Biochemistry (Moscow)

, Volume 79, Issue 3, pp 185–196 | Cite as

Photosystem II: Its function, structure, and implications for artificial photosynthesis

  • James BarberEmail author


Somewhere in the region of 3 billion years ago an enzyme emerged which would dramatically change the chemical composition of our planet and set in motion an unprecedented explosion in biological activity. This enzyme used solar energy to power the thermodynamically and chemically demanding reaction of water splitting. In so doing it provided biology with an unlimited supply of hydrogen equivalents needed to convert carbon dioxide into the organic molecules of life. The enzyme, which facilitates this reaction and therefore underpins virtually all life on our planet, is known as Photosystem II (PSII). It is a multisubunit enzyme embedded in the lipid environment of the thylakoid membranes of plants, algae, and cyanobacteria. Over the past 10 years, crystal structures of a 700 kDa cyanobacterial dimeric PSII complex have been reported with ever increasing improvement in resolution with the latest being at 1.9 details of its many subunits and cofactors are now well understood. The water splitting site was revealed as a cluster of four Mn ions and a Ca ion surrounded by amino acid side chains, of which seven provide ligands to the metals. The metal cluster is organized as a cubane-like structure composed of three Mn ions and the Ca2+ linked by oxo-bonds with the fourth Mn attached to the cubane via one of its bridging oxygens together with another oxo bridge to a Mn ion of the cubane. The overall structure of the catalytic site is providing a framework on which to develop a mechanistic scheme for the water splitting process and gives a blue print and confidence for the development of catalysts for mimicking the reaction in an artificial photo-electrochemical system to generate solar fuels.

Key words

photosynthesis photosystem II structure water splitting artificial photosynthesis manganese cluster oxygen evolving complex 











oxygen evolving complex






photosystem I(II)


reaction centre




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  1. 1.
    Barber, J. (2003) Biophys. Quart. Rev., 36, 71–89.CrossRefGoogle Scholar
  2. 2.
    De Las Rivas, J., Balsera, M., and Barber, J. (2004) Trends Plant Sci., 9, 18–25.PubMedCrossRefGoogle Scholar
  3. 3.
    Joliot, P., Barbieri, G., and Chabaud, R. (1969) Photochem. Photobiol., 10, 309–329.CrossRefGoogle Scholar
  4. 4.
    Kok, B., Forbush, B., and McGloin, M. (1970) Photochem. Photobiol., 11, 457–475.PubMedCrossRefGoogle Scholar
  5. 5.
    Zouni, A., Witt, H. T., Kern, J., Fromme, P., Krauss, N., Saenger, W., and Orth, P. (2001) Nature, 409, 739–743.PubMedCrossRefGoogle Scholar
  6. 6.
    Hankamer, B., Barber, J., and Boekema, E. J. (1997) Annu. Rev. Plant Phys. Mol. Biol., 48, 641–671.CrossRefGoogle Scholar
  7. 7.
    Rhee, K.-H., Morris, E. P., Zheleva, D., Hankamer, B., Kuhlbrandt, W., and Barber, J. (1997) Nature, 389, 522–526.CrossRefGoogle Scholar
  8. 8.
    Rhee, K.-H., Morris, E. P., Barber, J., and Kuhlbrandt, W. (1998) Nature, 396, 283–286.PubMedCrossRefGoogle Scholar
  9. 9.
    Hankamer, B., Morris, E. P., Nield, J., Gerle, C., and Barber, J. (2001) J. Struct. Biol., 135, 262–269.PubMedCrossRefGoogle Scholar
  10. 10.
    Hankamer, B., Morris, E. P., Nield, J., Carne, A., and Barber, J. (2001) FEBS Lett., 504, 142–151.PubMedCrossRefGoogle Scholar
  11. 11.
    Kamiya, N., and Shen, J. R. (2003) Proc. Natl. Acad. Sci. USA, 100, 98–103.PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J., and Iwata, S. (2004) Science, 303, 1831–1838.PubMedCrossRefGoogle Scholar
  13. 13.
    Kashino, Y., Takahashi, T., Inoue-Kashino, N., Ban, A., Yohei Ikeda, Y., Satoh, K., and Sugiura, M. (2007) Biochim. Biophys. Acta, 1767, 1269–1275.PubMedCrossRefGoogle Scholar
  14. 14.
    Umena, Y., Kawakami, K., Shen, J. R., and Kamiya, N. (2011) Nature, 473, 55–65.PubMedCrossRefGoogle Scholar
  15. 15.
    Loll, B., Kern, J., Saenger, W., Zouni, A., and Biesiadka, J. (2005) Nature, 438, 1040–1044.PubMedCrossRefGoogle Scholar
  16. 16.
    Guskov, A., Kern, J., Gabdulkhakov, A., Broser, M., Zouni, A., and Saenger, W. (2009) Nat. Struct. Mol. Biol., 16, 334–342.PubMedCrossRefGoogle Scholar
  17. 17.
    Barber, J. (1987) Trends Biochem. Sci., 12, 321–326.CrossRefGoogle Scholar
  18. 18.
    Michel, H., and Deisenhofer, J. (1988) Biochemistry, 27, 1–7.CrossRefGoogle Scholar
  19. 19.
    Schubert, W. D., Klukas, O., Saenger, W., Witt, H. T., Fromme, P., and Krauss, N. (1998) J. Mol. Biol., 280, 297–341.PubMedCrossRefGoogle Scholar
  20. 20.
    Murray, J. W., Duncan, J., and Barber, J. (2006) Trends Plant Sci., 11, 152–158.PubMedCrossRefGoogle Scholar
  21. 21.
    Durrant, J. R., Klug, D. R., Kwa, S. L. S., van Grondelle, R. V., Porter, G., and Klug, D. R. (1995) Proc. Natl. Acad. Sci. USA, 92, 4798–4802.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Holzwarth, A. R., Muller, M. G., Rees, M., Nowaczyk, M., Sander, J., and Rogner, M. (2006) Proc. Natl. Acad. Sci. USA, 103, 6895–6900.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Barber, J., and Archer, M. D. (2001) J. Photochem. Photobiol., A142, 97–106.CrossRefGoogle Scholar
  24. 24.
    Murray, J. W., and Barber, J. (2007) J. Struct. Biol., 159, 228–237.PubMedCrossRefGoogle Scholar
  25. 25.
    Faller, P., Debus, R. J., Brettel, K., Sugiura, M., Rutherford, A. W., and Boussac, A. (2001) Proc. Natl. Acad. Sci. USA, 98, 14368–14373.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Rutherford, A. W. (1989) Trends Biochem. Sci., 14, 227–232.PubMedCrossRefGoogle Scholar
  27. 27.
    Hienerwadel, R., and Berthomieu, C. (1995) Biochemistry, 34, 16288–16297.PubMedCrossRefGoogle Scholar
  28. 28.
    Hasegawa, K., Ono, T. A., Inoue, Y., and Kusunoki, M. (1999) Chem. Phys. Lett., 300, 9–19.CrossRefGoogle Scholar
  29. 29.
    Govindjee and van Rensen, J. J. S. (1993) in The Photosynthetic Reaction Center (Deisenhofer, J. B., and Norris, J., eds.) Academic Press, San Diego, pp. 357–389.Google Scholar
  30. 30.
    Barber, J., and Andersson, B. (1992) Trends Biochem. Sci., 17, 61–66.PubMedCrossRefGoogle Scholar
  31. 31.
    Arnon, D. I., and Whatley, F. R. (1949) Science, 110, 554–556.PubMedCrossRefGoogle Scholar
  32. 32.
    Bove, J. M., Bove, C., Whatley, F. R., and Arnon, D. I. (1963) Z. Naturforsch., 18b, 683–688.Google Scholar
  33. 33.
    Izawa, S., Heath, R. L., and Hind, G. (1969) Biochim. Biophys. Acta, 180, 388–389.PubMedCrossRefGoogle Scholar
  34. 34.
    Van Gorkom, H. J., and Yochum, C. F. (2005) in Photosystem II. The Light-Driven Water Plastoquinone Oxidoreductase (Wydrzynski, T. J., and Satoh, K., eds.) Springer, Dordrecht, pp. 307–327.Google Scholar
  35. 35.
    Wincencjusz, H., van Gorkom, H. J., and Yocum, C. F. (1997) Biochemistry, 36, 3663–3670.PubMedCrossRefGoogle Scholar
  36. 36.
    Boussac, A., Setif, P., and Rutherford, A. W. (1992) Biochemistry, 31, 1224–1234.PubMedCrossRefGoogle Scholar
  37. 37.
    Ono, T.-A., Noguchi, T., Inoue, Y., Kusunoki, M., Yamaguchi, H., and Oyanagi, H. (1995) J. Am. Chem. Soc., 117, 6386–6387.CrossRefGoogle Scholar
  38. 38.
    Murray, J. W., Maghlaoui, K., Kargul, J., Ishida, N., Lai, T.-L., Rutherford, A. W., Sugiura, M., Boussac, A., and Barber, J. (2008) Energy Environ. Sci., 1, 161–166.CrossRefGoogle Scholar
  39. 39.
    Kawakami, K., Umena, Y., Kamiya, N., and Shen, J.-R. (2009) Proc. Natl. Acad. Sci. USA, 106, 8567–8572.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Rivalta, I., Amin, M., Luber, S., Vassiliev, S., Pokhrel, R., Umena, Y., Kawakami, K., Shen, J.-R., Kamiya, N., Bruce, D., Brudvig, G. W., Gunner, M. R., and Batista, V. S. (2011) Biochemistry, 50, 6312–6315.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Peloquin, J. M., Campbell, K. A., Randall, D. W., Evanchik, M. A., Pecoraro, V. L., Armstrong, W. H., and Britt, R. D. (2000) J. Am. Chem. Soc., 122, 10926–10942.CrossRefGoogle Scholar
  42. 42.
    Hasegawa, K., Ono, T. A., Inoue, Y., and Kusunoki, M. (1999) Chem. Phys. Lett., 300, 9–19.CrossRefGoogle Scholar
  43. 43.
    Diner, B. A. (2001) Biochim. Biophys. Acta, 1503, 147–163.PubMedCrossRefGoogle Scholar
  44. 44.
    Debus, R. J. (2001) Biochim. Biophys. Acta, 1503, 164–186.PubMedCrossRefGoogle Scholar
  45. 45.
    Debus, R. J. (2008) Chem. Rev., 252, 244–258.Google Scholar
  46. 46.
    Diner, B. A., Nixon, P. J., and Farchaus, J. W. (1991) Curr. Opin. Struct. Biol., 1, 546–554.CrossRefGoogle Scholar
  47. 47.
    Yachandra, V. K. (2002) Phil. Trans. Roy. Soc. Lond. B, 357, 1347–1358.CrossRefGoogle Scholar
  48. 48.
    Lundberg, M., and Siegbahn, P. E. M. (2004) Phys. Chem. Chem. Phys., 6, 4772–4780.CrossRefGoogle Scholar
  49. 49.
    Sproviero, E. M., Gascon, J. A., McEvoy, J. P., Brudvig, G. W., and Batista, V. S. (2006) J. Chem. Theory Comput., 2, 1119–1134.CrossRefGoogle Scholar
  50. 50.
    Sproviero, E. M., Gascon, J. A., McEvoy, J. P., Brudvig, G. W., and Batista, V. S. (2007) Curr. Opin. Struct. Biol., 17, 173–180.PubMedCrossRefGoogle Scholar
  51. 51.
    Batista, V. S., Sproviero, E. M., Gascon, J. A., McEvoy, J. P., and Brudvig, G. W. (2008) Coord. Chem. Rev., 252, 395–415.PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    Mishra, A., Wernsdorfer, W., Abboud, K. A., and Christou, G. (2005) Chem. Commun., No. 1, 54–56.Google Scholar
  53. 53.
    Kanady, S., Tsui, E., Day, M., and Agapie, T. (2011) Science, 333, 733–736.PubMedCrossRefGoogle Scholar
  54. 54.
    Mukherjee, S., Stull, J. A., Yano, J., Stamatatos, T., Pringouri, K., Stich, T. A., Abboud, K. A., Britt, R. D., Yachandra, V. K., and Christou, G. (2012) Proc. Natl. Acad. Sci. USA, 109, 2257–2262.PubMedCrossRefPubMedCentralGoogle Scholar
  55. 55.
    McEvoy, J. P., and Brudvig, G. W. (2004) Phys. Chem. Chem. Phys., 6, 4754–4763.CrossRefGoogle Scholar
  56. 56.
    McEvoy, J. P., and Brudvig, G. W. (2006) Chem. Rev., 106, 4455–4483.PubMedCrossRefGoogle Scholar
  57. 57.
    Brudvig, G. W. (2008) Philos. Trans. R. Soc. Lond. B, 363, 1211–1218.CrossRefGoogle Scholar
  58. 58.
    Dau, H., Grundmeier, A., Loja, P., and Haumann, M. (2008) Philos. Trans. R. Soc. Lond. B, 363, 1237–1243.CrossRefGoogle Scholar
  59. 59.
    Siegbahn, P. E. M. (2006) Chemistry — A European Journal, 12, 9217–9237.CrossRefGoogle Scholar
  60. 60.
    Siegbahn, P. E. M. (2008) Chemistry, 14, 8290–8302.PubMedCrossRefGoogle Scholar
  61. 61.
    Siegbahn, P. E. M. (2009) Acc. Chem. Res., 42, 1871–1880.PubMedCrossRefGoogle Scholar
  62. 62.
    Siegbahn, P. E. M. (2012) Phys. Chem. Chem. Phys., 14, 4849–4856.PubMedCrossRefGoogle Scholar
  63. 63.
    Hoganson, C. W., and Babcock, G. T. (1997) Science, 277, 1953–1956.PubMedCrossRefGoogle Scholar
  64. 64.
    Kargul, J., Maghlaoui, K., Murray, J. W., Deak, Z., Boussac, A., Rutherford, A. W., Vass, I., and Barber, J. (2007) Biochim. Biophys. Acta, 1767, 404–413.PubMedCrossRefGoogle Scholar
  65. 65.
    Yano, J., Kern, J., Irrgang, K.-D., Latimer, M. J., Bergmann, U., Glatzel, P., Pushkar, Y., Biesiadka, J., Loll, B., Sauer, K., Messinger, J., Zouni, A., and Yachandra, V. K. (2005) Proc. Natl. Acad. Sci. USA, 102, 12047–12052.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Grabolle, M., Haumann, M., Muller, C., Liebisch, P., and Dau, H. (2006) J. Biol. Chem., 281, 4580–4588.PubMedCrossRefGoogle Scholar
  67. 67.
    Yano, J., Kern, J., Sauer, K., Latimer, M. J., Pushkar, Y., Biesiadka, J., Loll, B., Saenger, W., Messinger, J., Zouni, A., and Yachandra, V. K. (2006) Science, 314, 821–825.PubMedCrossRefGoogle Scholar
  68. 68.
    Sproviero, E. M., Gascon, J. A., McEvoy, J. P., Brudvig, G. W., and Batista, V. S. (2008) J. Am. Chem. Soc., 130, 3428–3442.PubMedCrossRefGoogle Scholar
  69. 69.
    Hwang, H. J., Dilbeck, P., Debus, R. J., and Burnap, R. L. (2007) Biochemistry, 46, 11987–11997.PubMedCrossRefGoogle Scholar
  70. 70.
    Service, R. J., Hillier, W., and Debus, R. J. (2010) Biochemistry, 49, 6655–6669.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Luber, S., Rivalta, I., Umena, Y., Kawakami, K., Shen, J.-R., Kamiya, N., Brudvig, G. W., and Batista, V. S. (2011) Biochemistry, 50, 6308–6311.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Messinger, J., Badger, M., and Wydrynski, T. (1995) Proc. Natl. Acad. Sci. USA, 92, 3209–3213.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Pecoraro, V. L., Baldwin, M. J., Caudle, M. T., Hsieh, W.-Y., and Law, N. A. (1998) Pure Appl. Chem., 70, 925–929.CrossRefGoogle Scholar
  74. 74.
    Limberg, J., Vrettos, J. S., Liable-Sands, L. M., Rheingold, A. L., Crabtree, R. H., and Brudvig, G. W. (1999) Science, 283, 1524–1527.CrossRefGoogle Scholar
  75. 75.
    Cox, N., Rapatskiy, L., Su, J.-H., Pantazis, D. A., Sugiura, M., Kulik, L., Dorlet, P., Rutherford, A. W., Neese, F., Boussac, A., Lubitz, W., and Messinger, J. (2011) J. Am. Chem. Soc., 133, 3635–3648.PubMedCrossRefGoogle Scholar
  76. 76.
    Tran, P. D., Wong, L. H., Barber, J., and Loo, J. S. C. (2012) Energy Environ. Sci., 5, 5902–5918.CrossRefGoogle Scholar
  77. 77.
    Eisenberg, E., and Gray, H. B. (2008) Inorg. Chem., 47, 1697–1699.PubMedCrossRefGoogle Scholar
  78. 78.
    Tagore, R., Crabtree, R. H., and Brudvig, G. W. (2008) Inorg. Chem., 47, 1815–1823.PubMedCrossRefGoogle Scholar
  79. 79.
    Gao, Y., Crabtree, R. H., and Brudvig, G. W. (2012) Inorg. Chem., 51, 4043–4050.PubMedCrossRefGoogle Scholar
  80. 80.
    Najafpour, M. M., Ehrenberg, T., Wiechen, M., and Kurz, P. (2010) Angewandte Chemie, 49, 2233–2237.PubMedCrossRefGoogle Scholar
  81. 81.
    Zaharieva, I., Najafpour, M. M., Wiechert, M., Haumann, M., Kurz, P., and Dau, H. (2011) Energy Environ. Sci., 4, 2400–2408.CrossRefGoogle Scholar
  82. 82.
    Jiao, F., and Frei, H. (2010) Chem. Commun., 46, 2920–2922.CrossRefGoogle Scholar
  83. 83.
    Gersten, S. W., Samuels, G. J., and Meyer, T. J. (1982) J. Am. Chem. Soc., 104, 4029–4030.CrossRefGoogle Scholar
  84. 84.
    Liu, F., Concepcion, J. J., Jurss, J. W., Cardolaccia, T., Templeton, J. L., and Meyer, T. J. (2008) Inorg. Chem., 47, 1727–1752.PubMedCrossRefGoogle Scholar
  85. 85.
    Romero, I., Rodriguez, M., Sens, C., Mola, J., Kollipara, M. R., Francas, L., Mas-Marza, E., Escriche, L., and Llobet, A. (2008) Inorg. Chem., 47, 1824–1834.PubMedCrossRefGoogle Scholar
  86. 86.
    Duan, L., Bogoglian, F., Mandal, S., Stewart, B., Privalot, T., Llobet, A., and Sun, L.-C. (2012) Nature Chemistry, 4, 418–423.PubMedCrossRefGoogle Scholar
  87. 87.
    Kanan, M. W., and Nocera, D. G. (2008) Science, 321, 1072–1075.PubMedCrossRefGoogle Scholar
  88. 88.
    Risch, M., Khare, V., Zaharieva, I., Gerencser, L., Chernev, P., and Dau, H. (2009) J. Am. Chem. Soc., 131, 6936–6937.PubMedCrossRefGoogle Scholar
  89. 89.
    Yin, Q., Tan, J. M., Besson, C., Geletii, Y. V., Musaev, D. G., Kuznetsov, A. E., Luo, Z., Hardcastle, K. I., and Hill, C. L. (2010) Science, 328, 342–345.PubMedCrossRefGoogle Scholar
  90. 90.
    Sivula, K., Le Formal, F., and Graetzel, M. (2011) ChemSusChem., 4, 432–449.PubMedCrossRefGoogle Scholar
  91. 91.
    Murphy, A. B., Barnes, P. R. F., Randeniya, L. K., Plumb, I. C., Grey, I. E., Horne, M. D., and Glasscock, J. A. (2006) Int. J. Hydrogen Energy, 31, 1999–2017.CrossRefGoogle Scholar
  92. 92.
    Wang, M., Chen, L., and Sun, L. (2012) Energy Environ. Sci., 5, 6763–6778.CrossRefGoogle Scholar
  93. 93.
    Tran, P. D., Artero, V., and Fontecave, M. (2010) Energy Environ. Sci., 3, 727–747.CrossRefGoogle Scholar
  94. 94.
    Zong, X., Han, J., Ma, G., Yan, H., Wu, G., and Li, C. (2011) J. Phys. Chem. C, 115, 12202–12208.CrossRefGoogle Scholar
  95. 95.
    Merki, D., and Hu, X. (2011) Energy Environ. Sci., 4, 3878–3888.CrossRefGoogle Scholar
  96. 96.
    Reece, S. Y., Hamel, J. A., Sung, K., Jarvi, T. D., Esswein, A. J., Pijpers, J. J. H., and Nocera, D. G. (2011) Science, 334, 645–648.PubMedCrossRefGoogle Scholar
  97. 97.
    Fujita, E. (2000) in McGraw-Hill Yearbook of Science & Technology (Licker, M. D., ed.) McGraw-Hill Book Co, New York, pp. 71–74.Google Scholar
  98. 98.
    Arakawa, H., Aresta, M., Armor, J. N., Barteau, M. A., Beckman, E. J., and Bell, A. T. (2001) Chem. Rev., 101, 953–996.PubMedCrossRefGoogle Scholar

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© Pleiades Publishing, Ltd. 2014

Authors and Affiliations

  1. 1.Department of Life SciencesImperial College LondonLondonUK

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