The nonheme iron in photosystem II

Abstract

Photosystem II (PSII), the light-driven water:plastoquinone (PQ) oxidoreductase of oxygenic photosynthesis, contains a nonheme iron (NHI) at its electron acceptor side. The NHI is situated between the two PQs QA and QB that serve as one-electron transmitter and substrate of the reductase part of PSII, respectively. Among the ligands of the NHI is a (bi)carbonate originating from CO2, the substrate of the dark reactions of oxygenic photosynthesis. Based on recent advances in the crystallography of PSII, we review the structure of the NHI in PSII and discuss ideas concerning its function and the role of bicarbonate along with a comparison to the reaction center of purple bacteria and other enzymes containing a mononuclear NHI site.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Andersson I, Backlund A (2008) Structure and function of Rubisco. Plant Physiol Biochem 46:275–291

    PubMed  CAS  Google Scholar 

  2. Astashkin AV, Kawamori A, Kodera Y, Kuroiwa S, Akabori K (1995) An electron-spin echo envelope modulation study of the primary acceptor quinone in Zn-substituted plant photosystem II. J Chem Phys 102:5583–5588

    CAS  Google Scholar 

  3. Astashkin AV, Hara H, Kuroiwa S, Kawamori A, Akabori K (1998) A comparative electron spin echo envelope modulation study of the primary electron acceptor quinone in Zn-substituted and cyanide-treated preparations of photosystem II. J Chem Phys 108:10143–10151

    CAS  Google Scholar 

  4. Baciou L, Sebban P (1995) Heterogeneity of the quinone electron-acceptor system in bacterial reaction centers. Photochem Photobiol 62:271–278

    CAS  Google Scholar 

  5. Baker EN, Baker HM (2005) Molecular structure, binding properties and dynamics of lactoferrin. Cell Mol Life Sci 62:2531–2539

    PubMed  CAS  Google Scholar 

  6. Bauwe H, Hagemann M, Fernie AR (2010) Photorespiration: players, partners and origin. Trends Plant Sci 15:330–336

    PubMed  CAS  Google Scholar 

  7. Bauwe H, Hagemann M, Kern R, Timm S (2012) Photorespiration has a dual origin and manifold links to central metabolism. Curr Opin Plant Biol 15:269–275

    PubMed  CAS  Google Scholar 

  8. Beijer C, Rutherford AW (1987) The iron–quinone acceptor complex in Rhodospirillum rubrum chromatophores studied by EPR. Biochim Biophys Acta 890:169–178

    CAS  Google Scholar 

  9. Beligni MV, Lamattina L (2001) Nitric oxide in plants: the history is just beginning. Plant, Cell Environ 24:267–278

    CAS  Google Scholar 

  10. Bernarding J, Eckert HJ, Eichler HJ, Napiwotzki A, Renger G (1994) Kinetic studies on the stabilization of the primary radical pair P680+ Pheo in different photosystem II preparations from higher plants. Photochem Photobiol 59:566–573

    CAS  Google Scholar 

  11. Biesiadka J, Loll B, Kern J, Irrgang KD, Zouni A (2004) Crystal structure of cyanobacterial photosystem II at 3.2 Å resolution: a closer look at the Mn-cluster. Phys Chem Chem Phys 6:4733–4736

    CAS  Google Scholar 

  12. Bondar AN, Dau H (2012) Extended protein/water H-bond networks in photosynthetic water oxidation. Biochim Biophys Acta 1817:1177–1190

    PubMed  CAS  Google Scholar 

  13. Bonnot F, Molle T, Menage S, Moreau Y, Duval S, Favaudon V, Houee-Levin C, Niviere V (2012) Control of the evolution of iron peroxide intermediate in superoxide reductase from Desulfoarculus baarsii. Involvement of lysine 48 in protonation. J Am Chem Soc 134:5120–5130

    PubMed  CAS  Google Scholar 

  14. Boussac A, Sugiura M, Rappaport F (2011) Probing the quinone binding site of photosystem II from Thermosynechococcus elongatus containing either PsbA1 or PsbA3 as the D1 protein through the binding characteristics of herbicides. Biochim Biophys Acta 1807:119–129

    PubMed  CAS  Google Scholar 

  15. Bowes JM, Crofts AR, Itoh S (1979) A high potential acceptor for photosystem II. Biochim Biophys Acta 547:320–335

    PubMed  CAS  Google Scholar 

  16. Bricker TM, Roose JL, Fagerlund RD, Frankel LK, Eaton-Rye JJ (2012) The extrinsic proteins of Photosystem II. Biochim Biophys Acta 1817:121–142

    PubMed  CAS  Google Scholar 

  17. Broser M, Gabdulkhakov A, Kern J, Guskov A, Müh F, Saenger W, Zouni A (2010) Crystal structure of monomeric photosystem II from Thermosynechococcus elongatus at 3.6 Å resolution. J Biol Chem 285:26255–26262

    PubMed  CAS  Google Scholar 

  18. Broser M, Glöckner C, Gabdulkhakov A, Guskov A, Buchta J, Kern J, Müh F, Dau H, Saenger W, Zouni A (2011) Structural basis of cyanobacterial photosystem II inhibition by the herbicide terbutryn. J Biol Chem 286:15964–15972

    PubMed  CAS  Google Scholar 

  19. Cardona T, Sedoud A, Cox N, Rutherford AW (2012) Charge separation in photosystem II: a comparative and evolutionary overview. Biochim Biophys Acta 1817:26–43

    PubMed  CAS  Google Scholar 

  20. Cheap H, Tandori J, Derrien V, Benoit M, de Oliveira P, Koepke J, Lavergne J, Maróti P, Sebban P (2007) Evidence for delocalized anticooperative flash induced proton binding as revealed by mutants at the M266His iron ligand in bacterial reaction centers. Biochemistry 46:4510–4521

    PubMed  CAS  Google Scholar 

  21. Chernev P, Zaharieva I, Dau H, Haumann M (2011) Carboxylate shifts steer interquinone electron transfer in photosynthesis. J Biol Chem 286:5368–5374

    PubMed  CAS  Google Scholar 

  22. Costas M, Mehn MP, Jensen MP, Que L (2004) Dioxygen activation at mononuclear nonheme iron active sites: enzymes, models, and intermediates. Chem Rev 104:939–986

    PubMed  CAS  Google Scholar 

  23. Cox N, Jin L, Jaszewski A, Smith PJ, Krausz E, Rutherford AW, Pace R (2009) The semiquinone-iron complex of photosystem II: structural insights from ESR and theoretical simulation; evidence that the native ligand to the non-heme iron is carbonate. Biophys J 97:2024–2033

    PubMed  CAS  Google Scholar 

  24. Dasgupta J, Ananyev GM, Dismukes GC (2008) Photoassembly of the water-oxidizing complex in photosystem II. Coord Chem Rev 252:347–360

    PubMed  CAS  Google Scholar 

  25. Day CL, Anderson BF, Tweedie JW, Baker EN (1993) Structure of the recombinant N-terminal lobe of human lactoferrin at 2.0-Å resolution. J Mol Biol 232:1084–1100

    PubMed  CAS  Google Scholar 

  26. Debus RJ, Feher G, Okamura MY (1985) LM complex of reaction centers from Rhodopseudomonas sphaeroides R-26: characterization and reconstitution with the H subunit. Biochemistry 24:2488–2500

    CAS  Google Scholar 

  27. Debus RJ, Feher G, Okamura MY (1986) Iron-depleted reaction centers from Rhodopseudomonas sphaeroides R-26.1—Characterization and reconstitution with Fe2+, Mn2+, Co2+, Ni2+, Cu2+, and Zn2+. Biochemistry 25:2276–2287

    PubMed  CAS  Google Scholar 

  28. Deisenhofer J, Michel H (1989) The photosynthetic reaction center from the purple bacterium Rhodopseudomonas viridis. Science 245:1463–1473

    PubMed  CAS  Google Scholar 

  29. Deligiannakis Y, Jegerschöld C, Rutherford AW (1997) EPR and ESEEM study of the plastoquinone anion radical Q −•A in photosystem II treated at high pH. Chem Phys Lett 270:564–572

    CAS  Google Scholar 

  30. Diaz A, Loewen PC, Fita I, Carpena X (2012) Thirty years of heme catalases structural biology. Arch Biochem Biophys 525:102–110

    PubMed  CAS  Google Scholar 

  31. Diner BA, Petrouleas V (1990) Formation by NO of nitrosyl adducts of redox components of the photosystem II reaction center. II. Evidence that HCO3 /CO2 binds to the acceptor-side non-heme iron. Biochim Biophys Acta 1015:141–149

    CAS  Google Scholar 

  32. Draber W, Tietjen K, Kluth JF, Trebst A (1991) Herbicides in photosynthesis research. Angew Chem Int Ed 30:1621–1633

    Google Scholar 

  33. Dutton PL, Leigh JS, Wraight CA (1973) Direct measurement of the midpoint potential of the primary electron acceptor in Rhodopseudomonas spheroides in situ and in the isolated state: some relationships with pH and o-phenanthroline. FEBS Lett 36:169–173

    PubMed  CAS  Google Scholar 

  34. Eaton-Rye JJ, Govindjee (1988) Electron-transfer through the quinone acceptor complex of Photosystem II after one or two actinic flashes in bicarbonate-depleted spinach thylakoid membranes. Biochim Biophys Acta 935:248–257

    CAS  Google Scholar 

  35. Eckert HJ, Renger G (1980) Photochemistry of the reaction centers of system II under repetitive flash group excitation in isolated chloroplasts. Photochem Photobiol 31:501–511

    CAS  Google Scholar 

  36. Egner U, Hover GA, Saenger W (1993) Modeling and energy minimization studies on the herbicide binding-protein (D1) in Photosystem II of plants. Biochim Biophys Acta 1142:106–114

    CAS  Google Scholar 

  37. Elstner EF, Heupel A (1973) Decarboxylation of α-keto acids by isolated chloroplasts. Biochim Biophys Acta 325:182–188

    PubMed  CAS  Google Scholar 

  38. Feher G, Okamura MY (1999) The primary and secondary acceptors in bacterial photosynthesis: II. The structure of the Fe2+-Q complex. Appl Magn Reson 16:63–100

    CAS  Google Scholar 

  39. Feher G, Allen JP, Okamura MY, Rees DC (1989) Structure and function of bacterial photosynthetic reaction centers. Nature 339:111–116

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  41. 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 

  42. Fromme R, Grotjohann I, Fromme P (2008) Structure and function of photosystem I. In: Renger G (ed) Primary processes of photosynthesis, principles and apparatus—part 2. RSC Publishing, Cambridge, pp 111–146

    Google Scholar 

  43. Fufezan C, Drepper F, Juhnke HD, Lancaster CRD, Un S, Rutherford AW, Krieger-Liszkay A (2005) Herbicide-induced changes in charge recombination and redox potential of QA in the T4 mutant of Blastochloris viridis. Biochemistry 44:5931–5939

    PubMed  CAS  Google Scholar 

  44. Gillmor SA, Villasenor A, Fletterick R, Sigal E, Browner MF (1997) The structure of mammalian 15-lipoxygenase reveals similarity to the lipases and the determinants of substrate specificity. Nat Struct Biol 4:1003–1009

    PubMed  CAS  Google Scholar 

  45. Ginet N, Lavergne J (2000) Interactions between the donor and acceptor sides in bacterial reaction centers. Biochemistry 39:16252–16262

    PubMed  CAS  Google Scholar 

  46. Golbeck JH (ed) (2006) Photosystem I—the light-driven plastocyanin:ferredoxin oxidoreductase, advances in photosynthesis and respiration. Springer, Dordrecht

    Google Scholar 

  47. Govindjee MPJ, Pulles R, Govindjee, van Gorkom HJ, Duysens LNM (1976) Inhibition of reoxidation of secondary electron acceptor of photosystem II by bicarbonate depletion. Biochim Biophys Acta 449:602–605

    PubMed  CAS  Google Scholar 

  48. Graige MS, Feher G, Okamura MY (1998) Conformational gating of the electron transfer reaction Q A *QB → QAQ B * in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay. Proc Natl Acad Sci USA 95:11679–11684

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  50. Hermes S, Bremm O, Garczarek F, Derrien V, Liebisch P, Loja P, Sebban P, Gerwert K, Haumann M (2006) A time-resolved iron-specific X-ray absorption experiment yields no evidence for an Fe2+ → Fe3+ transition during Q A  → QB electron transfer in the photosynthetic reaction center. Biochemistry 45:353–359

    PubMed  CAS  Google Scholar 

  51. Hienerwadel R, Berthomieu C (1995) Bicarbonate binding to the non-heme iron of photosystem II investigated by Fourier transform infrared difference spectroscopy and 13C-labeled bicarbonate. Biochemistry 34:16288–16297

    PubMed  CAS  Google Scholar 

  52. Hohmann-Marriott MF, Blankenship RE (2011) Evolution of photosynthesis. Annu Rev Plant Biol 62:515–548

    PubMed  CAS  Google Scholar 

  53. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14:33–38

    PubMed  CAS  Google Scholar 

  54. Ido K, Gross CM, Guerrero F, Sedoud A, Lai TL, Ifuku K, Rutherford AW, Krieger-Liszkay A (2011) High and low potential forms of the QA quinone electron acceptor in Photosystem II of Thermosynechococcus elongatus and spinach. J Photochem Photobiol B 104:154–157

    PubMed  CAS  Google Scholar 

  55. Igamberdiev AU, Bykova NV, Kleczkowski LA (1999) Origins and metabolism of formate in higher plants. Plant Physiol Biochem 37:503–513

    CAS  Google Scholar 

  56. Ikegami I, Katoh S (1973) Studies on chlorophyll fluorescence in chloroplasts. 2. Effect of ferricyaninde on induction of fluorescence in presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea. Plant Cell Physiol 14:829–836

    CAS  Google Scholar 

  57. Ishikita H, Knapp EW (2005) Oxidation of the non-heme iron complex in photosystem II. Biochemistry 44:14772–14783

    PubMed  CAS  Google Scholar 

  58. Ishikita H, Morra G, Knapp EW (2003) Redox potential of quinones in photosynthetic reaction centers from Rhodobacter sphaeroides: dependence on protonation of Glu-L212 and Asp-L213. Biochemistry 42:3882–3892

    PubMed  CAS  Google Scholar 

  59. Ishikita H, Galstyan A, Knapp EW (2007) Redox potential of the non-heme iron complex in bacterial photosynthetic reaction center. Biochim Biophys Acta 1767:1300–1309

    PubMed  CAS  Google Scholar 

  60. Ishikita H, Hasegawa K, Noguchi T (2011) How does the QB site influence propagate to the QA site in photosystem II? Biochemistry 50:5436–5442

    PubMed  CAS  Google Scholar 

  61. Jackson JB, Cogdell RJ, Crofts AR (1973) Some effects of o-phenanthroline on electron transport in chromatophores from photosynthetic bacteria. Biochim Biophys Acta 292:218–225

    PubMed  CAS  Google Scholar 

  62. Johnson GN, Rutherford AW, Krieger A (1995) A change in the midpoint potential of the quinone QA in photosystem II associated with photoactivation of oxygen evolution. Biochim Biophys Acta 1229:202–207

    Google Scholar 

  63. Joliot P, Joliot A (1981) A photosystem II electron acceptor which is not a plastoquinone. FEBS Lett 134:155–158

    CAS  Google Scholar 

  64. Joliot P, Barbieri G, Chabaud R (1969) A new model of photochemical centers in system II. Photochem Photobiol 10:309–329

    CAS  Google Scholar 

  65. Kamiya N, Shen JR (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7 Å resolution. Proc Natl Acad Sci USA 100:98–103

    PubMed  CAS  Google Scholar 

  66. Kato Y, Shibamoto T, Yamamoto S, Watanabe T, Ishida N, Sugiura M, Rappaport F, Boussac A (2012) Influence of the PsbA1/PsbA3, Ca2+/Sr2+ and Cl/Br exchanges on the redox potential of the primary quinone QA in Photosystem II from Thermosynechococcus elongatus as revealed by spectroelectrochemistry. Biochim Biophys Acta 1817:1998–2004

    PubMed  CAS  Google Scholar 

  67. Kawakami K, Umena Y, Kamiya N, Shen JR (2009) Location of chloride and its possible functions in oxygen-evolving photosystem II revealed by X-ray crystallography. Proc Natl Acad Sci USA 106:8567–8572

    PubMed  CAS  Google Scholar 

  68. Kern J, Guskov A (2011) Lipids in photosystem II: multifunctional cofactors. J Photochem Photobiol B 104:19–34

    PubMed  CAS  Google Scholar 

  69. Kern J, Loll B, Lüneberg C, DiFiore D, Biesiadka J, Irrgang KD, Zouni A (2005) Purification, characterisation and crystallisation of photosystem II from Thermosynechococcus elongatus cultivated in a new type of photobioreactor. Biochim Biophys Acta 1706:147–157

    PubMed  CAS  Google Scholar 

  70. Kern J, Alonso-Mori R, Hellmich J, Tran R, Hattne J, Laksmono H, Glöckner C, Echols N, Sierra RG, Sellberg J, Lassalle-Kaiser B, Gildea RJ, Glatzel P, Grosse-Kunstleve RW, Latimer MJ, McQueen TA, DiFiore D, Fry AR, Messerschmidt M, Miahnahri A, Schafer DW, Seibert MM, Sokaras D, Weng TC, Zwart PH, White WE, Adams PD, Bogan MJ, Boutet S, Williams GJ, Messinger J, Sauter NK, Zouni A, Bergmann U, Yano J, Yachandra VK (2012) Room temperature femtosecond X-ray diffraction of photosystem II microcrystals. Proc Natl Acad Sci USA 109:9721–9726

    PubMed  CAS  Google Scholar 

  71. Kern J, Alonso-Mori R, Tran R, Hattne J, Gildea RJ, Echols N, Glöckner C, Hellmich J, Laksmono H, Sierra RG, Lassalle-Kaiser B, Koroidov S, Lampe A, Han GY, Gul S, DiFiore D, Milathianaki D, Fry AR, Miahnahri A, Schafer DW, Messerschmidt M, Seibert MM, Koglin JE, Sokaras D, Weng TC, Sellberg J, Latimer MJ, Grosse-Kunstleve RW, Zwart PH, White WE, Glatzel P, Adams PD, Bogan MJ, Williams GJ, Boutet S, Messinger J, Zouni A, Sauter NK, Yachandra VK, Bergmann U, Yano J (2013) Simultaneous femtosecond X-ray spectroscopy and diffraction of photosystem II at room temperature. Science 340:491–495

    PubMed  CAS  Google Scholar 

  72. Kirmaier C, Holten D, Debus RJ, Feher G, Okamura MY (1986) Primary photochemistry of iron-depleted and zinc-reconstituted reaction centers from Rhodopseudomonas sphaeroides. Proc Natl Acad Sci USA 83:6407–6411

    PubMed  CAS  Google Scholar 

  73. Kitoh-Nishioka H, Ando K (2012) Fragment molecular orbital study on electron tunneling mechanisms in bacterial photosynthetic reaction center. J Phys Chem B 116:12933–12945

    PubMed  CAS  Google Scholar 

  74. Klimov VV, Dolan E, Shaw ER, Ke B (1980) Interaction between the intermediary electron-acceptor (pheophytin) and a possible plastoquinone–iron complex in photosystem II reaction centers. Proc Natl Acad Sci USA 77:7227–7231

    PubMed  CAS  Google Scholar 

  75. Knaff DB (1975) Effect of o-phenanthroline on the midpoint potential of primary electron acceptor of photosystem II. Biochim Biophys Acta 376:583–587

    PubMed  CAS  Google Scholar 

  76. Koepke J, Krammer EM, Klingen AR, Sebban P, Ullmann GM, Fritzsch G (2007) pH modulates the quinone position in the photosynthetic reaction center from Rhodobacter sphaeroides in the neutral and charge separated states. J Mol Biol 371:396–409

    PubMed  CAS  Google Scholar 

  77. Kok B, Forbush B, McGloin M (1970) Cooperation of charges in photosynthetic O2 evolution—I. A linear four step mechanism. Photochem Photobiol 11:457–475

    PubMed  CAS  Google Scholar 

  78. Kós PB, Deák Z, Cheregi O, Vass I (2008) Differential regulation of psbA and psbD gene expression, and the role of the different D1 protein copies in the cyanobacterium Thermosynechococcus elongatus BP-1. Biochim Biophys Acta 1777:74–83

    PubMed  Google Scholar 

  79. Koua FH, Umena Y, Kawakami K, Shen JR (2013) Structure of Sr-substituted photosystem II at 2.1 Å resolution and its implications in the mechanism of water oxidation. Proc Natl Acad Sci U S A 110:3889–3894

    PubMed  CAS  Google Scholar 

  80. Kovacs JA, Brines LM (2007) Understanding how the thiolate sulfur contributes to the function of the non-heme iron enzyme superoxide reductase. Acc Chem Res 40:501–509

    PubMed  CAS  Google Scholar 

  81. Kovaleva EG, Lipscomb JD (2008) Versatility of biological non-heme Fe(II) centers in oxygen activation reactions. Nat Chem Biol 4:186–193

    PubMed  CAS  Google Scholar 

  82. Krieger A, Weis E (1992) Energy-dependent quenching of chlorophyll a fluorescence—the involvement of proton-calcium exchange at photosystem II. Photosynthetica 27:89–98

    CAS  Google Scholar 

  83. Krieger A, Weis E, Demeter S (1993) Low-pH-induced Ca2+ ion release in the water-splitting system is accompanied by a shift in the midpoint redox potential of the primary quinone acceptor QA. Biochim Biophys Acta 1144:411–418

    CAS  Google Scholar 

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

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  86. Kuglstatter A, Ermler U, Michel H, Baciou L, Fritzsch G (2001) X-ray structure analyses of photosynthetic reaction center variants from Rhodobacter sphaeroides: structural changes induced by point mutations at position L209 modulate electron and proton transfer. Biochemistry 40:4253–4260

    PubMed  CAS  Google Scholar 

  87. Kurreck J, Garbers A, Reifarth F, Andreasson LE, Parak F, Renger G (1996) Isolation and properties of PS II membrane fragments depleted of the non heme iron center. FEBS Lett 381:53–57

    PubMed  CAS  Google Scholar 

  88. Lancaster CRD (2008) Structure of reaction centers in anoxygenic bacteria. In: Renger G (ed) Primary processes of photosynthesis, principles and apparatus—part 2. RSC Publishing, Cambridge, pp 5–56

    Google Scholar 

  89. Lancaster CRD, Michel H (1999) Refined crystal structures of reaction centres from Rhodopseudomonas viridis in complexes with the herbicide atrazine and two chiral atrazine derivatives also lead to a new model of the bound carotenoid. J Mol Biol 286:883–898

    PubMed  CAS  Google Scholar 

  90. Lancaster CRD, Bibikova MV, Sabatino P, Oesterhelt D, Michel H (2000) Structural basis of the drastically increased initial electron transfer rate in the reaction center from a Rhodopseudomonas viridis mutant described at 2.00-Å resolution. J Biol Chem 275:39364–39368

    PubMed  CAS  Google Scholar 

  91. Lancaster CRD, Hunte C, Kelley J, Trumpower BL, Ditchfield R (2007) A comparison of stigmatellin conformations, free and bound to the photosynthetic reaction center and the cytochrome bc 1 complex. J Mol Biol 368:197–208

    PubMed  CAS  Google Scholar 

  92. Leibl W, Breton J (1991) Kinetic properties of the acceptor quinone complex in Rhodopseudomonas viridis. Biochemistry 30:9634–9642

    PubMed  CAS  Google Scholar 

  93. Leibl W, Sinning I, Ewald G, Michel H, Breton J (1993) Evidence that serine L223 is involved in the proton-transfer pathway to QB in the photosynthetic reaction center of Rhodopseudomonas viridis. Biochemistry 32:1958–1964

    PubMed  CAS  Google Scholar 

  94. Li JL, Takahashi E, Gunner MR (2000) -ΔG°AB and pH dependence of the electron transfer from P+Q A QB to P+QAQ B in Rhodobacter sphaeroides reaction centers. Biochemistry 39:7445–7454

    PubMed  CAS  Google Scholar 

  95. 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 438:1040–1044

    PubMed  CAS  Google Scholar 

  96. Loll B, Broser M, Kos PB, Kern J, Biesiadka J, Vass I, Saenger W, Zouni A (2008) Modeling of variant copies of subunit D1 in the structure of photosystem II from Thermosynechococcus elongatus. Biol Chem 389:609–617

    PubMed  CAS  Google Scholar 

  97. Lubitz W, Feher G (1999) The primary and secondary acceptors in bacterial photosynthesis III. Characterization of the quinone radicals Q −•A and Q −•B by EPR and ENDOR. Appl Magn Reson 17:1–48

    CAS  Google Scholar 

  98. MacMillan F, Lendzian F, Renger G, Lubitz W (1995) EPR and ENDOR investigation of the primary electron acceptor radical anion Q •−A in iron-depleted photosystem II membrane fragments. Biochemistry 34:8144–8156

    PubMed  CAS  Google Scholar 

  99. Mathé C, Weill CO, Mattioli TA, Berthomieu C, Houee-Levin C, Tremey E, Niviere V (2007) Assessing the role of the active-site cysteine ligand in the superoxide reductase from Desulfoarculus baarsii. J Biol Chem 282:22207–22216

    PubMed  Google Scholar 

  100. Mathis P, Sinning I, Michel H (1992) Kinetics of electron transfer from the primary to the secondary quinone in Rhodopseudomonas viridis. Biochim Biophys Acta 1098:151–158

    CAS  Google Scholar 

  101. Michel H, Epp O, Deisenhofer J (1986) Pigment protein interactions in the photosynthetic reaction center from Rhodopseudomonas viridis. EMBO J 5:2445–2451

    PubMed  CAS  Google Scholar 

  102. Miller AF (2012) Superoxide dismutases: ancient enzymes and new insights. FEBS Lett 586:585–595

    PubMed  CAS  Google Scholar 

  103. Müh F, Zouni A (2011) Light-induced water oxidation in photosystem II. Front Biosci 16:3072–3132

    Google Scholar 

  104. Müh F, Rautter J, Lubitz W (1996) Effects of zwitterionic detergents on the primary donor of bacterial reaction centers. Ber Bunsenges Phys Chem (Phys Chem Chem Phys) 100:1974–1977

    Google Scholar 

  105. Müh F, Rautter J, Lubitz W (1997) Two distinct conformations of the primary electron donor in reaction centers from Rhodobacter sphaeroides revealed by ENDOR/TRIPLE-spectroscopy. Biochemistry 36:4155–4162

    PubMed  Google Scholar 

  106. Müh F, Schulz C, Schlodder E, Jones MR, Rautter J, Kuhn M, Lubitz W (1998) Effects of zwitterionic detergents on the electronic structure of the primary donor and the charge recombination kinetics of P+Q A in native and mutant reaction centers from Rhodobacter sphaeroides. Photosynth Res 55:199–205

    Google Scholar 

  107. Müh F, Glöckner C, Hellmich J, Zouni A (2012) Light-induced quinone reduction in photosystem II. Biochim Biophys Acta 1817:44–65

    PubMed  Google Scholar 

  108. Mulo P, Sicora C, Aro EM (2009) Cyanobacterial psbA gene family: optimization of oxygenic photosynthesis. Cell Mol Life Sci 66:3697–3710

    PubMed  CAS  Google Scholar 

  109. Mulo P, Sakurai I, Aro EM (2012) Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: from transcription to PSII repair. Biochim Biophys Acta 1817:247–257

    PubMed  CAS  Google Scholar 

  110. Murray JW, Maghlaoui K, Kargul J, Ishida N, Lai TL, Rutherford AW, Sugiura M, Boussac A, Barber J (2008) X-ray crystallography identifies two chloride binding sites in the oxygen evolving centre of Photosystem II. Energy Environ Sci 1:161–166

    CAS  Google Scholar 

  111. Nakamura Y, Kaneko T, Sato S, Ikeuchi M, Katoh H, Sasamoto S, Watanabe A, Iriguchi M, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M, Tabata S (2002) Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. DNA Res 9:123–130, Suppl. 135–148

  112. Nelson MJ (1988) Catecholate complexes of ferric soybean lipoxygenase-1. Biochemistry 27:4273–4278

    CAS  Google Scholar 

  113. Nicholls P (2012) Classical catalase: ancient and modern. Arch Biochem Biophys 525:95–101

    PubMed  CAS  Google Scholar 

  114. Nixon PJ, Michoux F, Yu JF, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1–16

    PubMed  CAS  Google Scholar 

  115. Nugent JHA (2001) Photoreducible high spin iron electron paramagnetic resonance signals in dark-adapted Photosystem II: are they oxidised non-haem iron formed from interaction of oxygen with PSII electron acceptors? Biochim Biophys Acta 1504:288–298

    PubMed  CAS  Google Scholar 

  116. Nugent JHA, Doetschman DC, MacLachlan DJ (1992) Characterization of the multiple ESR line shapes of iron semiquinones in photosystem 2. Biochemistry 31:2935–2941

    PubMed  CAS  Google Scholar 

  117. Ohad I, Kyle DJ, Arntzen CJ (1984) Membrane-protein damage and repair: removal and replacement of inactivated 32-kilodalton Polypeptides in chloroplast membranes. J Cell Biol 99:481–485

    PubMed  CAS  Google Scholar 

  118. Okamura MY, Isaacson RA, Feher G (1975) Primary acceptor in bacterial photosynthesis—Obligatory role of ubiquinone in photoactive reaction centers of Rhodopseudomonas spheroides. Proc Natl Acad Sci USA 72:3491–3495

    PubMed  CAS  Google Scholar 

  119. Okamura MY, Paddock ML, Graige MS, Feher G (2000) Proton and electron transfer in bacterial reaction centers. Biochim Biophys Acta 1458:148–163

    PubMed  CAS  Google Scholar 

  120. Ono T, Zimmermann JL, Inoue Y, Rutherford AW (1986) EPR evidence for a modified S-state transition in chloride-depleted photosystem II. Biochim Biophys Acta 851:193–201

    CAS  Google Scholar 

  121. Palavan-Unsal N, Arisan D (2009) Nitric oxide signalling in plants. Bot Rev 75:203–229

    Google Scholar 

  122. Petrouleas V, Crofts AR (2005) The iron–quinone acceptor complex. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light-driven water:plastoquinone oxidoreductase. Springer, Dordrecht, pp 177–206

    Google Scholar 

  123. Petrouleas V, Diner BA (1986) Identification of Q400, a high-potential electron acceptor of photosystem II, with the iron of the quinone-iron acceptor complex. Biochim Biophys Acta 849:264–275

    CAS  Google Scholar 

  124. Petrouleas V, Diner BA (1987) Light-induced oxidation of the acceptor-side Fe(II) of photosystem II by exogenous quinones acting through the QB binding site. 1. Quinones, kinetics and pH-dependence. Biochim Biophys Acta 893:126–137

    CAS  Google Scholar 

  125. Petrouleas V, Diner BA (1990) Formation by NO of nitrosyl adducts of redox components of the photosystem II reaction center. I. NO binds to the acceptor-side non-heme iron. Biochim Biophys Acta 1015:131–140

    CAS  Google Scholar 

  126. Pinto AF, Rodrigues JV, Teixeira M (2010) Reductive elimination of superoxide: structure and mechanism of superoxide reductases. Biochim Biophys Acta 1804:285–297

    PubMed  CAS  Google Scholar 

  127. Pospísil P (2009) Production of reactive oxygen species by photosystem II. Biochim Biophys Acta 1787:1151–1160

    PubMed  Google Scholar 

  128. Pospísil P, Arato A, Krieger-Liszkay A, Rutherford AW (2004) Hydroxyl radical generation by photosystem II. Biochemistry 43:6783–6792

    PubMed  Google Scholar 

  129. Qiao WH, Fan LM (2008) Nitric oxide signaling in plant responses to abiotic stresses. J Integr Plant Biol 50:1238–1246

    PubMed  CAS  Google Scholar 

  130. Renger G (2008) Functional pattern of photosystem II. In: Renger G (ed) Primary processes of photosynthesis, principles and apparatus—part 2. RSC Publishing, Cambridge, pp 237–290

    Google Scholar 

  131. Renger G, Renger T (2008) Photosystem II: the machinery of photosynthetic water splitting. Photosynth Res 98:53–80

    PubMed  CAS  Google Scholar 

  132. Renger T, Schlodder E (2011) Optical properties, excitation energy and primary charge transfer in photosystem II: theory meets experiment. J Photochem Photobiol B 104:126–141

    PubMed  CAS  Google Scholar 

  133. Robinson HH, Eaton-Rye JJ, van Rensen JJS, Govindjee (1984) The effects of bicarbonate depletion and formate incubation on the kinetics of oxidation–reduction reactions of the Photosystem II quinone acceptor complex. Z Naturforsch C 39:382–385

    Google Scholar 

  134. Rokka A, Suorsa M, Saleem A, Battchikova N, Aro EM (2005) Synthesis and assembly of thylakoid protein complexes: multiple assembly steps of photosystem II. Biochem J 388:159–168

    PubMed  CAS  Google Scholar 

  135. Rutherford AW, Zimmermann JL (1984) A new EPR signal attributed to the primary plastosemiquinone acceptor in photosystem II. Biochim Biophys Acta 767:168–175

    CAS  Google Scholar 

  136. Rutherford AW, Osyczka A, Rappaport F (2012) Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O2. FEBS Lett 586:603–616

    PubMed  CAS  Google Scholar 

  137. Saito K, Rutherford AW, Ishikita H (2013) Mechanism of proton-coupled quinone reduction in Photosystem II. Proc Natl Acad Sci USA 110:954–959

    PubMed  CAS  Google Scholar 

  138. Sander J, Nowaczyk M, Buchta J, Dau H, Vass I, Deak Z, Dorogi M, Iwai M, Rögner M (2010) Functional characterization and quantification of the alternative PsbA copies in Thermosynechococcus elongatus and their role in photoprotection. J Biol Chem 285:29851–29856

    PubMed  CAS  Google Scholar 

  139. Semenov AY, Kurashov VN, Mamedov MD (2011) Transmembrane charge transfer in photosynthetic reaction centers: some similarities and distinctions. J Photochem Photobiol B 104:326–332

    PubMed  CAS  Google Scholar 

  140. Sétif A, Leibl W (2008) Functional pattern of photosystem I in oxygen evolving organisms. In: Renger G (ed) Primary processes of photosynthesis, principles and apparatus. RSC Publishing, Cambridge, pp 147–191

    Google Scholar 

  141. Sharma S, Jasti J, Kumar J, Mohanty AK, Singh TP (2003) Crystal structure of a proteolytically generated functional monoferric C-lobe of bovine lactoferrin at 1.9 Å resolution. J Mol Biol 331:485–496

    PubMed  CAS  Google Scholar 

  142. Shevela D, Eaton-Rye JJ, Shen JR, Govindjee (2012) Photosystem II and the unique role of bicarbonate: a historical perspective. Biochim Biophys Acta 1817:1134–1151

    PubMed  CAS  Google Scholar 

  143. Shi LX, Hall M, Funk C, Schröder WP (2012) Photosystem II, a growing complex: updates on newly discovered components and low molecular mass proteins. Biochim Biophys Acta 1817:13–25

    PubMed  CAS  Google Scholar 

  144. Shibamoto T, Kato Y, Sugiura M, 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

    PubMed  CAS  Google Scholar 

  145. Shlyk-Kerner O, Samish I, Kaftan D, Holland N, Sai PS, Kless H, Scherz A (2006) Protein flexibility acclimatizes photosynthetic energy conversion to the ambient temperature. Nature 442:827–830

    PubMed  CAS  Google Scholar 

  146. Shongwe MS, Smith CA, Ainscough EW, Baker HM, Brodie AM, Baker EN (1992) Anion binding by human lactoferrin—results from crystallographic and physicochemical studies. Biochemistry 31:4451–4458

    PubMed  CAS  Google Scholar 

  147. Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248:447–455

    PubMed  CAS  Google Scholar 

  148. Sinning I (1992) Herbicide binding in the bacterial photosynthetic reaction center. Trends Biochem Sci 17:150–154

    PubMed  CAS  Google Scholar 

  149. Sinning I, Koepke J, Michel H (1990) Recent advances in the structure analysis of Rhodopseudomonas viridis reaction center mutants. In: Michel-Beyerle ME (ed) Reaction centers of photosynthetic bacteria. Springer, Berlin, pp 199–208

    Google Scholar 

  150. Smith CA, Anderson BF, Baker HM, Baker EN (1992) Metal substitution in transferrins—the crystal-structure of human copper-lactoferrin at 2.1-Å resolution. Biochemistry 31:4527–4533

    PubMed  CAS  Google Scholar 

  151. Smith CA, Anderson BF, Baker HM, Baker EN (1994) Structure of copper-substituted and oxalate-substituted human lactoferrin at 2.0 Å Resolution. Acta Cryst D 50:302–316

    CAS  Google Scholar 

  152. Snel JFH, van Rensen JJS (1984) Reevaluation of the role of bicarbonate and formate in the regulation of photosynthetic electron flow in broken chloroplasts. Plant Physiol 75:146–150

    PubMed  CAS  Google Scholar 

  153. Sobolev V, Edelman M (1995) Modeling the quinone-B binding-site of the photosystem-II reaction-center using notions of complementarity and contact-surface between atoms. Proteins 21:214–225

    PubMed  CAS  Google Scholar 

  154. Solomon EI, Brunold TC, Davis MI, Kemsley JN, Lee SK, Lehnert N, Neese F, Skulan AJ, Yang YS, Zhou J (2000) Geometric and electronic structure/function correlations in non-heme iron enzymes. Chem Rev 100:235–349

    PubMed  CAS  Google Scholar 

  155. Solomon EI, Decker A, Lehnert N (2003) Non-heme iron enzymes: contrasts to heme catalysis. Proc Natl Acad Sci USA 100:3589–3594

    PubMed  CAS  Google Scholar 

  156. Steiger HM, Beck E (1981) Formation of hydrogen peroxide and oxygen dependence of photosynthetic CO2 assimilation by intact chloroplasts. Plant Cell Physiol 22:561–576

    CAS  Google Scholar 

  157. Stemler A, Govindjee (1973) Bicarbonate ion as a critical factor in photosynthetic oxygen evolution. Plant Physiol 52:119–123

    PubMed  CAS  Google Scholar 

  158. Stemler A, Murphy J (1985) Inhibition of HCO3 binding to photosystem II by atrazine at a low-affinity herbicide binding site. Plant Physiol 77:179–182

    PubMed  CAS  Google Scholar 

  159. Takahashi R, Hasegawa K, Takano A, Noguchi T (2010) Structures and binding sites of phenolic herbicides in the QB pocket of photosystem II. Biochemistry 49:5445–5454

    PubMed  CAS  Google Scholar 

  160. Takano A, Takahashi R, Suzuki H, Noguchi T (2008) Herbicide effect on the hydrogen-bonding interaction of the primary quinone electron acceptor QA in photosystem II as studied by Fourier transform infrared spectroscopy. Photosynth Res 98:159–167

    PubMed  CAS  Google Scholar 

  161. Tandori J, Maróti P, Alexov E, Sebban P, Baciou L (2002) Key role of proline L209 in connecting the distant quinone pockets in the reaction center of Rhodobacter sphaeroides. Proc Natl Acad Sci USA 99:6702–6706

    PubMed  CAS  Google Scholar 

  162. Tiede DM, Vazquez J, Cordova J, Marone PA (1996) Time-resolved electrochromism associated with the formation of quinone anions in the Rhodobacter sphaeroides R26 reaction center. Biochemistry 35:10763–10775

    PubMed  CAS  Google Scholar 

  163. Tietjen KG, Kluth JF, Andree R, Haug M, Lindig M, Müller KH, Wroblowsky HJ, Trebst A (1991) The herbicide binding niche of photosystem II—a model. Pestic Sci 31:65–72

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  165. Utschig LM, Thurnauer NC (2004) Metal ion modulated electron transfer in photosynthetic proteins. Acc Chem Res 37:439–447

    PubMed  CAS  Google Scholar 

  166. Utschig LM, Greenfield SR, Tang J, Laible PD, Thurnauer MC (1997) Influence of iron-removal procedures on sequential electron transfer in photosynthetic bacterial reaction centers studied by transient EPR spectroscopy. Biochemistry 36:8548–8558

    PubMed  CAS  Google Scholar 

  167. Utschig LM, Ohigashi Y, Thurnauer MC, Tiede DM (1998) A new metal-binding site in photosynthetic bacterial reaction centers that modulates QA to QB electron transfer. Biochemistry 37:8278–8281

    PubMed  CAS  Google Scholar 

  168. Utschig LM, Poluektov O, Schlesselman SL, Thurnauer MC, Tiede DM (2001) Cu2+ site in photosynthetic bacterial reaction centers from Rhodobacter sphaeroides, Rhodobacter capsulatus, and Rhodopseudomonas viridis. Biochemistry 40:6132–6141

    PubMed  CAS  Google Scholar 

  169. van Rensen JJS, Klimov VV (2005) Bicarbonate interactions. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light-driven water:plastoquinone oxidoreductase. Springer, Dordrecht, pp 329–345

    Google Scholar 

  170. van Rensen JJS, Tonk WJM, Debruijn SM (1988) Involvement of bicarbonate in the protonation of the secondary quinone electron acceptor of photosystem II via the non-heme iron of the quinone-iron acceptor complex. FEBS Lett 226:347–351

    Google Scholar 

  171. van Rensen JJS, Xu CH, Govindjee (1999) Role of bicarbonate in photosystem II, the water-plastoquinone oxido-reductase of plant photosynthesis. Physiol Plant 105:585–592

    Google Scholar 

  172. Veitch NC (2004) Horseradish peroxidase: a modern view of a classic enzyme. Phytochemistry 65:249–259

    PubMed  CAS  Google Scholar 

  173. Wöhri AB, Katona G, Johansson LC, Fritz E, Malmerberg E, Andersson M, Vincent J, Eklund M, Cammarata M, Wulff M, Davidsson J, Groenhof G, Neutze R (2010) Light-induced structural changes in a photosynthetic reaction center caught by Laue diffraction. Science 328:630–633

    PubMed  Google Scholar 

  174. Wraight CA (2004) Proton and electron transfer in the acceptor quinone complex of photosynthetic reaction centers from Rhodobacter sphaeroides. Front Biosci 9:309–337

    PubMed  CAS  Google Scholar 

  175. Wydrzynski T, Satoh K (eds) (2005) Photosystem II: the light-driven water:plastoquinone oxidoreductase. Advances in photosynthesis and respiration. Springer, Dordrecht

    Google Scholar 

  176. Xiong J, Subramaniam S, Govindjee (1996) Modeling of the D1/D2 proteins and cofactors of the photosystem II reaction center: implications for herbicide and bicarbonate binding. Protein Sci 5:2054–2073

    PubMed  CAS  Google Scholar 

  177. Xu CH, Taoka S, Crofts AR, Govindjee (1991) Kinetic characteristics of formate/formic acid binding at the plastoquinone reductase site in spinach thylakoids. Biochim Biophys Acta 1098:32–40

    CAS  Google Scholar 

  178. Yeh AP, Hu Y, Jenney FE Jr, Adams MW, Rees DC (2000) Structures of the superoxide reductase from Pyrococcus furiosus in the oxidized and reduced states. Biochemistry 39:2499–2508

    PubMed  CAS  Google Scholar 

  179. Zimmermann K, Heck M, Frank J, Kern J, Vass I, Zouni A (2006) Herbicide binding and thermal stability of photosystem II isolated from Thermosynechococcus elongatus. Biochim Biophys Acta 1757:106–114

    PubMed  CAS  Google Scholar 

  180. 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, principles and apparatus—part 2. RSC Publishing, Cambridge, pp 193–236

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by DFG through SFB 1078 (project A5) and Cluster of Excellence “UniCat” coordinated by TU Berlin (Project B1).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Athina Zouni.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Müh, F., Zouni, A. The nonheme iron in photosystem II. Photosynth Res 116, 295–314 (2013). https://doi.org/10.1007/s11120-013-9926-y

Download citation

Keywords

  • Bicarbonate
  • Crystal structure
  • Electron transfer
  • Formate
  • Herbicide
  • Nitric oxide
  • Proton transfer
  • Quinone
  • Reaction center
  • Reactive oxygen species
  • Redox potential