Skip to main content
Log in

Structure-function investigations of bacterial photosynthetic reaction centers

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

During photosynthesis light energy is converted into energy of chemical bonds through a series of electron and proton transfer reactions. Over the first ultrafast steps of photosynthesis that take place in the reaction center (RC) the quantum efficiency of the light energy transduction is nearly 100%. Compared to the plant and cyanobacterial photosystems, bacterial RCs are well studied and have relatively simple structure. Therefore they represent a useful model system both for manipulating of the electron transfer parameters to study detailed mechanisms of its separate steps as well as to investigate the common principles of the photosynthetic RC structure, function, and evolution. This review is focused on the research papers devoted to chemical and genetic modifications of the RCs of purple bacteria in order to study principles and mechanisms of their functioning. Investigations of the last two decades show that the maximal rates of the electron transfer reactions in the RC depend on a number of parameters. Chemical structure of the cofactors, distances between them, their relative orientation, and interactions to each other are of great importance for this process. By means of genetic and spectral methods, it was demonstrated that RC protein is also an essential factor affecting the efficiency of the photochemical charge separation. Finally, some of conservative water molecules found in RC not only contribute to stability of the protein structure, but are directly involved in the functioning of the complex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

(B)Pheo:

(bacterio)pheophytin

(B)Chl:

(bacterio)chlorophyll

BA and BB :

monomeric BChl of A or B branch of electron transfer cofactors

β :

BChl molecule in BPheo binding site

cyt:

cytochrome

D:

BChl/BPheo heterodimer

Em P/P+ :

primary electron donor redox potential

EPR:

electron paramagnetic resonance

Φ :

BPheo molecule in monomeric BChl binding site

HA and HB :

BPheo of A or B branch of electron transfer cofactors

LH-1 and LH-2:

light-harvesting complexes of core and peripheral antenna

P:

BChl homodimer, primary electron donor, special pair

PA and PB :

BChl molecules forming primary electron donor

PGC:

photosynthetic gene cluster

PS:

photosystem

QA and QB :

primary and secondary quinone electron acceptors

RC:

reaction center

Blc. :

Blastochloris

Rba. :

Rhodobacter

Rsb. :

Roseobacter

Rsp. :

Rhodospirillum

Rvi. :

Rubrivivax.

References

  1. Yakovlev, A. G., Shkuropatov, A. Ya., and Shuvalov, V. A. (2002) Biochemistry, 41, 2667–2674.

    Article  PubMed  CAS  Google Scholar 

  2. Parson, W. W. (2007) Science, 316, 1438–1439.

    Article  PubMed  CAS  Google Scholar 

  3. Wang, H., Lin, S., Allen, J. P., Williams, J. C., Blankert, S., Laser, C., and Woodbury, N. W. (2007) Science, 316, 747–750.

    Article  PubMed  CAS  Google Scholar 

  4. Wakeham, M. C., and Jones, M. R. (2005) Biochem. Soc. Trans., 33, 851–857.

    Article  PubMed  CAS  Google Scholar 

  5. Jones, M. R. (2007) Progr. Lipid Res., 46, 56–87.

    Article  CAS  Google Scholar 

  6. Allen, J. P., and Williams, J. C. (2011) Photosynth. Res., 107, 59–69.

    Article  PubMed  CAS  Google Scholar 

  7. Deisenhofer, J., Epp, O., Miki, K., Huber, R., and Michel, H. (1984) J. Mol. Biol., 180, 385–398.

    Article  PubMed  CAS  Google Scholar 

  8. Deisenhofer, J., Epp, K., Miki, K., Huber, R., and Michel, H. (1985) Nature, 318, 618–624.

    Article  Google Scholar 

  9. Allen, J. P., Feher, G., Yeates, T. O., Rees, D. C., Deisenhofer, J., Michel, H., and Huber, R. (1986) PNAS USA, 83, 8589–8593.

    Article  PubMed  CAS  Google Scholar 

  10. Allen, J. P., Feher, G., Yeates, T. O., Komiya, H., and Rees, D. S. (1987) PNAS USA, 84, 5730–5734.

    Article  PubMed  CAS  Google Scholar 

  11. Nogi, T., Fathir, I., Kobayashi, M., Nozawa, T., and Miki, K. (2000) PNAS USA, 97, 13561–13566.

    Article  PubMed  CAS  Google Scholar 

  12. Camara-Artigas, A., Brune, D., and Allen, J. P. (2002) PNAS USA, 99, 11055–11060.

    Article  PubMed  CAS  Google Scholar 

  13. Deisenhofer, J., and Michel, H. (1989) EMBO J., 8, 2149–2170.

    PubMed  CAS  Google Scholar 

  14. Allen, J. P., Feher, G., Yeates, T. O., Komiya, H., and Rees, D. C. (1988) PNAS USA, 85, 8487–8491.

    Article  PubMed  CAS  Google Scholar 

  15. Feher, G., Allen, J. P., Okamura, M. Y., and Rees, D. C. (1989) Nature, 339, 111–116.

    Article  CAS  Google Scholar 

  16. Norris, J. R., Uphaus, R. A., Crespi, H. L., and Katz, J. J. (1971) PNAS USA, 68, 625–628.

    Article  PubMed  CAS  Google Scholar 

  17. Norris, J. R., Scheer, H., and Katz, J. J. (1975) Ann. NY Acad. Sci. USA, 244, 260–280.

    Article  CAS  Google Scholar 

  18. Feher, G., Hoff, A. J., Isaacson, R. A., and Ackerson, L. C. (1975) Ann. NY Acad. Sci. USA, 244, 239–259.

    Article  CAS  Google Scholar 

  19. Ermler, U., Fritzsch, G., Buchanan, S. K., and Michel, H. (1994) Structure, 2, 925–936.

    Article  PubMed  CAS  Google Scholar 

  20. Fritzsch, G., Kampmann, L., Kapaun, G., and Michel, H. (1998) Photosynth. Res., 55, 127–132.

    Article  CAS  Google Scholar 

  21. Potter, J. A., Fyfe, P. K., Frolov, D., Wakeham, M. C., van Grondelle, R., Robert, B., and Jones, M. R. (2005) J. Biol. Chem., 280, 27155–27164.

    Article  PubMed  CAS  Google Scholar 

  22. Yakovlev, A. G., Jones, M. R., Potter, J. A., Fyfe, P. K., Vasilieva, L. G., Shkuropatov, A. Ya., and Shuvalov, V. A. (2005) Chem. Phys., 319, 297–307.

    Article  CAS  Google Scholar 

  23. Zinth, W., Sander, M., Dobler, J., Kaiser, W., and Michel, H. (1985) in Antennas and Reaction Centers in Photosynthetic Bacteria (Michel-Beyerle, M.-E., ed.) Springer-Verlag, Berlin-New York, pp. 97–102.

    Google Scholar 

  24. Parson, W. W. (1991) in Chlorophylls (Scheer, H., ed.) CRC Press, Boca Raton, pp. 1153–1180.

    Google Scholar 

  25. Breton, J. (1988) The Photosynthetic Bacterial Reaction Center: Structure and Dynamics (Breton, J., and Vermeglio, A., eds.) Plenum Press, New York, pp. 59–69.

    Google Scholar 

  26. Breton, J., Bylina, E. J., and Youvan, D. C. (1989) Biochemistry, 28, 6423–6430.

    Article  CAS  Google Scholar 

  27. Kirmaier, C., and Holten, D. (1987) Photosynth. Res., 13, 225–260.

    Article  CAS  Google Scholar 

  28. Bylina, E. J., Kirmaier, C., McDowell, L., Holten, D., and Youvan, D. C. (1988) Nature, 336, 182–184.

    Article  CAS  Google Scholar 

  29. Wang, H., Lin, S., and Woodbury, N. W. (2006) J. Phys. Chem. B, 110, 6956–6961.

    Article  PubMed  CAS  Google Scholar 

  30. Kennis, J. T., Shkuropatov, A. Y., van Stokkum, I. H. M., Gast, P., Hoff, A. J., Shuvalov, V. A., and Aartsma, T. J. (1997) Biochemistry, 36, 16231–16238.

    Article  PubMed  CAS  Google Scholar 

  31. Vos, M. H., Jones, M. R., McGlynn, P., Hunter, C. N., Breton, J., and Martin, J. L. (1994) Biochim. Biophys. Acta, 1186, 117–122.

    Article  CAS  Google Scholar 

  32. Yakovlev, A. G., Shkuropatov, A. Y., and Shuvalov, V. A. (2000) FEBS Lett., 466, 209–212.

    Article  PubMed  CAS  Google Scholar 

  33. Yakovlev, A. G., Vasilieva, L. G., Shkuropatov, A. Ya., Bolgarina, T. I., Shkuropatova, V. A., and Shuvalov, V. A. (2003) J. Phys. Chem. A, 107, 8330–8338.

    Article  CAS  Google Scholar 

  34. Shuvalov, V. A., and Parson, W. W. (1981) PNAS USA, 78, 957–961.

    Article  PubMed  CAS  Google Scholar 

  35. Arlt, T., Schmidt, S., Kaiser, W., Lauterwasser, C., Meyer, M., Scheer, H., and Zinth, W. (1993) PNAS USA, 90, 11757–11761.

    Article  PubMed  CAS  Google Scholar 

  36. Schmidt, S., Arlt, T., Hamm, P., Huber, H., Nagele, T., Wachtveitl, J., Meyer, M., Scheer, H., and Zinth, W. (1994) Chem. Phys. Lett., 223, 116–120.

    Article  CAS  Google Scholar 

  37. Schmidt, S., Arlt, T., Hamm, P., Huber, H., Nagele, T., Wachtveitl, J., Zinth, W., Meyer, M., and Scheer, H. (1995) Spectrochim. Acta A, 51, 1565–1578.

    Article  Google Scholar 

  38. Gunner, M. R. (1991) Curr. Top. Bioenerg., 16, 319–367.

    CAS  Google Scholar 

  39. Arata, H., and Parson, W. W. (1981) Biochim. Biophys. Acta, 638, 201–209.

    Article  CAS  Google Scholar 

  40. Shuvalov, V. A. (1990) Primary Transformation of Light Energy in Photosynthesis [in Russian], Nauka, Moscow.

    Google Scholar 

  41. Du, M., Rosenthal, S. J., Xie, X., DiMagno, T. J., Schmidt, M., Hanson, D. K., Schiffer, M., Norris, J. R., and Fleming, G. R. (1992) PNAS USA, 89, 8517–8521.

    Article  PubMed  CAS  Google Scholar 

  42. Lancaster, C. R. D., and Michel, H. (2001) Handbook of Metalloproteins, Vol. 1 (Messerschmidt, A., Huber, R., Poulos, T., and Wieghardt, K., eds.) John Wiley & Sons, Ltd, Chichester, pp. 119–135.

    Google Scholar 

  43. Parson, W. W., and Warshel, A. (2009) The Purple Phototrophic Bacteria, Vol. 28 (Hunter, C. N., Daldal, F., Thurnauer, M. C., and Beatty, J. T., eds.) Springer, Dordrecht, The Netherlands, pp. 337–353.

    Google Scholar 

  44. Shuvalov, V. A. (2000) Transformation of Solar Energy during Primary Charge Separation Act in Photosynthesis Reaction Center [in Russian], Nauka, Moscow.

    Google Scholar 

  45. Axelrod, H., Miyashita, O., and Okamura, M. (2009) in The Purple Phototrophic Bacteria, Vol. 28 (Hunter, C. N., Daldal, F., Thurnauer, M. C., and Beatty, J. T., eds.) Springer, Dordrecht, The Netherlands, pp. 323–336.

    Chapter  Google Scholar 

  46. Okamura, M. Y., Isaacson, R. A., and Feher, G. (1975) PNAS USA, 72, 3491–3495.

    Article  PubMed  CAS  Google Scholar 

  47. Gunner, M. R., and Dutton, P. L. (1989) J. Am. Chem. Soc., 111, 3400–3412.

    Article  CAS  Google Scholar 

  48. Woodbury, N. W., Parson, W. W., Gunner, M. R., Prince, R. C., and Dutton, P. L. (1986) Biochim. Biophys. Acta, 851, 6–22.

    Article  PubMed  CAS  Google Scholar 

  49. Allen, J. P., Williams, J. C., Graige, M. S., Paddock, M. L., Labahn, A., Feher, G., and Okamura, M. Y. (1998) Photosynth. Res., 55, 227–233.

    Article  CAS  Google Scholar 

  50. Paddock, M. L., Graige, M. S., Feher, G., and Okamura, M. Y. (1999) PNAS USA, 96, 6183–6188.

    Article  PubMed  CAS  Google Scholar 

  51. Li, J. L., Takahashi, E., and Gunner, M. R. (2000) Biochemistry, 39, 7445–7454.

    Article  PubMed  CAS  Google Scholar 

  52. Okamura, M. Y., Paddock, M. L., Graige, M. S., and Feher, G. (2000) Biochim. Biophys. Acta. Bioenerg., 1458, 148–163.

    Article  CAS  Google Scholar 

  53. Schmid, R., and Labahn, A. (2000) Phys. Chem. B, 104, 2928–2936.

    Article  CAS  Google Scholar 

  54. Jones, M. R. (2009) The Purple Phototrophic Bacteria, Vol. 28 (Hunter, C. N., Daldal, F., Thurnauer, M. C., and Beatty, J. T., eds.) Springer, Dordrecht, The Netherlands, pp. 295–321.

    Chapter  Google Scholar 

  55. Scheer, H., and Hartwich, G. (1995) Anoxygenic Photosynthetic Bacteria, Vol. 2 (Blankenship, R. E., Madigan, M. T., and Bauer, C., eds.) Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 649–663.

    Google Scholar 

  56. Scheer, H., and Struck, A. (1993) The Photosynthetic Reaction Center, Vol. 1 (Deisenhofer, J., and Norris, J. R., eds.) Academic Press, San Diego, USA, pp. 157–192.

    Google Scholar 

  57. Struck, A., and Scheer, H. (1990) FEBS Lett., 261, 385–388.

    Article  CAS  Google Scholar 

  58. Shkuropatov, A. Y., and Shuvalov, V. A. (1993) FEBS Lett., 322, 168–172.

    Article  PubMed  CAS  Google Scholar 

  59. Meyer, M., and Scheer, H. (1995) Photosynth. Res., 44, 55–65.

    Article  CAS  Google Scholar 

  60. Franken, E. M., Shkuropatov, A. Y., Francke, C., Neerken, S., Gast, P., Shuvalov, V. A., Hoff, A. J., and Aartsma, T. J. (1997) Biochim. Biophys. Acta, 1319, 242–250.

    Article  CAS  Google Scholar 

  61. Franken, E. M., Shkuropatov, A. Y., Francke, C., Neerken, S., Gast, P., Shuvalov, V. A., Hoff, A. J., and Aartsma, T. J. (1997) Biochim. Biophys. Acta, 1321, 1–9.

    Article  CAS  Google Scholar 

  62. Storch, K. F., Cmiel, E., Schafer, W., and Scheer, H. (1996) Eur. J. Biochem., 238, 280–286.

    Article  PubMed  CAS  Google Scholar 

  63. Shkuropatov, A. Ya., Proskuryakov, I. I., Shkuropatova, V. A., Zvereva, M. G., and Shuvalov, V. A. (1994) FEBS Lett., 351, 249–252.

    Article  CAS  Google Scholar 

  64. Hartwich, G., Friese, M., Scheer, H., Ogrodnik, A., and Michel-Beyerle, M. E. (1995) Chem. Phys., 197, 423–434.

    Article  CAS  Google Scholar 

  65. Hartwich, G., Scheer, H., Aust, V., and Angerhofer, A. (1995) Biochim. Biophys. Acta Bioenerg., 1230, 97–113.

    Article  Google Scholar 

  66. Finkele, U., Lauterwasser, C., Struck, A., Scheer, H., and Zinth, W. (1992) PNAS USA, 89, 9514–9518.

    Article  PubMed  CAS  Google Scholar 

  67. Sporlein, S., Zinth, W., Meyer, M., Scheer, H., and Wachtveitl, J. (2000) Chem. Phys. Lett., 322, 454–464.

    Article  CAS  Google Scholar 

  68. Frank, H. A., Chynwat, V., Hartwich, G., Meyer, M., Katheder, I., and Scheer, H. (1993) Photosynth. Res., 37, 193–203.

    Article  CAS  Google Scholar 

  69. Frank, H. A., Chynwat, V., Posteraro, A., Hartwich, G., Simonin, I., and Scheer, H. (1996) Photochem. Photobiol., 64, 823–831.

    Article  PubMed  CAS  Google Scholar 

  70. Huber, H., Meyer, M., Scheer, H., Zinth, W., and Wachtveitl, J. (1998) Photosynth. Res., 55, 153–162.

    Article  CAS  Google Scholar 

  71. Shkuropatov, A. Y., Neerken, S., Permentier, H. P., de Wijn, R., Schmidt, K. A., Shuvalov, V. A., Aartsma, T. S. J., Gast, P., and Hoff, A. J. (2003) Biochim. Biophys. Acta Bioenerg., 1557, 1–12.

    Article  CAS  Google Scholar 

  72. Shuvalov, V. A., and Yakovlev, A. G. (1998) Membr. Cell Biol., 12, 563–569.

    PubMed  CAS  Google Scholar 

  73. Nowak, F. R., Kennis, J. T. M., Franken, E. M., Shkurupatov, A. Ya., Yakovlev, A. G., Gast, P., Hoff, A. J., Aartsma, T. J., and Shuvalov, V. A. (1998) Photosynthesis: Mechanisms and Effects, Vol. 2 (Garab, G., ed.) Kluwer Academic Publishers, The Netherlands, pp. 783–786.

    Google Scholar 

  74. Kobayashi, M., Takaya, A., Kanai, N., Ota, Y., Saito, T., Wang, Z.-Y., and Nozawa, T. (2004) J. Biochem., 136, 363–369.

    Article  PubMed  CAS  Google Scholar 

  75. Chadwick, B. W., and Frank, H. A. (1986) Biochim. Biophys. Acta, 851, 257–266.

    Article  CAS  Google Scholar 

  76. Frank, H. A., Chadwick, B. W., Taremi, S., Kolaczkowski, S., and Bowman, M. K. (1986) FEBS Lett., 203, 157–163.

    Article  CAS  Google Scholar 

  77. Farhoosh, R., Chynwat, V., Gebhard, R., Lugtenburg, J., and Frank, H. A. (1997) Photochem. Photobiol., 66, 97–104.

    Article  PubMed  CAS  Google Scholar 

  78. Yanagi, K., Shimizu, M., Hashimoto, H., Gardiner, A. T., Roszak, A. W., and Cogdell, R. J. (2005) J. Phys. Chem. B, 109, 992–998.

    Article  PubMed  CAS  Google Scholar 

  79. Roszak, A. W., McKendrick, K., Gardiner, A. T., Mitchell, I. A., Isaacs, N. W., Cogdell, R. J., Hashimoto, H., and Frank, H. A. (2004) Structure, 12, 765–773.

    Article  PubMed  CAS  Google Scholar 

  80. Utschig, L. M., and Thurnauer, M. C. (2004) Acc. Chem. Res., 37, 439–447.

    Article  PubMed  CAS  Google Scholar 

  81. Kirmaier, C., Holten, D., Debus, R. J., Feher, G., and Okamura, M. Y. (1986) PNAS USA, 83, 6407–6411.

    Article  PubMed  CAS  Google Scholar 

  82. Debus, R. J., Feher, G., and Okamura, M. Y. (1986) Biochemistry, 25, 2276–2287.

    Article  PubMed  CAS  Google Scholar 

  83. Stehlik, D., and Mubius, K. (1997) Ann. Rev. Phys. Chem., 48, 745–784.

    Article  CAS  Google Scholar 

  84. Lubitz, W., Lendzian, F., and Bittl, R. (2002) Acc. Chem. Res., 35, 313–320.

    Article  PubMed  CAS  Google Scholar 

  85. Lubitz, W., and Feher, G. (1999) Appl. Mag. Res., 17, 1–48.

    Article  CAS  Google Scholar 

  86. Schnegg, A., Fuhs, M., Rohrer, M., Lubitz, W., Prisner, T. F., and Mubius, K. (2002) J. Phys. Chem. B, 106, 9454–9462.

    Article  CAS  Google Scholar 

  87. Flores, M., Isaacson, R., Abresch, E., Calvo, R., Lubitz, W., and Feher, G. (2006) Biophys. J., 90, 3356–3362.

    Article  PubMed  CAS  Google Scholar 

  88. Zech, S. G., Bittl, R., Gardiner, A. T., and Lubitz, W. (1997) Appl. Mag. Res., 13, 517–529.

    Article  CAS  Google Scholar 

  89. Borovykh, I. V., Dzuba, S. A., Proskuryakov, I. I., Gast, P., and Hoff, A. J. (1998) Biochim. Biophys. Acta Bioenerg., 1363, 182–186.

    Article  CAS  Google Scholar 

  90. Poluektov, O. G., Utschig, L. M., Tang, J., Dubinski, A. A., Schlesselman, S., and Thurnauer, M. C. (2001) Appl. Mag. Res., 21, 311–323.

    Article  CAS  Google Scholar 

  91. Poluektov, O. G., Utschig, L. M., Dubinskij, A. A., and Thurnauer, M. C. (2005) J. Am. Chem. Soc., 127, 4049–4059.

    Article  PubMed  CAS  Google Scholar 

  92. Hulsebosch, R. J., Borovykh, I. V., Paschenko, S. V., Gast, P., and Hoff, A. J. (1999) J. Phys. Chem. B, 103, 6815–6823.

    Article  CAS  Google Scholar 

  93. Utschig, L. M., Thurnauer, M. C., Tiede, D. M., and Poluektov, O. G. (2005) Biochemistry, 44, 14131–14142.

    Article  PubMed  CAS  Google Scholar 

  94. Calvo, R., Abresch, E. C., Bittl, R., Feher, G., Hofbauer, W., Isaacson, R. A., Lubitz, W., Okamura, M. Y., and Paddock, M. L. (2000) J. Am. Chem. Soc., 122, 7327–7341.

    Article  CAS  Google Scholar 

  95. Calvo, R., Isaacson, R. A., Paddock, M. L., Abresch, E. C., Okamura, M. Y., Maniero, A. L., Brunel, L. C., and Feher, G. (2001) J. Phys. Chem. B, 105, 4053–4057.

    Article  CAS  Google Scholar 

  96. Calvo, R., Isaacson, R. A., Abresch, E. C., Okamura, M. Y., and Feher, G. (2002) Biophys. J., 83, 2440–2456.

    Article  PubMed  CAS  Google Scholar 

  97. Wellington, C. L., Taggart, A. K. P., and Beatty, J. T. (1991) J. Bacteriol., 173, 2954–2961.

    PubMed  CAS  Google Scholar 

  98. Swingley, W. D., Blankenship, R. E., and Raymond, J. (2009) The Purple Phototrophic Bacteria, Vol. 28 (Hunter, C. N., Daldal, F., Thurnauer, M. C., and Beatty, J. T., eds.) Springer, Dordrecht, The Netherlands, pp. 17–29.

    Chapter  Google Scholar 

  99. Wellington, C. L., Bauer, C. E., and Beatty, J. T. (1992) Can. J. Micribiol., 38, 20–27.

    Article  CAS  Google Scholar 

  100. Youvan, D. C., Bylina, E. J., Alberti, M., Begusch, H., and Hearst, J. E. (1984) Cell, 37, 949–957.

    Article  PubMed  CAS  Google Scholar 

  101. Coomber, S. A., Chaudri, M., Connor, A., Britton, G., and Hunter, C. N. (1990) Mol. Microbiol., 4, 977–989.

    Article  PubMed  CAS  Google Scholar 

  102. Hunter, C. M., McGlynn, P., Ashby, M. K., Burgess, J. G., and Olsen, J. D. (1991) Mol. Microbiol., 5, 2649–2661.

    Article  PubMed  CAS  Google Scholar 

  103. Kaplan, S. (2002) Photosynth. Res., 73, 95–108.

    Article  PubMed  CAS  Google Scholar 

  104. Donohue, T. J., Kiley, P. J., and Kaplan, S. (1988) Photosynth. Res., 19, 39–61.

    Article  CAS  Google Scholar 

  105. Belasco, J. G., Beatty, J. T., Adams, C. W., von Gabain, A., and Cohen, S. N. (1985) Cell, 40, 171–181.

    Article  PubMed  CAS  Google Scholar 

  106. Kaplan, S., and Donohue, T. J. (1993) The Photosynthetic Reaction Center, Vol. 2 (Deisenhofer, J., and Norris, J. P., eds.) Academic Press, JNC, pp. 101–131.

    Google Scholar 

  107. Vermeglio, A., and Joliot, P. (1999) Trends Microbiol., 7, 435–440.

    Article  PubMed  CAS  Google Scholar 

  108. Holden-Dye, K., Crouch, L. I., and Jones, M. R. (2008) Biochim. Biophys. Acta, 1777, 613–630.

    Article  PubMed  CAS  Google Scholar 

  109. Tsukatani, Y., Matsuura, K., Masuda, S., Shimada, K., Hiraishi, A., and Nagashima, K. V. P. (2004) Photosynth. Res., 79, 83–91.

    Article  PubMed  CAS  Google Scholar 

  110. Roszak, A. W., Howard, T. D., Southall, J., Gardiner, A. T., Law, C. J., Isaacs, N. W., and Cogdell, R. J. (2003) Science, 302, 1969–1972.

    Article  PubMed  CAS  Google Scholar 

  111. Williams, J. C., and Taguchi, A. K. W. (1995) Anoxygenic Photosynthetic Bacteria, Vol. 2 (Blankenship, R. E., Madigan, M. T., and Bauer, C., eds.) Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 1029–1065.

    Google Scholar 

  112. Youvan, D. C., and Marrs, B. L. (1984) Cell, 39, 1–3.

    Article  PubMed  CAS  Google Scholar 

  113. Youvan, D. C., Ismail, S., and Bylina, E. J. (1985) Gene, 38, 19–30.

    Article  PubMed  CAS  Google Scholar 

  114. Bylina, E. J., Ismail, S., and Youvan, D. C. (1986) Plasmid, 16, 175–181.

    Article  PubMed  CAS  Google Scholar 

  115. Bylina, E. J., Kolaczowski, S. V., Norris, S. V., and Youvan, C. Y. (1990) Biochemistry, 29, 6203–6210.

    Article  PubMed  CAS  Google Scholar 

  116. Lang, F. S., and Oesterhelt, D. J. (1989) Bacteriology, 171, 4425–4435.

    CAS  Google Scholar 

  117. Farchaus, J. W., and Oesterhelt, D. A. (1989) EMBO J., 8, 47–54.

    PubMed  CAS  Google Scholar 

  118. Paddock, M. L., Rongey, S. H., Feher, G., and Okamura, M. Y. (1989) PNAS USA, 86, 6602–6606.

    Article  PubMed  CAS  Google Scholar 

  119. Jones, M. R., Visschers, R. W., van Grondelle, R., and Hunter, C. N. (1992) Biochemistry, 31, 4458–4465.

    Article  PubMed  CAS  Google Scholar 

  120. Jones, M. R., Fowler, G. J. C., Gibson, L. C. D., Grief, G. G., Olsen, J. D., Crielaard, W., and Hunter, C. N. (1992) Mol. Microbiol., 6, 1173–1184.

    Article  PubMed  CAS  Google Scholar 

  121. Williams, J. C., Steiner, L. A., Feher, G., and Simon, M. I. (1984) PNAS USA, 81, 7303–7307.

    Article  PubMed  CAS  Google Scholar 

  122. Robles, S. J., Breton, J., and Youvan, D. C. (1990) Science, 248, 1402–1405.

    Article  PubMed  CAS  Google Scholar 

  123. Vos, M. H., Lambry, J. C., Robles, S. J., Youvan, D. C., Breton, J., and Martin, J. L. (1991) PNAS USA, 88, 8885–8889.

    Article  PubMed  CAS  Google Scholar 

  124. Vos, M. H., Rappaport, F., Lambry, J. C., Breton, J., and Martin, J. L. (1993) Nature, 363, 320–325.

    Article  CAS  Google Scholar 

  125. Carter, B., Boxer, S. G., Holten, D., and Kirmaier, C. (2009) Biochemistry, 48, 2571–2573.

    Article  PubMed  CAS  Google Scholar 

  126. Taguchi, A. K. W., Stocker, J. W., Alden, R. G., Causgrove, T. P., Peloquin, J. M., Boxer, S. G., and Woodbury, N. W. (1992) Biochemistry, 31, 10345–10355.

    Article  PubMed  CAS  Google Scholar 

  127. Stocker, J. W., Taguchi, A. K. W., Murchison, H. A., Woodbury, N. W., and Boxer, S. G. (1992) Biochemistry, 31, 10356–10362.

    Article  PubMed  CAS  Google Scholar 

  128. Wachtveitl, J., Farchaus, J. W., Das, R., Lutz, M., Robert, B., and Mattioli, T. A. (1993) Biochemistry, 32, 12875–12886.

    Article  PubMed  CAS  Google Scholar 

  129. Mattioli, T. A., Williams, J. C., Allen, J. P., and Robert, B. (1994) Biochemistry, 33, 1636–1643.

    Article  PubMed  CAS  Google Scholar 

  130. Mattioli, T. A., Lin, X., Allen, J. P., and Williams, J. C. (1995) Biochemistry, 34, 6142–6152.

    Article  PubMed  CAS  Google Scholar 

  131. Taguchi, A. K. W., Eastman, J. E., Gallo, D. M., Sheagley, E., Xiao, W. Z., and Woodbury, N. W. (1996) Biochemistry, 35, 3175–3186.

    Article  PubMed  CAS  Google Scholar 

  132. Coleman, W. J., and Youvan, D. C. (1993) Nature, 366, 517–518.

    Article  PubMed  CAS  Google Scholar 

  133. Ridge, J. P., van Brederode, M. E., Goodwin, M. G., van Grondelle, R., and Jones, M. R. (1999) Photosynth. Res., 59, 9–26.

    Article  CAS  Google Scholar 

  134. Wakeham, M. C., Goodwin, M. G., McKibbin, C., and Jones, M. R. (2003) FEBS Lett., 540, 234–240.

    Article  PubMed  CAS  Google Scholar 

  135. Wakeham, M. C., Breton, J., Nabedryk, E., and Jones, M. R. (2004) Biochemistry, 43, 4755–4763.

    Article  PubMed  CAS  Google Scholar 

  136. McAuley, K. E., Fyfe, P. K., Ridge, J. P., Cogdell, R. J., Isaacs, N. W., and Jones, M. R. (2000) Biochemistry, 39, 15032–15043.

    Article  PubMed  CAS  Google Scholar 

  137. Coleman, W. J., and Youvan, D. C. (1990) Annu. Rev. Biophys. Biophys. Chem., 19, 333–367.

    Article  PubMed  Google Scholar 

  138. Stilz, H. U., Finkele, U., Holzapfel, W., Lauterwasser, C., Zinth, W., and Oesterhelt, D. (1994) Eur. J. Biochem., 223, 233–242.

    Article  PubMed  CAS  Google Scholar 

  139. Watson, A. J., Fyfe, P. K., Frolov, D., Wakeham, M. C., Nabedryk, E., van Grondelle, R., Breton, J., and Jones, M. R. (2005) Biochim. Biophys. Acta Bioenerg., 1710, 34–46.

    Article  CAS  Google Scholar 

  140. Jackson, J. A., Lin, S., Taguchi, A. K. W., Williams, J. C., Allen, J. P., and Woodbury, N. W. (1997) J. Phys. Chem. B, 101, 5747–5754.

    Article  CAS  Google Scholar 

  141. Moore, L. J., and Boxer, S. G. (1998) Photosynth. Res., 55, 173–180.

    Article  CAS  Google Scholar 

  142. Khatypov, R. A., Khmelnitskiy, A. Yu., Leonova, M. M., Vasilieva, L. G., and Shuvalov, V. A. (2008) Doklady Biokhim. Biofiz., 422, 319–324.

    Article  CAS  Google Scholar 

  143. Khatypov, R. A., Khmelnitskiy, A. Yu., Leonova, M. M., Vasilieva, L. G., and Shuvalov, V. A. (2008) Photosynth. Res., 98, 81–93.

    Article  PubMed  CAS  Google Scholar 

  144. Leonova, M. M., Vasilieva, L. G., Khatypov, R. A., Boichenko, V. A., and Shuvalov, V. A. (2009) Biochemistry (Moscow), 74, 452–460.

    Article  CAS  Google Scholar 

  145. Bylina, E. J., and Youvan, D. C. (1988) PNAS USA, 85, 7226–7230.

    Article  PubMed  CAS  Google Scholar 

  146. Kirmaier, C., Holten, D., Bylina, E. J., and Youvan, D. C. (1988) PNAS USA, 85, 7562–7566.

    Article  PubMed  CAS  Google Scholar 

  147. McDowell, L. M., Gaul, D., Kirmaier, C., Holten, D., and Schenck, C. C. (1991) Biochemistry, 30, 8315–8322.

    Article  PubMed  CAS  Google Scholar 

  148. Allen, J. P., Artz, K., Lin, X., Williams, J. C., Ivancich, A., Albouy, D., Mattioli, T. A., Fetsch, A., Kuhn, M., and Lubitz, W. (1996) Biochemistry, 35, 6612–6619.

    Article  PubMed  CAS  Google Scholar 

  149. Nabedryk, E., Schulz, C., Muh, F., Lubitz, W., and Breton, J. (2000) Photochem. Photobiol., 71, 582–588.

    Article  PubMed  CAS  Google Scholar 

  150. Bylina, E. J., and Youvan, D. C. (1990) in Current Research in Photosynthesis, Vol. 1 (Baltscheffsky, M., ed.) Kluwer Academic, The Netherlands, pp. 53–59.

    Google Scholar 

  151. Fajer, J., Borg, D. C., Forman, A., Dolphin, D., and Felton, R. H. (1973) J. Am. Chem. Soc., 95, 2739–2741.

    Article  PubMed  CAS  Google Scholar 

  152. Fajer, J., Brune, D. C., Davis, M. S., Forman, A., and Spaulding, L. D. (1975) PNAS USA, 72, 4956–4960.

    Article  PubMed  CAS  Google Scholar 

  153. Kirmaier, C., Bautista, J. A., Laible, P. D., Hanson, D. K., and Holten, D. (2005) J. Phys. Chem. B, 109, 24160–24172.

    Article  PubMed  CAS  Google Scholar 

  154. Laporte, L. L., Palaniappan, V., Davis, D. G., Kirmaier, C., Schenck, C. C., Holten, D., and Bocian, D. F. (1996) J. Phys. Chem., 100, 17696–17707.

    Article  CAS  Google Scholar 

  155. Woodbury, N. W., and Allen, J. P. (1995) Anoxygenic Photosynthetic Bacteria, Vol. 2 (Blankenship, R. E., Madigan, M. T., and Bauer, C., eds.) Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 527–557.

    Google Scholar 

  156. Albouy, D., Kuhn, M., Williams, J. C., Allen, J. P., Lubitz, W., and Mattioli, T. A. (1997) Biochim. Biophys. Acta Bioenerg., 1321, 137–148.

    Article  CAS  Google Scholar 

  157. Moore, L. J., Zhou, H. L., and Boxer, S. G. (1999) Biochemistry, 38, 11949–11960.

    Article  PubMed  CAS  Google Scholar 

  158. King, B. A., de Winter, A., McAnaney, T. B., and Boxer, S. G. (2001) J. Phys. Chem. B, 105, 1856–1862.

    Article  CAS  Google Scholar 

  159. Chirino, A. J., Lous, E. J., Huber, M., Allen, J. P., Schenck, C. C., Paddock, M. L., Feher, G., and Rees, D. C. (1994) Biochemistry, 33, 4584–4593.

    Article  PubMed  CAS  Google Scholar 

  160. Camara-Artigas, A., Magee, C., Goetsch, A., and Allen, J. P. (2002) Photosynth. Res., 74, 87–93.

    Article  PubMed  CAS  Google Scholar 

  161. Katilius, E., Turanchik, T., Lin, S., Taguchi, A. K. W., and Woodbury, N. W. (1999) J. Phys. Chem. B, 103, 7386–7389.

    Article  CAS  Google Scholar 

  162. Arlt, T., Dohse, B., Schmidt, S., Wachtveitl, J., Laussermair, E., Zinth, W., and Oesterhelt, D. (1996) Biochemistry, 35, 9235–9244.

    Article  PubMed  CAS  Google Scholar 

  163. Katilius, E., Babendure, J. L., Lin, S., and Woodbury, N. W. (2004) Photosynth. Res., 81, 165–180.

    Article  CAS  Google Scholar 

  164. Callahan, P., and Cotton, T. J. (1987) Am. Chem. Soc., 109, 7001–7007.

    Article  CAS  Google Scholar 

  165. Kirmaier, C., Gaul, D., DeBey, R., Holten, D., and Schenck, C. C. (1991) Science, 251, 922–927.

    Article  PubMed  CAS  Google Scholar 

  166. Heller, B. A., Holten, D., and Kirmaier, C. (1995) Science, 269, 940–945.

    Article  PubMed  CAS  Google Scholar 

  167. Heller, B. A., Holten, D., and Kirmaier, C. (1995) Biochemistry, 34, 5294–5302.

    Article  PubMed  CAS  Google Scholar 

  168. Paddock, M. L., Chang, C., Xu, Q., Abresch, E. C., Axelrod, H. L., Feher, G., and Okamura, M. Y. (2005) Biochemistry, 44, 6920–6928.

    Article  PubMed  CAS  Google Scholar 

  169. Jaschke, P. R., and Beatty, J. T. (2007) Biochemistry, 46, 12491–12500.

    Article  PubMed  CAS  Google Scholar 

  170. Lin, S., Jaschke, P. R., Wang, H., Paddock, M., Tufts, A., Allen, J. P., Rosell, F. I., Mauk, A. G., Woodbury, N. W., and Beatty, J. T. (2009) PNAS USA, 106, 8537–8542.

    Article  PubMed  CAS  Google Scholar 

  171. Allen, J. P., and Williams, J. C. (2006) Chlorophylls and Bacteriochlorophylls, Biochemistry, Biophysics, Functions and Applications, Vol. 25 (Grimm, B., Porra, R. J., Rudiger, W., and Scheer, H., eds.) Springer, Dordrecht, pp. 283–295.

    Google Scholar 

  172. Williams, J. C., and Allen, J. P. (2009) The Purple Phototrophic Bacteria, Vol. 28 (Hunter, C. N., Daldal, F., Thurnauer, M. C., and Beatty, J. T., eds.) Springer, Dordrecht, The Netherlands, pp. 337–353.

    Chapter  Google Scholar 

  173. Williams, J. C., Haffa, A. L. M., McCulley, J. L., Woodbury, N. W., and Allen, J. P. (2001) Biochemistry, 40, 15403–15407.

    Article  PubMed  CAS  Google Scholar 

  174. Johnson, E. T., and Parson, W. W. (2002) Biochemistry, 41, 6483–6494.

    Article  PubMed  CAS  Google Scholar 

  175. Johnson, E. T., Muh, F., Nabedryk, E., Williams, J. C., Allen, J. P., Lubitz, W., Breton, J., and Parson, W. W. (2002) J. Phys. Chem. B, 106, 11859–11869.

    Article  CAS  Google Scholar 

  176. Haffa, A. L. M., Lin, S., Katilius, E., Williams, J. C., Taguchi, A. K. W., Allen, J. P., and Woodbury, N. W. (2002) J. Phys. Chem., 106, 7376–7384.

    CAS  Google Scholar 

  177. Murchison, H. A., Alden, R. G., Allen, J. P., Peloquin, J. M., Taguchi, A. K. W., Woodbury, N. W., and Williams, J. C. (1993) Biochemistry, 32, 3498–3505.

    Article  PubMed  CAS  Google Scholar 

  178. Spiedel, D., Jones, M. R., and Robert, B. (2002) FEBS Lett., 527, 171–175.

    Article  PubMed  CAS  Google Scholar 

  179. Williams, J. C., Alden, R. G., Murchison, H. A., Peloquin, J. M., Woodbury, N. W., and Allen, J. P. (1992) Biochemistry, 31, 11029–11037.

    Article  PubMed  CAS  Google Scholar 

  180. Lin, X., Murchison, H. A., Nagarajan, V., Parson, W. W., Allen, J. P., and Williams, J. C. (1994) PNAS USA, 91, 10265–10269.

    Article  PubMed  CAS  Google Scholar 

  181. Nabedryk, E., Allen, J. P., Taguchi, A. K. W., Williams, J. C., Woodbury, N. W., and Breton, J. (1993) Biochemistry, 32, 13879–13885.

    Article  PubMed  CAS  Google Scholar 

  182. Deshmukh, S. S., Williams, J. C., Allen, J. P., and Kalman, L. (2011) Biochemistry, 50, 340–348.

    Article  CAS  Google Scholar 

  183. Thielges, M., Uyeda, G., Camara-Artigas, A., Kalman, L., Williams, J. C., and Allen, J. P. (2005) Biochemistry, 44, 7389–7394.

    Article  PubMed  CAS  Google Scholar 

  184. Muh, F., Lendzian, F., Roy, M., Williams, J. C., Allen, J. P., and Lubitz, W. (2002) J. Phys. Chem. B, 106, 3226–3236.

    Article  CAS  Google Scholar 

  185. Deisenhofer, J., Epp, O., Sinning, I., and Michel, H. (1995) J. Mol. Biol., 246, 429–457.

    Article  PubMed  CAS  Google Scholar 

  186. Ivancich, A., Kobayashi, M., Drepper, F., Fathir, I., Saito, T., Nozawa, T., and Mattioli, T. A. (1996) Biochemistry, 35, 10529–10538.

    Article  PubMed  CAS  Google Scholar 

  187. Wachtveitl, J., Farchaus, J. W., Das, R., Lutz, M., Robert, B., and Mattioli, T. A. (1993) Biochemistry, 32, 12875–12886.

    Article  PubMed  CAS  Google Scholar 

  188. Kuglstatter, A., Hellwig, P., Fritzsch, G., Wachtveitl, J., Oesterhelt, D., Mantele, W., and Michel, H. (1999) FEBS Lett., 463, 169–174.

    Article  PubMed  CAS  Google Scholar 

  189. Dracheva, S. M., Drachev, L. A., Konstantinov, A. A., Semenov, A. Y., Skulachev, V. P., Arutjunjan, A. M., Shuvalov, V. A., and Zaberezhnaya, S. M. (1988) Eur. J. Biochem., 171, 253–264.

    Article  PubMed  CAS  Google Scholar 

  190. Ullmann, G. M., Kloppmann, E., Essigke, T., Krammer, E. M., Klingen, A. R., Becker, T., and Bombarda, E. (2008) Photosynth. Res., 97, 33–53.

    Article  PubMed  CAS  Google Scholar 

  191. Krammer, E., Sebban, P., and Ullmann, G. M. (2009) Biochemistry, 48, 1230–1243.

    Article  PubMed  CAS  Google Scholar 

  192. Holden-Dye, K., Crouch, L. I., Williams, C. M., Bone, R. A., Cheng, J., Bohles, F., Heathcote, P., and Jones, M. R. (2011) Arch. Biochem. Biophys., 505, 160–170.

    Article  PubMed  CAS  Google Scholar 

  193. Hamm, P., Gray, K. A., Oesterhelt, D., Feik, R., Scheer, H., and Zinth, W. (1993) Biochim. Biophys. Acta, 1142, 90–105.

    Google Scholar 

  194. Vos, M. H., Jones, M. R., Breton, J., Lambry, J. C., and Martin, J.-L. (1996) Biochemistry, 35, 2687–2692.

    Article  PubMed  CAS  Google Scholar 

  195. Shochat, S., Arlt, T., Francke, C., Gast, P., van Noort, P. I., Otte, S. C., Schelvis, H. P. M., Schmidt, S., Vijgenboom, E., Vrieze, J., Zinth, W., and Hoff, A. J. (1994) Photosynth. Res., 40, 55–66.

    Article  CAS  Google Scholar 

  196. Parson, W. W., Chu, Z. T., and Warshel, A. (1990) Biochim. Biophys. Acta, 1017, 251–272.

    Article  PubMed  CAS  Google Scholar 

  197. Alden, R. G., Parson, W. W., Chu, Z. T., and Warshel, A. (1996) J. Phys. Chem., 100, 16761–16770.

    Article  CAS  Google Scholar 

  198. Beekman, L. M. P., van Stokkum, I. H. M., Monshouwer, R., Rijnders, A. J., McGlynn, P., Visschers, R. W., Jones, M. R., and van Grondelle, R. (1996) J. Phys. Chem., 100, 7256–7268.

    Article  CAS  Google Scholar 

  199. Nagarajan, V., Parson, W. W., Davis, D., and Schenck, C. C. (1993) Biochemistry, 32, 12324–12336.

    Article  PubMed  CAS  Google Scholar 

  200. Jia, Y., DiMagno, T. J., Chan, C.-K., Wang, Z., Du, M., Hanson, D. K., Schiffer, M., Norris, J. R., Fleming, G. R., and Popov, M. S. (1993) J. Phys. Chem., 97, 13180–13191.

    Article  CAS  Google Scholar 

  201. Yakovlev, A. G., Vasilieva, L. G., Shkuropatov, A. Y., and Shuvalov, V. A. (2009) Biochemistry (Moscow), 74, 1203–1210.

    Article  CAS  Google Scholar 

  202. Yakovlev, A. G., Vasilieva, L. G., Khmelnitskaya, T. I., Shkuropatova, V. A., Shkuropatov, A. Y., and Shuvalov, V. A. (2010) Biochemistry (Moscow), 75, 832–840.

    Article  CAS  Google Scholar 

  203. Roberts, J. A., Holten, D., and Kirmaier, C. (2001) J. Phys. Chem. B, 105, 5575–5584.

    Article  CAS  Google Scholar 

  204. Kirmaier, C., Weems, D., and Holten, D. (1999) Biochemistry, 38, 11516–11530.

    Article  PubMed  CAS  Google Scholar 

  205. Kee, H. L., Laible, P. D., Bautista, J. A., Hanson, D. K., Holten, D., and Kirmaier, C. (2006) Biochemistry, 45, 7314–7322.

    Article  PubMed  CAS  Google Scholar 

  206. Kirmaier, C., and Holten, D. (2009) J. Phys. Chem. B, 113, 1132–1142.

    Article  PubMed  CAS  Google Scholar 

  207. Chuang, J. I., Boxer, S. G., Holten, D., and Kirmaier, C. (2008) J. Phys. Chem. B, 112, 5487–5499.

    Article  PubMed  CAS  Google Scholar 

  208. Kirmaier, C., Laible, P. D., Czarnecki, K., Hata, A. N., Hanson, D. K., Bocian, D. F., and Holten, D. (2002) J. Phys. Chem. B, 106, 1799–1808.

    Google Scholar 

  209. Katilius, E., Katiliene, Z., Lin, S., Taguchi, A. K. W., and Woodbury, N. W. (2002) J. Phys. Chem. B, 106, 1471–1475.

    Article  CAS  Google Scholar 

  210. Katilius, E., Babendure, J. L., Katiliene, Z., Lin, S., Taguchi, A. K. W., and Woodbury, N. W. (2003) J. Phys. Chem. B, 107, 12029–12034.

    Article  CAS  Google Scholar 

  211. Yakovlev, A. G., Shkuropatova, T. A., Shkuropatova, V. A., and Shuvalov, V. A. (2010) Biochemistry (Moscow), 75, 412–422.

    Article  CAS  Google Scholar 

  212. Axelrod, H. L., Abresch, E. C., Okamura, M. Y., Yeh, A. P., Rees, D. C., and Feher, G. (2002) J. Mol. Biol., 319, 501–515.

    Article  PubMed  CAS  Google Scholar 

  213. Long, J., Durham, B., Okamura, M., and Millett, F. (1989) Biochemistry, 28, 6970–6974.

    Article  PubMed  CAS  Google Scholar 

  214. Tetreault, M., Rongey, S. H., Feher, G., and Okamura, M. (2001) Biochemistry, 40, 8452–8462.

    Article  PubMed  CAS  Google Scholar 

  215. Caffrey, M. S., Bartsch, R. G., and Cusanovich, M. A. (1992) J. Biol. Chem., 267, 6317–6321.

    PubMed  CAS  Google Scholar 

  216. Gong, X., Paddock, M., and Okamura, M. (2003) Biochemistry, 42, 14492–14500.

    Article  PubMed  CAS  Google Scholar 

  217. Abresch, E. C., Paddock, M. L., Villalobos, M., Chang, C., and Okamura, M. Y. (2008) Biochemistry, 47, 13318–13325.

    Article  PubMed  CAS  Google Scholar 

  218. Abresch, E. C., Gong, X. M., Paddock, M. L., and Okamura, M. Y. (2009) Biochemistry, 48, 11390–11398.

    Article  PubMed  CAS  Google Scholar 

  219. Koepke, J., Krammer, E.-M., Klingen, A. R., Sebban, P. G., Ullmann, M., and Fritzsch, G. (2007) J. Mol. Biol., 371, 396–409.

    Article  PubMed  CAS  Google Scholar 

  220. Paddock, M. L., Feher, G., and Okamura, M. Y. (1995) Biochemistry, 34, 15742–15750.

    Article  PubMed  CAS  Google Scholar 

  221. Miksovska, J., Kalman, L., Schiffer, M., Maroti, P., Sebban, P., and Hanson, D. K. (1997) Biochemistry, 36, 12216–12226.

    Article  PubMed  CAS  Google Scholar 

  222. Goldsmith, J. O., King, B., and Boxer, S. G. (1996) Biochemistry, 35, 2421–2428.

    Article  PubMed  CAS  Google Scholar 

  223. Michel, H., and Deisenhofer, J. (1988) Biochemistry, 27, 1–7.

    Article  CAS  Google Scholar 

  224. Kalman, L., LoBrutto, R., Allen, J. P., and Williams, J. P. (1999) Nature, 402, 696–699.

    Article  Google Scholar 

  225. Kalman, L., LoBrutto, R., Narvaez, A. J., Williams, J. C., and Allen, J. P. (2003) Biochemistry, 42, 13280–13286.

    Article  PubMed  CAS  Google Scholar 

  226. Narvaez, A. J., LoBrutto, R., Allen, J. P., and Williams, J. C. (2004) Biochemistry, 43, 14379–14384.

    Article  PubMed  CAS  Google Scholar 

  227. Kalman, L., Williams, J. C., and Allen, J. P. (2003) FEBS Lett., 545, 193–198.

    Article  PubMed  CAS  Google Scholar 

  228. Kalman, L., Williams, J. C., and Allen, J. P. (2005) Photosystem II, the Light-Driven Water Plastoquinone Oxidoreductase (Wydrzynski, T., and Satoh, K., eds.) Springer, Dordrecht, The Netherlands, pp. 715–727.

    Google Scholar 

  229. Coleman, W. J., Mattioli, T. A., Youvan, D. C., and Rutherford, A. W. (1997) Biochemistry, 36, 2178–2187.

    Article  PubMed  CAS  Google Scholar 

  230. Wraight, C. A. (2004) Front. Biosci., 9, 309–337.

    Article  PubMed  CAS  Google Scholar 

  231. Sebban, P., Maroti, P., Schiffer, M., and Hanson, D. K. (1995) Biochemistry, 34, 8390–8397.

    Article  PubMed  CAS  Google Scholar 

  232. Tandori, J., Baciou, L., Alexov, E., Maroti, P., Schiffer, M., Hanson, D. K., and Sebban, P. (2001) J. Biol. Chem., 276, 45513–45515.

    Article  PubMed  CAS  Google Scholar 

  233. Fufina, T. Yu., Vasilieva, L. G., Khatypov, R. A., Shkuropatov, A. Ya., and Shuvalov, V. A. (2007) FEBS Lett., 581, 5769–5773.

    Article  PubMed  CAS  Google Scholar 

  234. Khatypov, T. I., Vasilieva, L. G., Fufina, T. Y., Bolgarina T. I., and Shuvalov, V. A. (2005) Biochemistry (Moscow), 70, 1256–1261.

    Article  CAS  Google Scholar 

  235. Fufina, T. Y., Vasilieva, L. G., and Shuvalov, V. A. (2010) Biochemistry (Moscow), 75, 208–213.

    Article  CAS  Google Scholar 

  236. Bolgarina, T. I., Khatypov, T. I., Vasilieva, L. G., Shkuropatov, A. Y., and Shuvalov, V. A. (2004) Doklady Biokhim. Biofiz., 394, 26–29.

    Article  CAS  Google Scholar 

  237. Frolov, D., Marsh, M., Crouch, L. I., Fyfe, P. K., Robert, B., van Grondelle, R., Hadfield, A., and Jones, M. R. (2010) Biochemistry, 49, 1882–1892.

    Article  PubMed  CAS  Google Scholar 

  238. Fufina, T. Y., Vasilieva, L. G., Khatypov, R. A., and Shuvalov, V. A. (2011) Biochemistry (Moscow), 76, 450–454.

    Article  CAS  Google Scholar 

  239. Fufina, T. Y., Vasilieva, L. G., Khatypov, R. A., and Shuvalov, V. A. (2010) Proc. Phot. Congress, China, in press.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. M. Leonova.

Additional information

Original Russian Text © M. M. Leonova, T. Yu. Fufina, L. G. Vasilieva, V. A. Shuvalov, 2011, published in Uspekhi Biologicheskoi Khimii, 2011, Vol. 51, pp. 193–232.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Leonova, M.M., Fufina, T.Y., Vasilieva, L.G. et al. Structure-function investigations of bacterial photosynthetic reaction centers. Biochemistry Moscow 76, 1465–1483 (2011). https://doi.org/10.1134/S0006297911130074

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297911130074

Key words

Navigation