals two acidic residues involved in the binding of cytochrome c. Biochim Biophys Acta 1230: 74–76

    Article  PubMed  Google Scholar 

  • Witt H, Wittershagen A, Bill A, Kolbesen BA and Ludwig B (1997) Asp-193 and Glu-218 of subunit II are involved in the Mn2+-binding of Paracoccus denitrificans cytochrome c oxidase. FEBS Lett 409: 128–130

    Article  PubMed  CAS  Google Scholar 

  • Witt H and Ludwig B (1997) Isolation, analysis, and deletion of the gene coding for subunit IV of cytochrome c oxidase in Paracoccus denitrificans. J Biol Chem 272: 5514–5517

    Article  PubMed  CAS  Google Scholar 

  • Witt H, Malatesta F, Nicoletti F, Brunori M and Ludwig B (1998a) Cytochrome c binding site on cytochrome oxidase in Paracoccus denitrificans. Eur J Biochem 251: 367–373

    Article  CAS  Google Scholar 

  • Witt H, Malatesta F, Nicoletti F, Brunori M and Ludwig B (1998b) Tryptophan 121 of subunit II is the electron entry site to cytochrome c oxidase in Paracoccus denitrificans—involvement of a hydrophobic patch in the docking reaction. J Biol Chem 273: 5132–5136

    Article  CAS  Google Scholar 

  • Worrest RC and Caldwell MM (eds) (1986) Stratospheric ozone reduction, solar ultraviolet radiation and plant life, Springer, Berlin, pp 171–184

    Book  Google Scholar 

  • Xiong J and Bauer CE (2002) Complex evolution of photosynthesis. Annu Rev Plant Biol 53: 503–521

    Article  PubMed  CAS  Google Scholar 

  • Yachandra VK (2005) The catalytic manganese cluster: organisation of the metal ions. In: Wydrzynski T and Satoh K (eds) Photosystem II. The Light-Driven Water:Plastoquinone Oxidoreductase, Springer, Dordrecht, pp 235–260

    Chapter  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yoshikawa S and Shinzawa-Itoh K (1998) Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280: 1723–1729

    Article  PubMed  CAS  Google Scholar 

  • Zamaraev KI and Parmon VN (1980) Potential methods and perspectives of solar energy conversion via photocatalytic processes. Rev Sci Eng 22: 261–324

    Article  CAS  Google Scholar 

  • Zein S, Kulik LV, Yano J, Kern J, Pushkar Y, Zouni A, Yachandra VK, Lubitz W, Neese F and Messinger J (2008) Focusing the view on nature’s water-splitting catalyst. Phil Trans R Soc B 363: 1167–1177

    Article  PubMed  CAS  Google Scholar 

  • Zhang C (2007) Low-barrier hydrogen bond plays key role in active Photosystem II — A new model for photosynthetic water oxidation. Biochim Biophys Acta 1767: 493–499

    Article  PubMed  CAS  Google Scholar 

  • Zouni A (2008) From cell growth to the 3.0 Å resolution crystal structure of cyanobacterial Photosystem II. In: Renger G (ed) Primary processes of photosynthesis: Priniciples and apparatus, Part II reaction centers/photosystems, electron transport chains, photophosphorylation and evolution, Royal Society Chemistry, Cambridge, pp 193–236

    Google Scholar 

  • Zouni A, Witt HT, Kern J, Fromme P, Krauß N, Saenger W and Orth P (2001) Crystal structure of Photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409: 739–743

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

G.R. would like to thank Susanne Renger for preparing the electronic version of Fig. 13.1, J. Kern for Figs. 13.2 and  13.5a, b and P. Kühn for Fig. 13.7, Fig. 13.5c was kindly provided by V. Yachandra. The financial support by Deutsche Forschungsgemeinschaft (SFB 429 TPA1) is gratefully acknowledged. B.L. thanks O. Richter for providing Fig. 13.10; work from his lab was supported by long-term funding by Deutsche Forschungsgemeinschaft (SFB 472 P8, and Cluster of Excellence “Macromolecular Complexes”, Project EXC 115).

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  1. Max-Volmer-Laboratorium für Biophysikalische Chemie, Technische Universität Berlin, Berlin, Germany

    Gernot Renger

  2. Institute Biochemistry, Biocenter of Goethe University Inst, Max-von-Laue-Str. 9, 60438, Frankfurt, Germany

    Bernd Ludwig

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  1. Inst. Physikalische Chemie, Molecular Bioenergetics Group, Univ. Wien, Währingerstr. 42, Wien, 1090, Austria

    Guenter A. Peschek

  2. Department für Chemie, Abteilung für Biochemie, Universität für Bodenkultur Wien, Althanstrasse 14, Wien, 1190, Austria

    Christian Obinger

  3. Fak. II Mathematik/Naturwissenschaften, Institut für Chemie, TU Berlin, Straße des 17. Juni 135, Berlin, 10587, Berlin, Germany

    Gernot Renger

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Renger, G., Ludwig, B. (2011). Mechanism of Photosynthetic Production and Respiratory Reduction of Molecular Dioxygen: A Biophysical and Biochemical Comparison. In: Peschek, G., Obinger, C., Renger, G. (eds) Bioenergetic Processes of Cyanobacteria. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0388-9_13

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