Principles of Natural Photosynthesis

  • Vera Krewald
  • Marius Retegan
  • Dimitrios A. PantazisEmail author
Part of the Topics in Current Chemistry book series (TOPCURRCHEM, volume 371)


Nature relies on a unique and intricate biochemical setup to achieve sunlight-driven water splitting. Combined experimental and computational efforts have produced significant insights into the structural and functional principles governing the operation of the water-oxidizing enzyme Photosystem II in general, and of the oxygen-evolving manganese–calcium cluster at its active site in particular. Here we review the most important aspects of biological water oxidation, emphasizing current knowledge on the organization of the enzyme, the geometric and electronic structure of the catalyst, and the role of calcium and chloride cofactors. The combination of recent experimental work on the identification of possible substrate sites with computational modeling have considerably limited the possible mechanistic pathways for the critical O–O bond formation step. Taken together, the key features and principles of natural photosynthesis may serve as inspiration for the design, development, and implementation of artificial systems.


Manganese Oxygen-evolving complex Photosystem II Water oxidation 


  1. 1.
    Blankenship RE (2001) Molecular mechanisms of photosynthesis. Blackwell, OxfordGoogle Scholar
  2. 2.
    Hillier W, Messinger J (2005) Mechanism of photosynthetic oxygen production. In: Wydrzynski T, Satoh K (eds) Photosystem II. The light-driven water:plastoquinone oxidoreductase, vol 22, Advances in photosynthesis and respiration. Springer, Dordrecht, pp 567–608CrossRefGoogle Scholar
  3. 3.
    McEvoy JP, Brudvig GW (2006) Chem Rev 106:4455–4483CrossRefGoogle Scholar
  4. 4.
    Messinger J, Renger G (2008) Photosynthetic water splitting. In: Renger G (ed) Primary processes of photosynthesis, part 2: principles and apparatus, vol 9. The Royal Society of Chemistry, Cambridge, pp 291–349Google Scholar
  5. 5.
    Cox N, Pantazis DA, Neese F, Lubitz W (2013) Acc Chem Res 46:1588–1596CrossRefGoogle Scholar
  6. 6.
    Pantazis DA, Cox N, Lubitz W, Neese F (2014) Oxygen-evolving photosystem II. In: Scott RA (ed) Encyclopedia of inorganic and bioinorganic chemistry. Wiley. doi: 10.1002/9781119951438.eibc2166
  7. 7.
    Vinyard DJ, Ananyev GM, Dismukes GC (2013) Annu Rev Biochem 82:577–606CrossRefGoogle Scholar
  8. 8.
    Lubitz W, Reijerse EJ, Messinger J (2008) Energy Environ Sci 1:15–31CrossRefGoogle Scholar
  9. 9.
    Faunce TA, Lubitz W, Rutherford AW, MacFarlane D, Moore GF, Yang P, Nocera DG, Moore TA, Gregory DH, Fukuzumi S, Yoon KB, Armstrong FA, Wasielewski MR, Styring S (2013) Energy Environ Sci 6:695–698CrossRefGoogle Scholar
  10. 10.
    Lewis NS, Nocera DG (2006) Proc Natl Acad Sci U S A 103:15729–15735CrossRefGoogle Scholar
  11. 11.
    Nocera DG (2012) Acc Chem Res 45:767–776CrossRefGoogle Scholar
  12. 12.
    Schlögl R (2010) ChemSusChem 3:209–222CrossRefGoogle Scholar
  13. 13.
    Cogdell RJ, Gardiner AT, Cronin L (2012) Philos Trans R Soc A 370:3819–3826CrossRefGoogle Scholar
  14. 14.
    Dau H, Zaharieva I (2009) Acc Chem Res 42:1861–1870CrossRefGoogle Scholar
  15. 15.
    Dau H, Limberg C, Reier T, Risch M, Roggan S, Strasser P (2010) ChemCatChem 2:724–761CrossRefGoogle Scholar
  16. 16.
    Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Nature 409:739–743CrossRefGoogle Scholar
  17. 17.
    Kamiya N, Shen J-R (2003) Proc Natl Acad Sci U S A 100:98–103CrossRefGoogle Scholar
  18. 18.
    Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Science 303:1831–1838CrossRefGoogle Scholar
  19. 19.
    Biesiadka J, Loll B, Kern J, Irrgang K-D, Zouni A (2004) Phys Chem Chem Phys 6:4733–4736CrossRefGoogle Scholar
  20. 20.
    Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Nature 438:1040–1044CrossRefGoogle Scholar
  21. 21.
    Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Nat Struct Mol Biol 16:334–342CrossRefGoogle Scholar
  22. 22.
    Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Nature 473:55–60CrossRefGoogle Scholar
  23. 23.
    Suga M, Akita F, Hirata K, Ueno G, Murakami H, Nakajima Y, Shimizu T, Yamashita K, Yamamoto M, Ago H, Shen J-R (2014) Nature 517:99–103CrossRefGoogle Scholar
  24. 24.
    Becker K, Cormann KU, Nowaczyk MM (2011) J Photochem Photobiol B 104:204–211CrossRefGoogle Scholar
  25. 25.
    Shi L-X, Hall M, Funk C, Schröder WP (2012) Biochim Biophys Acta Bioenerg 1817:13–25CrossRefGoogle Scholar
  26. 26.
    Fagerlund RD, Eaton-Rye JJ (2011) J Photochem Photobiol B 104:191–203CrossRefGoogle Scholar
  27. 27.
    Wydrzynski T, Satoh K (eds) (2005) Photosystem II. The light-driven water:plastoquinone oxidoreductase, vol 22. Springer, DordrechtGoogle Scholar
  28. 28.
    Rappaport F, Diner BA (2008) Coord Chem Rev 252:259–272CrossRefGoogle Scholar
  29. 29.
    Diner BA, Rappaport F (2002) Annu Rev Plant Biol 53:551–580CrossRefGoogle Scholar
  30. 30.
    Murray JW, Barber J (2007) J Struct Biol 159:228–237CrossRefGoogle Scholar
  31. 31.
    Ho FM, Styring S (2008) Biochim Biophys Acta Bioenerg 1777:140–153CrossRefGoogle Scholar
  32. 32.
    Ho FM (2008) Photosynth Res 98:503–522CrossRefGoogle Scholar
  33. 33.
    Gabdulkhakov A, Guskov A, Broser M, Kern J, Müh F, Saenger W, Zouni A (2009) Structure 17:1223–1234CrossRefGoogle Scholar
  34. 34.
    Ishikita H, Saenger W, Loll B, Biesiadka J, Knapp E-W (2006) Biochemistry 45:2063–2071CrossRefGoogle Scholar
  35. 35.
    Vassiliev S, Comte P, Mahboob A, Bruce D (2010) Biochemistry 49:1873–1881CrossRefGoogle Scholar
  36. 36.
    Vassiliev S, Zaraiskaya T, Bruce D (2012) Biochim Biophys Acta Bioenerg 1817:1671–1678CrossRefGoogle Scholar
  37. 37.
    Rivalta I, Amin M, Luber S, Vassiliev S, Pokhrel R, Umena Y, Kawakami K, Shen JR, Kamiya N, Bruce D, Brudvig GW, Gunner MR, Batista VS (2011) Biochemistry 50:6312–6315CrossRefGoogle Scholar
  38. 38.
    Najafpour MM, Fekete M, Sedigh DJ, Aro E-M, Carpentier R, Eaton-Rye JJ, Nishihara H, Shen J-R, Allakhverdiev SI, Spiccia L (2015) ACS Catal 1499–1512Google Scholar
  39. 39.
    Cardona T, Sedoud A, Cox N, Rutherford AW (2012) Biochim Biophys Acta Bioenerg 1817:26–43CrossRefGoogle Scholar
  40. 40.
    Niyogi KK (2000) Curr Opin Plant Biol 3:455–460CrossRefGoogle Scholar
  41. 41.
    Pascal AA, Liu Z, Broess K, van Oort B, van Amerongen H, Wang C, Horton P, Robert B, Chang W, Ruban A (2005) Nature 436:134–137CrossRefGoogle Scholar
  42. 42.
    Derks A, Schaven K, Bruce D (2015) Biochim Biophys Acta Bioenerg 1847:468–485CrossRefGoogle Scholar
  43. 43.
    Joliot P, Barbieri G, Chabaud R (1969) Photochem Photobiol 10:309–329CrossRefGoogle Scholar
  44. 44.
    Kok B, Forbush B, McGloin M (1970) Photochem Photobiol 11:457–475CrossRefGoogle Scholar
  45. 45.
    Dau H, Haumann M (2008) Coord Chem Rev 252:273–295CrossRefGoogle Scholar
  46. 46.
    Klauss A, Haumann M, Dau H (2012) Proc Natl Acad Sci U S A 109:16035–16040CrossRefGoogle Scholar
  47. 47.
    Dau H, Haumann M (2007) Biochim Biophys Acta Bioenerg 1767:472–483CrossRefGoogle Scholar
  48. 48.
    Klauss A, Haumann M, Dau H (2015) J Phys Chem B 119:2677–2689CrossRefGoogle Scholar
  49. 49.
    Lavergne J, Junge W (1993) Photosynth Res 38:279–296CrossRefGoogle Scholar
  50. 50.
    Rappaport F, Lavergne J (2001) Biochim Biophys Acta Bioenerg 1503:246–259CrossRefGoogle Scholar
  51. 51.
    Klauss A, Krivanek R, Dau H, Haumann M (2009) Photosynth Res 102:499–509CrossRefGoogle Scholar
  52. 52.
    Haumann M, Liebisch P, Müller C, Barra M, Grabolle M, Dau H (2005) Science 310:1019–1021CrossRefGoogle Scholar
  53. 53.
    Gerencsér L, Dau H (2010) Biochemistry 49:10098–10106CrossRefGoogle Scholar
  54. 54.
    Rappaport F, Ishida N, Sugiura M, Boussac A (2011) Energy Environ Sci 4:2520–2524CrossRefGoogle Scholar
  55. 55.
    Bao H, Dilbeck P, Burnap R (2013) Photosynth Res 116:215–229CrossRefGoogle Scholar
  56. 56.
    Service RJ, Hillier W, Debus RJ (2014) Biochemistry 53:1001–1017CrossRefGoogle Scholar
  57. 57.
    Bondar A-N, Dau H (2012) Biochim Biophys Acta Bioenerg 1817:1177–1190CrossRefGoogle Scholar
  58. 58.
    Vogt L, Vinyard DJ, Khan S, Brudvig GW (2015) Curr Opin Chem Biol 25:152–158CrossRefGoogle Scholar
  59. 59.
    Kirby JA, Robertson AS, Smith JP, Thompson AC, Cooper SR, Klein MP (1981) J Am Chem Soc 103:5529–5537CrossRefGoogle Scholar
  60. 60.
    Yano J, Pushkar Y, Glatzel P, Lewis A, Sauer K, Messinger J, Bergmann U, Yachandra V (2005) J Am Chem Soc 127:14974–14975CrossRefGoogle Scholar
  61. 61.
    Grundmeier A, Dau H (2012) Biochim Biophys Acta Bioenerg 1817:88–105CrossRefGoogle Scholar
  62. 62.
    Glöckner C, Kern J, Broser M, Zouni A, Yachandra V, Yano J (2013) J Biol Chem 288:22607–22620CrossRefGoogle Scholar
  63. 63.
    Yano J, Yachandra V (2014) Chem Rev 114:4175–4205CrossRefGoogle Scholar
  64. 64.
    Yano J, Kern J, Sauer K, Latimer MJ, Pushkar Y, Biesiadka J, Loll B, Saenger W, Messinger J, Zouni A, Yachandra VK (2006) Science 314:821–825CrossRefGoogle Scholar
  65. 65.
    Dau H, Liebisch P, Haumann M (2004) Phys Chem Chem Phys 6:4781–4792CrossRefGoogle Scholar
  66. 66.
    Grabolle M, Haumann M, Müller C, Liebisch P, Dau H (2006) J Biol Chem 281:4580–4588CrossRefGoogle Scholar
  67. 67.
    Yano J, Kern J, Irrgang K-D, Latimer MJ, Bergmann U, Glatzel P, Pushkar Y, Biesiadka J, Loll B, Sauer K, Messinger J, Zouni A, Yachandra VK (2005) Proc Natl Acad Sci U S A 102:12047–12052CrossRefGoogle Scholar
  68. 68.
    Luber S, Rivalta I, Umena Y, Kawakami K, Shen JR, Kamiya N, Brudvig GW, Batista VS (2011) Biochemistry 50:6308–6311CrossRefGoogle Scholar
  69. 69.
    Galstyan A, Robertazzi A, Knapp EW (2012) J Am Chem Soc 134:7442–7449CrossRefGoogle Scholar
  70. 70.
    Krewald V, Retegan M, Cox N, Messinger J, Lubitz W, DeBeer S, Neese F, Pantazis DA (2015) Chem Sci 6:1676–1695CrossRefGoogle Scholar
  71. 71.
    Askerka M, Vinyard DJ, Wang J, Brudvig GW, Batista VS (2015) Biochemistry 54:1713–1716CrossRefGoogle Scholar
  72. 72.
    Siegbahn PEM (2008) Chem Eur J 14:8290–8302CrossRefGoogle Scholar
  73. 73.
    Siegbahn PEM (2009) Acc Chem Res 42:1871–1880CrossRefGoogle Scholar
  74. 74.
    Zimmermann JL, Rutherford AW (1984) Biochim Biophys Acta Bioenerg 767:160–167CrossRefGoogle Scholar
  75. 75.
    Brudvig GW, Casey JL, Sauer K (1983) Biochim Biophys Acta Bioenerg 723:366–371CrossRefGoogle Scholar
  76. 76.
    Baldwin MJ, Stemmler TL, Riggs-Gelasco PJ, Kirk ML, Penner-Hahn JE, Pecoraro VL (1994) J Am Chem Soc 116:11349–11356CrossRefGoogle Scholar
  77. 77.
    Krewald V, Lassalle-Kaiser B, Boron TT, Pollock CJ, Kern J, Beckwith MA, Yachandra VK, Pecoraro VL, Yano J, Neese F, DeBeer S (2013) Inorg Chem 52:12904–12914CrossRefGoogle Scholar
  78. 78.
    Cox N, Retegan M, Neese F, Pantazis DA, Boussac A, Lubitz W (2014) Science 345:804–808CrossRefGoogle Scholar
  79. 79.
    Dismukes GC, Siderer Y (1981) Proc Natl Acad Sci U S A 78:274–278CrossRefGoogle Scholar
  80. 80.
    Penner-Hahn JE, Fronko RM, Pecoraro VL, Yocum CF, Betts SD, Bowlby NR (1990) J Am Chem Soc 112:2549–2557CrossRefGoogle Scholar
  81. 81.
    Zheng M, Dismukes GC (1996) Inorg Chem 35:3307–3319CrossRefGoogle Scholar
  82. 82.
    Roelofs TA, Liang W, Latimer MJ, Cinco RM, Rompel A, Andrews JC, Sauer K, Yachandra VK, Klein MP (1996) Proc Natl Acad Sci U S A 93:3335–3340CrossRefGoogle Scholar
  83. 83.
    Iuzzolino L, Dittmer J, Dörner W, Meyer-Klaucke W, Dau H (1998) Biochemistry 37:17112–17119CrossRefGoogle Scholar
  84. 84.
    Dau H, Liebisch P, Haumann M (2003) Anal Bioanal Chem 376:562–583CrossRefGoogle Scholar
  85. 85.
    Ono T-A, Noguchi T, Inoue Y, Kusunoki M, Matsushita T, Oyanagi H (1992) Science 258:1335–1337CrossRefGoogle Scholar
  86. 86.
    Hansson O, Andreasson LE (1982) Biochim Biophys Acta 679:261–268CrossRefGoogle Scholar
  87. 87.
    De Paula JC, Brudvig GW (1985) J Am Chem Soc 107:2643–2648CrossRefGoogle Scholar
  88. 88.
    De Paula JC, Beck WF, Brudvig GW (1986) J Am Chem Soc 108:4002–4009CrossRefGoogle Scholar
  89. 89.
    de Paula JC, Beck WF, Miller A-F, Wilson RB, Brudvig GW (1987) J Chem Soc Faraday Trans 83:3635–3651CrossRefGoogle Scholar
  90. 90.
    Pace RJ, Jin L, Stranger R (2012) Dalton Trans 41:11145–11160CrossRefGoogle Scholar
  91. 91.
    Dasgupta J, Ananyev GM, Dismukes GC (2008) Coord Chem Rev 252:347–360CrossRefGoogle Scholar
  92. 92.
    Kolling DRJ, Cox N, Ananyev GM, Pace RJ, Dismukes GC (2012) Biophys J 103:313–322CrossRefGoogle Scholar
  93. 93.
    Kuntzleman T, Yocum CF (2005) Biochemistry 44:2129–2142CrossRefGoogle Scholar
  94. 94.
    Messinger J, Seaton G, Wydrzynski T, Wacker U, Renger G (1997) Biochemistry 36:6862–6873CrossRefGoogle Scholar
  95. 95.
    Messinger J, Badger M, Wydrzynski T (1995) Proc Natl Acad Sci U S A 92:3209–3213CrossRefGoogle Scholar
  96. 96.
    Beckmann K, Messinger J, Badger M, Wydrzynski T, Hillier W (2009) Photosynth Res 102:511–522CrossRefGoogle Scholar
  97. 97.
    Cox N, Messinger J (2013) Biochim Biophys Acta Bioenerg 1827:1020–1030CrossRefGoogle Scholar
  98. 98.
    Hillier W, Wydrzynski T (2001) Biochim Biophys Acta Bioenerg 1503:197–209CrossRefGoogle Scholar
  99. 99.
    Messinger J (2004) Phys Chem Chem Phys 6:4764–4771CrossRefGoogle Scholar
  100. 100.
    Hillier W, Wydrzynski T (2008) Coord Chem Rev 252:306–317CrossRefGoogle Scholar
  101. 101.
    Haddy A (2007) Photosynth Res 92:357–368CrossRefGoogle Scholar
  102. 102.
    Åhrling KA, Peterson S, Styring S (1997) Biochemistry 36:13148–13152CrossRefGoogle Scholar
  103. 103.
    Messinger J, Nugent JHA, Evans MCW (1997) Biochemistry 36:11055–11060CrossRefGoogle Scholar
  104. 104.
    Messinger J, Robblee JH, Yu WO, Sauer K, Yachandra VK, Klein MP (1997) J Am Chem Soc 119:11349–11350CrossRefGoogle Scholar
  105. 105.
    Åhrling KA, Peterson S, Styring S (1998) Biochemistry 37:8115–8120CrossRefGoogle Scholar
  106. 106.
    Koulougliotis D, Hirsh DJ, Brudvig GW (1992) J Am Chem Soc 114:8322–8323CrossRefGoogle Scholar
  107. 107.
    Hsieh W-Y, Campbell KA, Gregor W, Britt RD, Yoder DW, Penner-Hahn JE, Pecoraro VL (2004) Biochim Biophys Acta Bioenerg 1655:149–157CrossRefGoogle Scholar
  108. 108.
    Zimmermann JL, Rutherford AW (1986) Biochemistry 25:4609–4615CrossRefGoogle Scholar
  109. 109.
    Haddy A, Lakshmi KV, Brudvig GW, Frank HA (2004) Biophys J 87:2885–2896CrossRefGoogle Scholar
  110. 110.
    Horner O, Rivière E, Blondin G, Un S, Rutherford AW, Girerd J-J, Boussac A (1998) J Am Chem Soc 120:7924–7928CrossRefGoogle Scholar
  111. 111.
    Ioannidis N, Petrouleas V (2000) Biochemistry 39:5246–5254CrossRefGoogle Scholar
  112. 112.
    Boussac A, Sugiura M, Rutherford AW, Dorlet P (2009) J Am Chem Soc 131:5050–5051CrossRefGoogle Scholar
  113. 113.
    Kulik LV, Epel B, Lubitz W, Messinger J (2005) J Am Chem Soc 127:2392–2393CrossRefGoogle Scholar
  114. 114.
    Kulik LV, Epel B, Lubitz W, Messinger J (2007) J Am Chem Soc 129:13421–13435CrossRefGoogle Scholar
  115. 115.
    Sauer K, Yano J, Yachandra VK (2005) Photosynth Res 85:73–86CrossRefGoogle Scholar
  116. 116.
    Sauer K, Yano J, Yachandra VK (2008) Coord Chem Rev 252:318–335CrossRefGoogle Scholar
  117. 117.
    Yachandra VK, DeRose VJ, Latimer MJ, Mukerji I, Sauer K, Klein MP (1993) Science 260:675–679CrossRefGoogle Scholar
  118. 118.
    Gatt P, Stranger R, Pace RJ (2011) J Photochem Photobiol B Biol 104:80–93CrossRefGoogle Scholar
  119. 119.
    Jaszewski AR, Petrie S, Pace RJ, Stranger R (2011) Chem Eur J 17:5699–5713CrossRefGoogle Scholar
  120. 120.
    Jaszewski AR, Stranger R, Pace RJ (2011) J Phys Chem B 115:4484–4499CrossRefGoogle Scholar
  121. 121.
    Petrie S, Stranger R, Pace RL (2008) Chem Eur J 14:5482–5494CrossRefGoogle Scholar
  122. 122.
    Gatt P, Petrie S, Stranger R, Pace RJ (2012) Angew Chem Int Ed 51:12025–12028CrossRefGoogle Scholar
  123. 123.
    Petrie S, Gatt P, Stranger R, Pace RJ (2012) Phys Chem Chem Phys 14:11333–11343CrossRefGoogle Scholar
  124. 124.
    Siegbahn PEM (2013) Biochim Biophys Acta Bioenerg 1827:1003–1019CrossRefGoogle Scholar
  125. 125.
    Kusunoki M (2007) Biochim Biophys Acta Bioenerg 1767:484–492CrossRefGoogle Scholar
  126. 126.
    Sproviero EM, Gascon JA, McEvoy JP, Brudvig GW, Batista VS (2008) J Am Chem Soc 130:6728–6730CrossRefGoogle Scholar
  127. 127.
    Sproviero EM, Gascon JA, McEvoy JP, Brudvig GW, Batista VS (2008) J Am Chem Soc 130:3428–3442CrossRefGoogle Scholar
  128. 128.
    Kusunoki M (2011) Photochem Photobiol B 104:100–110CrossRefGoogle Scholar
  129. 129.
    Saito T, Yamanaka S, Kanda K, Isobe H, Takano Y, Shigeta Y, Umena Y, Kawakami K, Shen JR, Kamiya N, Okumura M, Shoji M, Yoshioka Y, Yamaguchi K (2012) Int J Quantum Chem 112:253–276CrossRefGoogle Scholar
  130. 130.
    Pantazis DA, Orio M, Petrenko T, Zein S, Lubitz W, Messinger J, Neese F (2009) Phys Chem Chem Phys 11:6788–6798CrossRefGoogle Scholar
  131. 131.
    Yamaguchi K, Isobe H, Yamanaka S, Saito T, Kanda K, Shoji M, Umena Y, Kawakami K, Shen JR, Kamiya N, Okumura M (2012) Int J Quantum Chem 113:525–541CrossRefGoogle Scholar
  132. 132.
    Bovi D, Narzi D, Guidoni L (2013) Angew Chem Int Ed 52:11744–11749CrossRefGoogle Scholar
  133. 133.
    Schinzel S, Schraut J, Arbuznikov AV, Siegbahn PEM, Kaupp M (2010) Chem Eur J 16:10424–10438CrossRefGoogle Scholar
  134. 134.
    Ames W, Pantazis DA, Krewald V, Cox N, Messinger J, Lubitz W, Neese F (2011) J Am Chem Soc 133:19743–19757CrossRefGoogle Scholar
  135. 135.
    Cox N, Rapatskiy L, Su J-H, Pantazis DA, Sugiura M, Kulik L, Dorlet P, Rutherford AW, Neese F, Boussac A, Lubitz W, Messinger J (2011) J Am Chem Soc 133:3635–3648CrossRefGoogle Scholar
  136. 136.
    Su J-H, Cox N, Ames W, Pantazis DA, Rapatskiy L, Lohmiller T, Kulik LV, Dorlet P, Rutherford AW, Neese F, Boussac A, Lubitz W, Messinger J (2011) Biochim Biophys Acta Bioenerg 1807:829–840CrossRefGoogle Scholar
  137. 137.
    Pantazis DA, Ames W, Cox N, Lubitz W, Neese F (2012) Angew Chem Int Ed 51:9935–9940CrossRefGoogle Scholar
  138. 138.
    Retegan M, Neese F, Pantazis DA (2013) J Chem Theory Comput 9:3832–3842CrossRefGoogle Scholar
  139. 139.
    Lohmiller T, Krewald V, Pérez Navarro M, Retegan M, Rapatskiy L, Nowaczyk MM, Boussac A, Neese F, Lubitz W, Pantazis DA, Cox N (2014) Phys Chem Chem Phys 16:11877–11892CrossRefGoogle Scholar
  140. 140.
    Retegan M, Cox N, Lubitz W, Neese F, Pantazis DA (2014) Phys Chem Chem Phys 16:11901–11910CrossRefGoogle Scholar
  141. 141.
    Zein S, Kulik LV, Yano J, Kern J, Pushkar Y, Zouni A, Yachandra VK, Lubitz W, Neese F, Messinger J (2008) Philos Trans R Soc B 363:1167–1177CrossRefGoogle Scholar
  142. 142.
    Orio M, Pantazis DA, Neese F (2009) Photosynth Res 102:443–453CrossRefGoogle Scholar
  143. 143.
    Pantazis DA, Orio M, Petrenko T, Zein S, Bill E, Lubitz W, Messinger J, Neese F (2009) Chem Eur J 15:5108–5123CrossRefGoogle Scholar
  144. 144.
    Neese F, Ames W, Christian G, Kampa M, Liakos DG, Pantazis DA, Roemelt M, Surawatanawong P, Ye SF (2010) Adv Inorg Chem 62:301–349CrossRefGoogle Scholar
  145. 145.
    Neese F (2009) Coord Chem Rev 253:526–563CrossRefGoogle Scholar
  146. 146.
    DeBeer George S, Petrenko T, Neese F (2008) J Phys Chem A 112:12936–12943CrossRefGoogle Scholar
  147. 147.
    Kusunoki M, Ono T, Noguchi T, Inoue Y, Oyanagi H (1993) Photosynth Res 38:331–339CrossRefGoogle Scholar
  148. 148.
    Messinger J, Robblee JH, Bergmann U, Fernandez C, Glatzel P, Visser H, Cinco RM, McFarlane KL, Bellacchio E, Pizarro SA, Cramer SP, Sauer K, Klein MP, Yachandra VK (2001) J Am Chem Soc 123:7804–7820CrossRefGoogle Scholar
  149. 149.
    Haumann M, Müller C, Liebisch P, Iuzzolino L, Dittmer J, Grabolle M, Neisius T, Meyer-Klaucke W, Dau H (2005) Biochemistry 44:1894–1908CrossRefGoogle Scholar
  150. 150.
    Peloquin JM, Campbell KA, Randall DW, Evanchik MA, Pecoraro VL, Armstrong WH, Britt RD (2000) J Am Chem Soc 122:10926–10942CrossRefGoogle Scholar
  151. 151.
    Peloquin JM, Britt RD (2001) Biochim Biophys Acta Bioenerg 1503:96–111CrossRefGoogle Scholar
  152. 152.
    Kulik L, Lubitz W (2009) Photosynth Res 102:391–401CrossRefGoogle Scholar
  153. 153.
    Hasegawa K, Ono T, Inoue Y, Kusunoki M (1999) Bull Chem Soc Jpn 72:1013–1023CrossRefGoogle Scholar
  154. 154.
    Hasegawa K, Ono T-A, Inoue Y, Kusunoki M (1999) Chem Phys Lett 300:9–19CrossRefGoogle Scholar
  155. 155.
    Barber J, Murray JW (2008) Philos Trans R Soc B 363:1129–1137CrossRefGoogle Scholar
  156. 156.
    Krewald V, Neese F, Pantazis DA (2013) J Am Chem Soc 135:5726–5739CrossRefGoogle Scholar
  157. 157.
    Isobe H, Shoji M, Yamanaka S, Umena Y, Kawakami K, Kamiya N, Shen JR, Yamaguchi K (2012) Dalton Trans 41:13727–13740CrossRefGoogle Scholar
  158. 158.
    Narzi D, Bovi D, Guidoni L (2014) Proc Natl Acad Sci U S A 111:8723–8728CrossRefGoogle Scholar
  159. 159.
    Ghanotakis DF, Babcock GT, Yocum CF (1984) FEBS Lett 167:127–130CrossRefGoogle Scholar
  160. 160.
    Boussac A, Rutherford AW (1988) Biochemistry 27:3476–3483CrossRefGoogle Scholar
  161. 161.
    Ishida N, Sugiura M, Rappaport F, Lai T-L, Rutherford AW, Boussac A (2008) J Biol Chem 283:13330–13340CrossRefGoogle Scholar
  162. 162.
    Boussac A, Rappaport F, Carrier P, Verbavatz J-M, Gobin R, Kirilovsky D, Rutherford AW, Sugiura M (2004) J Biol Chem 279:22809–22819CrossRefGoogle Scholar
  163. 163.
    Brudvig GW (2008) Philos Trans R Soc B 363:1211–1219CrossRefGoogle Scholar
  164. 164.
    Lee C-I, Lakshmi KV, Brudvig GW (2007) Biochemistry 46:3211–3223CrossRefGoogle Scholar
  165. 165.
    Vrettos JS, Limburg J, Brudvig GW (2001) Biochim Biophys Acta Bioenerg 1503:229–245CrossRefGoogle Scholar
  166. 166.
    McEvoy JP, Brudvig GW (2004) Phys Chem Chem Phys 6:4754–4763CrossRefGoogle Scholar
  167. 167.
    Vrettos JS, Stone DA, Brudvig GW (2001) Biochemistry 40:7937–7945CrossRefGoogle Scholar
  168. 168.
    Tsui EY, Agapie T (2013) Proc Natl Acad Sci U S A 110:10084–10088CrossRefGoogle Scholar
  169. 169.
    Tsui EY, Kanady JS, Agapie T (2013) Inorg Chem 52:13833–13848CrossRefGoogle Scholar
  170. 170.
    Siegbahn PEM (2014) Phys Chem Chem Phys 16:11893–11900CrossRefGoogle Scholar
  171. 171.
    Polander BC, Barry BA (2013) J Phys Chem Lett 786–791Google Scholar
  172. 172.
    Kawakami K, Umena Y, Kamiya N, Shen J-R (2009) Proc Natl Acad Sci U S A 106:8567–8572CrossRefGoogle Scholar
  173. 173.
    Siegbahn PEM (2009) Dalton Trans 10063–10068Google Scholar
  174. 174.
    Olesen K, Andréasson L-E (2003) Biochemistry 42:2025–2035CrossRefGoogle Scholar
  175. 175.
    Amin M, Vogt L, Szejgis W, Vassiliev S, Brudvig GW, Bruce D, Gunner MR (2015) J Phys Chem B 119:7366–7377CrossRefGoogle Scholar
  176. 176.
    Pokhrel R, McConnell IL, Brudvig GW (2011) Biochemistry 50:2725–2734CrossRefGoogle Scholar
  177. 177.
    Pokhrel R, Service RJ, Debus RJ, Brudvig GW (2013) Biochemistry 52:4758–4773CrossRefGoogle Scholar
  178. 178.
    van Vliet P, Rutherford AW (1996) Biochemistry 35:1829–1839CrossRefGoogle Scholar
  179. 179.
    Hillier W, Wydrzynski T (2004) Phys Chem Chem Phys 6:4882–4889CrossRefGoogle Scholar
  180. 180.
    Hendry G, Wydrzynski T (2003) Biochemistry 42:6209–6217CrossRefGoogle Scholar
  181. 181.
    Noguchi T (2008) Philos Trans R Soc B 363:1189–1195CrossRefGoogle Scholar
  182. 182.
    Noguchi T, Sugiura M (2002) Biochemistry 41:15706–15712CrossRefGoogle Scholar
  183. 183.
    Chu H-A, Sackett H, Babcock GT (2000) Biochemistry 39:14371–14376CrossRefGoogle Scholar
  184. 184.
    Rapatskiy L, Cox N, Savitsky A, Ames WM, Sander J, Nowaczyk MM, Rögner M, Boussac A, Neese F, Messinger J, Lubitz W (2012) J Am Chem Soc 134:16619–16634CrossRefGoogle Scholar
  185. 185.
    McConnell IL, Grigoryants VM, Scholes CP, Myers WK, Chen P-Y, Whittaker JW, Brudvig GW (2012) J Am Chem Soc 134:1504–1512CrossRefGoogle Scholar
  186. 186.
    Pokhrel R, Brudvig G (2014) Phys Chem Chem Phys 16:11812–11821CrossRefGoogle Scholar
  187. 187.
    Pérez Navarro M, Ames WM, Nilsson H, Lohmiller T, Pantazis DA, Rapatskiy L, Nowaczyk MM, Neese F, Boussac A, Messinger J, Lubitz W, Cox N (2013) Proc Natl Acad Sci U S A 110:15561–15566CrossRefGoogle Scholar
  188. 188.
    Schraut J, Kaupp M (2014) Chem Eur J 20:7300–7308CrossRefGoogle Scholar
  189. 189.
    Tagore R, Chen H, Crabtree RH, Brudvig GW (2006) J Am Chem Soc 128:9457–9465CrossRefGoogle Scholar
  190. 190.
    Siegbahn PEM (2013) J Am Chem Soc 135:9442–9449CrossRefGoogle Scholar
  191. 191.
    Yamaguchi K, Takahara Y, Fueno T (1986) Ab-initio molecular orbital studies of structure and reactivity of transition metal-oxo compounds. In: Smith VH Jr, Scheafer HF III, Morokuma K (eds) Applied quantum chemistry. Reidel, Boston, pp 155–184CrossRefGoogle Scholar
  192. 192.
    Pecoraro VL, Baldwin MJ, Caudle MT, Hsieh W-Y, Law NA (1998) Pure Appl Chem 70:925–929CrossRefGoogle Scholar
  193. 193.
    Barber J, Ferreira K, Maghlaoui K, Iwata S (2004) Phys Chem Chem Phys 6:4737–4742CrossRefGoogle Scholar
  194. 194.
    Yamaguchi K, Yamanaka S, Isobe H, Tanaka K, Ueyama N (2012) Int J Quantum Chem 112:3849–3866CrossRefGoogle Scholar
  195. 195.
    Siegbahn PEM, Crabtree RH (1999) J Am Chem Soc 121:117–127CrossRefGoogle Scholar
  196. 196.
    Siegbahn PEM (2006) Chem Eur J 12:9217–9227CrossRefGoogle Scholar
  197. 197.
    Shevela D, Koroidov S, Najafpour MM, Messinger J, Kurz P (2011) Chem Eur J 17:5415–5423CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Vera Krewald
    • 1
  • Marius Retegan
    • 1
  • Dimitrios A. Pantazis
    • 1
    Email author
  1. 1.Max Planck Institute for Chemical Energy ConversionMülheim an der RuhrGermany

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