RSS feeds
РусскийEnglish
Issue 12, 2024
Volume year page
Issues Authors PACS Subscription For authors

Issues

 / 

2016

 / 

June

←  →

Reviews of topical problems


Physical stage of photosynthesis charge separation

 a,  a, b
a Lomonosov Moscow State University, Belozersky Research Institute of Physico-Chemical Biology, Vorobevy gory, build. A, Moscow, 119899, Russian Federation
b Institute of Fundamental Problems of Biology, Russian Academy of Sciences, Pushchino, Moscow Region, Russian Federation

An analytical review is given of the biophysical aspects of primary light-driven charge separation in photosynthesis reaction centers (RCs), which are special pigment-protein complexes residing in a cell membrane. The primary (physical) stage of charge separation occurs in the pico- and femtosecond ranges and consists in transferring an electron along the active A-branch of pigments. The review presents vast factual material both on the general issues of primary photosynthesis and some more specific topics, including 1) the role of inactive B-branch of pigments, 2) the effect of protein environment on the charge separation, and 3) the participation of monomeric bacteriochlorophyll BA in primary electron acception. It is shown that the electron transfer and stabilization are strongly influenced by crystallographic water and tyrosine M210 molecules from the nearest environment of BA. A connection between the collective nuclear motions and electron transfer at charge separation is shown. The nature of the high quantum efficiency of the primary charge separation reactions is discussed.

Fulltext pdf (892 KB)
Fulltext is also available at DOI: 10.3367/UFNe.2016.02.037701
Keywords: photosynthesis, reaction center, charge separation, electron transfer
PACS: 87.15.ht, 87.15.M−, 87.15.R− (all)
DOI: 10.3367/UFNe.2016.02.037701
URL: https://ufn.ru/en/articles/2016/6/b/
000386349400002
2-s2.0-84987597397
2016PhyU...59..531Y
Citation: Yakovlev A G, Shuvalov V A "Physical stage of photosynthesis charge separation" Phys. Usp. 59 531–557 (2016)
BibTexBibNote ® (generic)BibNote ® (RIS)MedlineRefWorks

Received: 19th, October 2015, revised: 28th, January 2016, 2nd, February 2016

Оригинал: Яковлев А Г, Шувалов В А «Физическая стадия разделения зарядов при фотосинтезе» УФН 186 597–625 (2016); DOI: 10.3367/UFNr.2016.02.037701

References (318) ↓ Cited by (4) Similar articles (20)

  1. Rubin A B, Shinkarev V P Transport Elektronov v Biologicheskikh Sistemakh (M.: Nauka, 1984)
  2. Shuvalov V A Pervichnoe Preobrazovanie Svetovoi Energii pri Fotosinteze (M.: Nauka, 1990)
  3. Deisenhofer J, Norris J R (Eds) The Photosynthetic Reaction Center Vol. 1, 2 (San Diego, CA: Academic Press, 1993)
  4. Parson W W Protein Electron Transfer (Ed. D S Bendall) (Oxford: BIOS Sci. Publ., 1996) p. 125
  5. Hoff A J, Deisenhofer J Phys. Rep. 287 1 (1997)
  6. Okamura M Y et al. Biochim. Biophys. Acta BBA Bioenerg. 1458 148 (2000)
  7. Shuvalov V A Preobrazovanie Solnechnoi Energii v Pervichnom Akte Razdeleniya Zaryadov v Reaktsionnykh Tsentrakh Fotosinteza (Timiryazevskie Chteniya, Vyp. 60) (M.: Nauka, 2000)
  8. van Brederode M E, Jones M R Enzyme-Catalyzed Electron And Radical Transfer (Subcellular Biochemistry) Vol. 35 (Eds A Holzenburg,NS Scrutton) (New York: Kluwer Acad./Plenum Publ., 2000) p. 621
  9. Wraight C A Front. Biosci. 9 309 (2004)
  10. Parson W W, Warshel A The Purple Phototrophic Bacteria (Advances in Photosynthesis and Respiration) Vol. 28 (Eds C N Hunter et al.) (Dordreht: Springer, 2009) p. 355
  11. Williams J C, Allen J P The Purple Phototrophic Bacteria (Advances in Photosynthesis and Respiration) Vol. 28 (Eds C N Hunter et al.) (Dordreht: Springer, 2009) p. 337
  12. Yakovlev A G Pervichnyi Fotosintez (Saarbrücken: LAMBERT Acad. Publ., 2013)
  13. Allakhverdiev S I, Rubin A B, Shuvalov V A (Red.) Fotosintez: Otkrytye Voprosy i Chto My Znaem Segodnya (M.-Izhevsk: Inst. komp’yut. issled., 2013)
  14. Olson J M, Thornber J P Membrane Proteins In Energy Transduction (Ed. R A Capaldi) (New York: M. Dekker, 1979) p. 279
  15. Feher G, Okamura M Y The Photosynthetic Bacteria (Eds R K Clayton, W R Sistrom) (New York: Plenum Press, 1978) p. 349
  16. Deisenhofer J et al. Nature 318 618 (1985)
  17. Deisenhofer J, Michel H, Huber R Trends Biochem. 10 243 (1985)
  18. Blankenship R E et al. J. Cell. Biochem. 22 251 (1983)
  19. Pierson B K, Thornber J P Proc. Natl. Acad. Sci. USA 80 80 (1983)
  20. Hale M B, Blankenship R E, Fuller R C Biochim. Biophys. Acta BBA Bioenerg. 723 376 (1983)
  21. Michel H et al. EMBO J. 5 1149 (1986)
  22. Deisenhofer J et al. J. Mol. Biol. 180 385 (1984)
  23. Chang C-H et al. J. Mol. Biol. 186 201 (1985)
  24. Chang C-H et al. FEBS Lett. 205 82 (1986)
  25. Allen J P et al. Proc. Natl. Acad. Sci. USA 84 5730 (1987)
  26. Allen J P et al. Proc. Natl. Acad. Sci. USA 84 6162 (1987)
  27. Ermler U et al. Structure 2 925 (1994)
  28. Plato M et al. The Photosynthetic Bacterial Reaction Center II: Structure, Spectroscopy, And Dynamics (NATO ASI Ser. A, Eds J Breton, A Verméglio) (New York: Plenum Press, 1992) p. 109
  29. Artz K et al. Proc. Natl. Acad. Sci. USA 94 13582 (1997)
  30. Müh F et al. J. Phys. Chem. B 106 3226 (2002)
  31. Holten D et al. Biochim. Biophys. Acta BBA Bioenerg. 592 461 (1980)
  32. Paschenko V Z et al. FEBS Lett. 191 245 (1985)
  33. Woodbury N W et al. Biochemistry 24 7516 (1985)
  34. Woodbury N W et al. Biochemistry 33 8101 (1994)
  35. Breton J et al. Proc. Natl. Acad. Sci. USA 83 5121 (1986)
  36. Martin J-L et al. Proc. Natl. Acad. Sci. USA 83 957 (1986)
  37. Wasielewski M R, Tiede D M FEBS Lett. 204 368 (1986)
  38. Kirmaier C, Holten D Israel J. Chem. 28 79 (1988)
  39. Holzapfel W et al. Chem. Phys. Lett. 160 1 (1989)
  40. Holzapfel W et al. Proc. Natl. Acad. Sci. USA 87 5168 (1990)
  41. Lauterwasser C et al. Chem. Phys. Lett. 183 471 (1991)
  42. Peloquin J M et al. Biochemistry 33 8089 (1994)
  43. Holzwarth A R, Muller M G Biochemistry 35 11820 (1996)
  44. Huppman P et al. Biophys. J. 82 3186 (2002)
  45. Kaufmann K J et al. Science 188 1301 (1975)
  46. Rockley M G et al. Proc. Natl. Acad. Sci. USA 72 2251 (1975)
  47. Holten D et al. Biochim. Biophys. Acta BBA Bioenerg. 501 112 (1978)
  48. Kirmaier C, Holten D, Parson W W Biochim. Biophys. Acta BBA Bioenerg. 810 49 (1985)
  49. Kirmaier C, He C, Holten D Biochemistry 40 12132 (2001)
  50. Kirmaier C et al. J. Phys. Chem. B 108 11827 (2004)
  51. Kellog E C et al. Photosynth. Res. 22 47 (1989)
  52. Mar T, Gingras G Biochim. Biophys. Acta BBA Bioenerg. 1017 112 (1990)
  53. Robles S J, Breton J, Youvan D C Science 248 1402 (1990)
  54. Heller BA, Holten D, Kirmaier C Science 269 940 (1995)
  55. de Boer A L et al. Biochemistry 41 3081 (2002)
  56. Katilius E et al. J. Phys. Chem. B 106 1471 (2002)
  57. Haffa A L M et al. J. Phys. Chem. B 108 4 (2004)
  58. Bylina E J et al. Nature 336 182 (1988)
  59. Wraight C A, Clayton R K Biochim. Biophys. Acta BBA Bioenerg. 333 246 (1974)
  60. Biochim. Biophys. Acta BBA Bioenerg. 1015 322 (1990)
  61. J. Phys. Chem. B 102 735 (1998)
  62. Breton J et al. Biochemistry 27 8276 (1988)
  63. Fleming G R, Martin J-L, Breton J Nature 333 190 (1988)
  64. Nagarajan V et al. Proc. Natl. Acad. Sci. USA 87 7888 (1990)
  65. Nagarajan V et al. Biochemistry 32 12324 (1993)
  66. Jia Y et al. J. Phys. Chem. 97 13180 (1993)
  67. Haffa A L M et al. J. Phys. Chem. B 106 7376 (2002)
  68. Schenck C C et al. Biophys. J. 36 479 (1981)
  69. Kirmaier C, Holten D, Parson W W Biochim. Biophys. Acta BBA Bioenerg. 810 33 (1985)
  70. Gunner M R, Dutton P L J. Am. Chem. Soc. 111 3400 (1989)
  71. Wang H, Lin S, Woodbury N W J. Phys. Chem. B 110 6956 (2006)
  72. Lin S et al. J. Phys. Chem. B 107 14103 (2003)
  73. Dahlbom M G, Reimers J R Mol. Phys. 103 1057 (2005)
  74. Katilius E et al. J. Phys. Chem. B 103 7386 (1999)
  75. Katilius E et al. Photosynth. Res. 81 165 (2004)
  76. Feick R, Shiozawa J A, Ertlmaier A Anoxygenic Photosynthetic Bacteria (Advances in Photosynthesis) Vol. 2 (Eds R E Blankenship, M T Madigan, C E Bauer) (Dordrecht: Kluwer Acad. Publ., 1995) p. 699
  77. Bruce B D, Fuller R C, Blankenship R E Proc. Natl. Acad. Sci. USA 79 6532 (1982)
  78. Kirmaier C et al. FEBS Lett. 158 73 (1983)
  79. Kirmaier C, Blankenship R E, Holten D Biochim. Biophys. Acta BBA Bioenerg. 850 275 (1986)
  80. Vasmel H, Amesz J Biochim. Biophys. Acta BBA Bioenerg. 724 118 (1983)
  81. Venturoli G et al. Eur. J. Biochem. 202 625 (1991)
  82. Ovchinnikov Yu A et al. FEBS Lett. 231 237 (1988)
  83. Ovchinnikov Yu A et al. FEBS Lett. 232 364 (1988)
  84. Shiozawa J A et al. Eur. J. Biochem. 180 75 (1989)
  85. Parot P et al. Biochim. Biophys. Acta BBA Bioenerg. 809 137 (1985)
  86. Shuvalov V A et al. Biochim. Biophys. Acta BBA Bioenerg. 849 337 (1986)
  87. Vasmel H, Amesz J, Hoff A J Biochim. Biophys. Acta BBA Bioenerg. 852 159 (1986)
  88. Scherer P O J, Fischer S F Biochim. Biophys. Acta BBA Bioenerg. 891 157 (1987)
  89. Becker M et al. Biochim Biophys Acta BBA Bioenerg. 1057 299 (1991)
  90. Feick R et al. Reaction Centers Of Photosynthetic Bacteria. Feldafing-II-Meeting (Springer Series in Biophysics) Vol. 6 (Ed. M E Michel-Beyerle) (Berlin: Springer-Verlag, 1990) p. 181
  91. Volk M et al. Biochim. Biophys. Acta BBA Bioenerg. 1058 217 (1991)
  92. Wachtveitl J et al. Spectrochim. Acta A 54 1231 (1998)
  93. Parson W W, Chu Z-T, Warshel A Biochim. Biophys. Acta BBA Bioenerg. 1017 251 (1990)
  94. Gunner M, Nicholls A, Honig B J. Phys. Chem. 100 4277 (1996)
  95. Watanabe T, Kobayashi M Chlorophylls (Ed. H Scheer) (Boca Raton, Fla.: CRC Press, 1991) p. 287
  96. Fajer J et al. Proc. Natl. Acad. Sci. USA 72 4956 (1975)
  97. Schweitzer G et al. Chem. Phys. Lett. 190 149 (1992)
  98. Aumeier W et al. Current Research in Photosynthesis. Proc. of the VIIIth Intern. Congress on Photosynthesis, Stockholm, Sweden, August 6 - 11, 1989 Vol. 1 (Ed. M Baltscheffsky) (Dordrecht: Kluwer Acad. Publ., 1990) p. 133
  99. van Brederode M E et al. Biochemistry 36 6855 (1997)
  100. van Brederode M E et al. Proc. Natl. Acad. Sci. USA 96 2054 (1999)
  101. van Brederode M E et al. Biochemistry 38 7545 (1999)
  102. Lin S et al. J. Phys. Chem. B 103 4757 (1999)
  103. Lin S et al. Biochemistry 40 13767 (2001)
  104. Zhou H, Boxer S G J. Phys. Chem. B 102 9139 (1998)
  105. Zhou H, Boxer S G J. Phys. Chem. B 102 9148 (1998)
  106. King B A et al. J. Phys. Chem. B 105 1856 (2001)
  107. Kennis J T M et al. Biochemistry 36 16231 (1997)
  108. Shuvalov V A, Parson W W Proc. Natl. Acad. Sci. USA 78 957 (1980)
  109. Vos M H et al. Proc. Natl. Acad. Sci. USA 88 8885 (1991)
  110. Vos M H et al. Proc. Natl. Acad. Sci. USA 89 613 (1992)
  111. Du M et al. Proc. Natl. Acad. Sci. USA 89 8517 (1992)
  112. Hamm P et al. Biochim. Biophys. Acta BBA Bioenerg. 1142 99 (1993)
  113. Stanley R J, Boxer S G J. Phys. Chem. 99 859 (1995)
  114. Beekman L M P et al. J. Phys. Chem. 100 7256 (1996)
  115. Ogrodnik A et al. Chem. Phys. 244 461 (1999)
  116. Wang H W et al. Science 316 747 (2007)
  117. Kirmaier C, Holten D Proc. Natl. Acad. Sci. USA 87 3552 (1990)
  118. Wang Z et al. Chem. Phys. 176 421 (1993)
  119. Gehlen J N, Marchi M, Chandler D Science 263 499 (1994)
  120. Hartwich G et al. J. Phys. Chem. B 102 3815 (1998)
  121. Peloquin J M et al. J. Phys. Chem. 99 1349 (1995)
  122. Peloquin J M et al. J. Phys. Chem. 100 14228 (1996)
  123. Small G J, Hayes J M, Silbey R J J. Phys. Chem. 96 7499 (1992)
  124. Lyle P A, Kolaczkowski S V, Small G J J. Phys. Chem. 97 6924 (1993)
  125. Small G J Chem. Phys. 197 239 (1995)
  126. Hamm P, Zinth W J. Phys. Chem. 99 13537 (1995)
  127. Johnson S G et al. J. Phys. Chem. 94 5849 (1990)
  128. Middendorf T R et al. J. Phys. Chem. 95 10142 (1991)
  129. Reddy N R S, Lyle P A, Small G J Photosynth. Res. 31 167 (1992)
  130. Vos M H et al. Nature 363 320 (1993)
  131. Vos M H et al. Proc. Natl. Acad. Sci. USA 91 12701 (1994)
  132. Vos M H et al. Biochemistry 33 6750 (1994)
  133. Vos M H et al. Biochemistry 35 2687 (1996)
  134. Vos M H, Jones M R, Martin J-L Chem. Phys. 233 179 (1998)
  135. Vos M H et al. Biochemistry 39 8353 (2000)
  136. Martin J-L, Vos M H Annu. Rev. Biophys. Biomol. Struct. 21 199 (1992)
  137. Vos M, Martin J-L Biochim. Biophys. Acta BBA Bioenerg. 1411 1 (1999)
  138. Spörlein S, Zinth W, Wachtveitl J J. Phys. Chem. B 102 7492 (1998)
  139. Rischel C et al. Proc. Natl. Acad. Sci. USA 95 12306 (1998)
  140. Parson W W, Warshel A Chem. Phys. 296 201 (2004)
  141. Parson W W, Warshel A J. Phys. Chem. B 108 10474 (2004)
  142. Czarnecki K et al. J. Am. Chem. Soc. 119 415 (1997)
  143. Kitzing E, Kühn H J. Phys. Chem. 94 1699 (1990)
  144. Lin S, Taguchi A K W, Woodbury N W J. Phys. Chem. 100 17067 (1996)
  145. Taguchi A K W et al. Biochemistry 35 3175 (1996)
  146. Wakeham M C, Jones M R Biochem. Soc. Trans. 133 851 (2005)
  147. Kirmaier C et al. J. Phys. Chem. B 106 495 (2002)
  148. Kirmaier C et al. J. Phys. Chem. B 106 1799 (2002)
  149. Kirmaier C et al. Biochemistry 42 2016 (2003)
  150. Kee H L et al. Biochemistry 45 7314 (2006)
  151. Paddock M L et al. Biochemistry 45 14032 (2006)
  152. Laible P D et al. Biochemistry 42 1718 (2003)
  153. Breton J et al. Biochim. Biophys. Acta BBA Bioenerg. 1656 127 (2004)
  154. Paddock M L et al. Biochemistry 44 6920 (2005)
  155. Wakeham M C et al. FEBS Lett. 540 234 (2003)
  156. Wakeham M C et al. Biochemistry 43 4755 (2004)
  157. Frolov D et al. Biochim. Biophys. Acta BBA Bioenerg. 1707 189 (2005)
  158. Allen J P et al. Photosynth. Res. 55 227 (1998)
  159. Parson W W, Warshel A Biophysical Techniques In Photosynthesis(Advances In Photosynthesis And Respiration, Vol. 26, Eds T J Aartsma, J Matysik) Vol. 2 (Dordrecht: Springer, 2008) p. 401
  160. Warshel A, Parson W W Quart. Rev. Biophys. 34 563 (2001)
  161. Alden R G et al. J. Phys. Chem. 100 16761 (1996)
  162. Finkele U et al. Biochemistry 29 8517 (1990)
  163. Chan C K et al. Chem. Phys. Lett. 176 366 (1991)
  164. Shochat S et al. Photosynth. Res. 40 55 (1994)
  165. Heller B A, Holten D, Kirmaier C Biochemistry 34 5294 (1995)
  166. Heller B A, Holten D, Kirmaier C Biochemistry 35 15418 (1996)
  167. Kirmaier C et al. J. Phys. Chem. 99 8903 (1995)
  168. Kirmaier C et al. J. Phys. Chem. 99 8910 (1995)
  169. Kirmaier C, Weems D, Holten D Biochemistry 38 11516 (1999)
  170. Lin S et al. Biochemistry 35 3187 (1996)
  171. Czarnecki K et al. J. Phys. Chem. A 103 2235 (1999)
  172. Chuang J I et al. Biochemistry 45 3845 (2006)
  173. Ivashin N et al. J. Phys. Chem. B 102 5017 (1998)
  174. Kolbasov D, Scherz A Photosynthesis: Mechanisms and Effects. Proc. of the XIth Intern. Congress on Photosynthesis, Budapest, Hungary, August 17 - 22, 1998 Vol. 2 (Ed. G Garab) (Dordrecht: Kluwer Acad. Publ., 1998) p. 719
  175. Kolbasov D, Scherz A J. Phys. Chem. B 104 1802 (2000)
  176. Zhang L Y, Friesner R A Proc. Natl. Acad. Sci. USA 95 13603 (1998)
  177. Parson W W, Creighton S, Warshel A Primary Processes in Photobiology. Proc. of the 12th Taniguchi Symp., Fujiyoshida, Yamanashi Prefecture, Japan, December 7 - 12, 1986 (Ed. T Kobayashi) (Berlin: Springer-Verlag, 1987) p. 43
  178. Warshel A, Creighton S, Parson W W J. Phys. Chem. 92 2698 (1988)
  179. Moser C C et al. Nature 355 796 (1992)
  180. Gray H B, Winkler J R Annu. Rev. Biochem. 65 537 (1996)
  181. Newton M D Theor. Chem. Acc. 110 307 (2003)
  182. Skourtis S S et al. Proc. Natl. Acad. Sci. USA 102 3552 (2005)
  183. Steffen M A, Lao K Q, Boxer S G Science 264 810 (1994)
  184. Lin J, Beratan D N J. Phys. Chem. B 109 7529 (2005)
  185. Gray H B, Winkler J R Proc. Natl. Acad. Sci. USA 102 3534 (2005)
  186. Noy D, Moser C C, Dutton P L Biochim. Biophys. Acta BBA Bioenerg. 1757 90 (2006)
  187. Katilius E et al. J. Phys. Chem. B 106 12344 (2002)
  188. Kirmaier C et al. J. Phys. Chem. B 109 24160 (2005)
  189. Ishikita H et al. FEBS Lett. 579 712 (2005)
  190. Ishikita H et al. Biochemistry 45 2063 (2006)
  191. Middendorf T R et al. Biochim. Biophys. Acta BBA Bioenerg. 1143 223 (1993)
  192. Yanagi K et al. J. Phys. Chem. B 109 992 (2005)
  193. Haffa A L M et al. J. Phys. Chem. B 107 12503 (2003)
  194. Yakovlev A G et al. Biochim. Biophys. Acta BBA Bioenerg. 1757 369 (2006)
  195. Yakovlev A G et al. J. Bioinform. Comput. Biol. 6 643 (2008)
  196. McDowell L M et al. Biochemistry 30 8315 (1991)
  197. Allen J P et al. Biochemistry 35 6612 (1996)
  198. Kirmaier C et al. Science 251 922 (1991)
  199. Watson A J et al. Biochim. Biophys. Acta BBA Bioenerg. 1710 34 (2005)
  200. Williams J C et al. Appl. Magn. Reson. 31 45 (2007)
  201. Jackson J A et al. J. Phys. Chem. B 101 5747 (1997)
  202. Moore L J, Boxer S G Photosynth. Res. 55 173 (1998)
  203. Robles S J, Breton J, Youvan D C Reaction Centers Of Photosynthetic Bacteria. Feldafing-II-Meeting (Springer Series in Biophysics) Vol. 6 (Ed. M-E Michel-Beyerle) (Berlin: Springer-Verlag, 1990) p. 283
  204. Khatypov R A et al. Biochemistry Moscow 70 1527 (2005)
  205. Spiedel D, Jones M R, Robert B FEBS Lett. 527 171 (2002)
  206. Stocker J W et al. Biochemistry 31 10356 (1992)
  207. Williams J C et al. Biochemistry 31 11029 (1992)
  208. Murchison H A et al. Biochemistry 32 3498 (1993)
  209. Allen J P, Williams J C J. Bioenerg. Biomembr. 27 275 (1995)
  210. Allen J P, Williams J C Chlorophylls And Bacteriochlorophylls. Biochemistry, Biophysics, Functions And Applications (Advances in Photosynthesis and Respiration) Vol. 25 (Eds B Grimm et al.) (Dordrecht: Springer, 2006) p. 283
  211. Lin X et al. Proc. Natl. Acad. Sci. USA 91 10265 (1994)
  212. Chen L et al. J. Phys. Chem. B 108 10457 (2004)
  213. Müh F et al. Biochemistry 37 13066 (1998)
  214. Williams J C et al. Biochemistry 40 15403 (2001)
  215. Johnson E T, Parson W W Biochemistry 41 6483 (2002)
  216. Johnson E T et al. J. Phys. Chem. B 106 11859 (2002)
  217. Treynor T P, Yoshina-Ishii C, Boxer S G J. Phys. Chem. B 108 13523 (2004)
  218. Alden R G et al. Reaction Centers Of Photosynthetic Bacteria: Structure And Dynamics (Ed. M-E Michel-Beyerle) (Berlin: Springer, 1996) p. 105
  219. Reimers J R, Hush N S J. Am. Chem. Soc. 126 4132 (2004)
  220. Kanchanawong P et al. J. Phys. Chem. B 110 18688 (2006)
  221. Goldsmith J O, Boxer S G Biochim. Biophys. Acta BBA Bioenerg. 1276 171 (1996)
  222. Bylina E J et al. Biochemistry 29 6203 (1990)
  223. Arlt T et al. J. Phys. Chem. 100 12060 (1996)
  224. Arlt T et al. Biochemistry 35 9235 (1996)
  225. Katilius E et al. J. Phys. Chem. B 107 12029 (2003)
  226. Bylina E J, Youvan D C Proc. Natl. Acad. Sci. USA 85 7226 (1988)
  227. Kálmán L et al. Nature 402 696 (1999)
  228. Kálmán L et al. Biochemistry 42 13280 (2003)
  229. Narváez A J et al. Biochemistry 41 15253 (2002)
  230. Narváez A J et al. Biochemistry 43 14379 (2004)
  231. Thielges M et al. Biochemistry 44 7389 (2005)
  232. Kálmán L et al. Biochemistry 44 13266 (2005)
  233. Johnson E T et al. Biochemistry 42 13673 (2003)
  234. de Boer A L et al. Photosynth. Res. 71 221 (2002)
  235. Woodbury N W et al. Chem. Phys. 197 405 (1995)
  236. McAuley K E et al. FEBS Lett. 467 285 (2000)
  237. Yakovlev A G et al. J. Phys. Chem. A 107 8330 (2003)
  238. Yakovlev A G i dr. Biokhimiya 74 1479 (2009); Yakovlev A G et al. Biochemistry Moscow 74 1203 (2009)
  239. Yakovlev A G i dr. Biokhimiya 75 944 (2010); Yakovlev A G et al. Biochemistry Moscow 75 832 (2010)
  240. Pawlowicz N P et al. Phys. Chem. Chem. Phys. 12 2693 (2010)
  241. Plato M et al. The Photosynthetic Bacterial Reaction Center: Structure And Dynamics, NATO ASI Series A) Vol. 149 (Eds J Breton, A Vermeglio (New York: Plenum Press, 1988) p. 379
  242. Yakovlev A G, Shkuropatov A Ya, Shuvalov V A Biochemistry 41 14019 (2002)
  243. Yakovlev A G, Shkuropatov A Ya, Shuvalov V A Biochemistry 41 2667 (2002)
  244. Fok M V, Borisov A Yu Molekulyar. Biologiya 15 575 (1981)
  245. Yakovlev A G et al. Chem. Phys. 319 297 (2005)
  246. Potter J A et al. J. Biol. Chem. 280 27155 (2005)
  247. Deisenhofer J et al. J. Mol. Biol. 246 429 (1995)
  248. Stowell M H B et al. Science 276 812 (1997)
  249. Fyfe P K et al. Biochemistry 39 5953 (2000)
  250. Herzberg G Infrared And Raman Spectra Of Polyatomic Molecules (New York: Van Nostrand, 1945); Per. na russk. yaz., Gertsberg G Kolebatel’nye i Vrashchatel’nye Spektry Mnogoatomnykh Molekul (M.: IL, 1949)
  251. de Rege P J F, Williams S A, Therien M J Science 269 1409 (1995)
  252. Bixon M, Jortner J, Michel-Beyerle M E Biochim. Biophys. Acta BBA Bioenerg. 1056 301 (1991)
  253. Creighton S et al. Biochemistry 27 774 (1988)
  254. Alden R G et al. J. Am. Chem. Soc. 117 12284 (1995)
  255. Warshel A et al. Biochim. Biophys. Acta BBA Bioenerg. 1764 1647 (2006)
  256. Scherer P O J, Fischer S F J. Phys. Chem. 93 1633 (1989)
  257. Scherer P O J, Fischer S F Spectrochim. Acta A 54 1191 (1998)
  258. Thompson M A, Zerner M C, Fajer J J. Am. Chem. Soc. 113 8210 (1991)
  259. Marchi M et al. J. Am. Chem. Soc. 115 4178 (1993)
  260. Blomberg M R A, Siegbahn P H M, Babcock G T J. Am. Chem. Soc. 120 8812 (1998)
  261. Hasegawa J, Nakatsuji H J. Phys. Chem. B 102 10420 (1998)
  262. Hughes J M et al. J. Am. Chem. Soc. 123 8550 (2001)
  263. Gilson M K et al. J. Mol. Biol. 184 503 (1985)
  264. Warshel A, Russell S T Quart. Rev. Biophys. 17 283 (1984)
  265. Hunenberger P H, Mark A E, van Gunsteren W F J. Mol. Biol. 252 492 (1995)
  266. Figueirido F, Del Buono G S, Levy R M J. Phys. Chem. B 101 5622 (1997)
  267. Sham Y Y, Warshel A J. Chem. Phys. 109 7940 (1998)
  268. Procacci et al. J. Comp. Chem. 18 1848 (1997)
  269. Ceccarelli M, Marchi M J. Phys. Chem. B 107 5630 (2003)
  270. Parson W W, Chu Z T, Warshel A Biophys. J. 74 182 (1998)
  271. Parson W W, Chu Z T, Warshel A Photosynth. Res. 55 147 (1998)
  272. Schmidt S et al. Chem. Phys. Lett. 223 116 (1994)
  273. Schmidt S et al. Spectrochim. Acta A 51 1565 (1995)
  274. Egger R, Mak C H J. Phys. Chem. 98 9903 (1994)
  275. Bixon M, Jortner J, Michel-Beyerle M E Chem. Phys. 197 389 (1995)
  276. Bixon M, Jortner J, Michel-Beyerle M E The Reaction Center Of Photosynthetic Bacteria: Structure And Dynamics (Ed. M-E Michel-Beyerle) (Berlin: Springer, 1996) p. 287
  277. Sim E, Makri N J. Phys. Chem. B 101 5446 (1997)
  278. Zusman L D, Beratan D N Spectrochim. Acta A 54 1211 (1998)
  279. Spörlein S et al. Chem. Phys. Lett. 322 454 (2000)
  280. Roberts J A, Holten D, Kirmaier C J. Phys. Chem. B 105 5575 (2001)
  281. Ivashin N, Larsson S J. Phys. Chem. B 106 3996 (2002)
  282. Shuvalov V A, Yakovlev A G Biol. Membr. 15 459 (1998); Shuvalov V A, Yakovlev A G Biochemistry Moscow Suppl. A 12 563 (1998)
  283. Shuvalov V A, Klimov V V Biochim. Biophys. Acta BBA Bioenerg. 440 587 (1976)
  284. Godik V I, Borisov A Y Biochim. Biophys. Acta BBA Bioenerg. 548 296 (1979)
  285. Rademaker J, Hoff A J Biophys. J. 34 325 (1981)
  286. Godik V I, Kotova E A, Borisov A Y Photobiochem. Photobiophys. 4 219 (1982)
  287. Schenck C C, Blankenship R E, Parson W W Biochim. Biophys. Acta BBA Bioenerg. 680 44 (1982)
  288. Woodbury N W T, Parson W W Biochim. Biophys. Acta BBA Bioenerg. 767 345 (1984)
  289. Hörber J K H et al. FEBS Lett. 198 273 (1986)
  290. Woodbury N W et al. Biochim. Biophys. Acta BBA Bioenerg. 851 6 (1986)
  291. Goldstein R A, Boxer S G Biochim. Biophys. Acta BBA Bioenerg. 977 70 (1988)
  292. Ogrodnik A Biochim. Biophys. Acta BBA Bioenerg. 1020 65 (1990)
  293. Ogrodnik A et al. J. Phys. Chem. 98 3432 (1994)
  294. Parson W W, Clayton R K, Cogdell R J Biochim. Biophys. Acta BBA Bioenerg. 387 265 (1975)
  295. Takiff L, Boxer S G Biochim. Biophys. Acta BBA Bioenerg. 932 325 (1988)
  296. Blankenship R E, Schaafsma T J, Parson W W Biochim. Biophys. Acta BBA Bioenerg. 461 297 (1977)
  297. Haberkorn R, Michel-Beyerle M E Biophys. J. 26 489 (1979)
  298. Hoff A J Quart. Rev. Biophys. 14 599 (1981)
  299. Boxer S G, Chidsey E D, Roelofs M G Annu. Rev. Phys. Chem. 34 389 (1983)
  300. Chidsey C E D et al. Proc. Natl. Acad. Sci. USA 82 6850 (1985)
  301. Ogrodnik A et al. Biochim. Biophys. Acta BBA Bioenerg. 936 361 (1988)
  302. Boxer S G et al. J. Phys. Chem. 93 8280 (1989)
  303. Shuvalov V A et al. FEBS Lett. 91 135 (1978)
  304. Shuvalov V A, Duysens L N M Proc. Natl. Acad. Sci. USA 83 1690 (1986)
  305. Chekalin S V et al. FEBS Lett. 216 245 (1987)
  306. Matveets Yu A i dr. Dokl. Akad. Nauk SSSR 294 1480 (1987)
  307. Arlt T et al. Proc. Natl. Acad. Sci. USA 90 11757 (1993)
  308. Bixon M et al. The Photosynthetic Bacterial Reaction Center: Structure And Dynamics (NATO ASI Series A) Vol. 149 (Eds J Breton, A Vermeglio) (New York: Plenum Press, 1988) p. 399
  309. van Stokkum I H M et al. Biochemistry 36 11360 (1997)
  310. Shkuropatov A Y, Shuvalov V A FEBS Lett. 322 168 (1993)
  311. Yakovlev A G, Shkuropatov A Ya, Shuvalov V A FEBS Lett. 466 209 (2000)
  312. Redfield A G Advances In Magnetic Resonance Vol. 1 (Ed. J S Waugh) (New York: Academic Press, 1965) p. 1
  313. Novoderezhkin V I et al. J. Phys. Chem. B 108 7445 (2004)
  314. Eisenmayer T J et al. J. Phys. Chem. Lett. 3 694 (2012)
  315. Eisenmayer T J et al. J. Phys. Chem. B 117 11162 (2013)
  316. Milanovsky G E et al. J. Phys. Chem. B 119 13656 (2015)
  317. Cherepy N J et al. J. Phys. Chem. 98 6023 (1994)
  318. Cherepy N J et al. Biochemistry 36 8559 (1997)
© 1918–2024 Uspekhi Fizicheskikh Nauk
Email: ufn@ufn.ru Editorial office contacts About the journal Terms and conditions