Advertisement

Photosystem I pp 319-338 | Cite as

Electrogenic Reactions Associated with Electron Transfer in Photosystem I

  • Alexey Yu. Semenov
  • Mahir D. Mamedov
  • Sergey K. Chamorovsky
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 24)

Abstract

Photoelectric methods to study charge transfer processes in photosynthetic organisms are reviewed along with comparative analyses of photoelectric reactions in Photosystem I, Photosystem II, and the reaction center of purple bacteria. Particular emphasis is placed on a comparison of dielectrically weighted photoelectric signal amplitudes with local structural parameters obtained from the X-ray diffraction data.

Keywords

Purple Bacterium Acceptor Side Sulfur Cluster Photosynthetic Reaction Center Effective Dielectric Constant 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1987) Structure of the reaction center from Rhodobacter sphaeroides R-26: the cofactors. Proc Natl Acad Sci USA 84: 5730–5734PubMedCrossRefGoogle Scholar
  2. Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1988) Structure of the reaction center from Rhodobacter sphaeroides R-26: protein –cofactor (quinones and Fe2 + interactions. Proc Natl Acad Sci USA 85: 8487–8491PubMedCrossRefGoogle Scholar
  3. Antonkine ML, Jordan P, Fromme P, Krauß N, Golbeck JH and Stehlik D (2003) Assembly of protein subunits within the stromal ridge of photosystem I. Structural changes between unbound and sequentially PS I-bound polypeptides and correlated changes of the magnetic properties of the terminal iron–sulfur clusters. J Mol Biol 327: 671–697PubMedCrossRefGoogle Scholar
  4. Brettel K and Leibl W (2001) Electron transfer in photosystem I. Biochim Biophys Acta 1507: 100–114PubMedCrossRefGoogle Scholar
  5. Bulychev AA, Andrianov VK, Kurella GA and Litvin FF (1972) Micro-electrode measurements of the transmembrane potential of chloroplasts and its photoinduced changes. Nature 236: 175–177CrossRefGoogle Scholar
  6. Cherepanov DA and Krishtalik LI (1990) Intramembrane electric fields: a single charge, protein α-helix, photosynthetic reaction center. Bioelectrochem Bioenerg 24: 113–127CrossRefGoogle Scholar
  7. Deisenhofer J, Epp O, Miki K, Huber R and Michel H (1985) Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3 Å resolution. Nature 318: 618–624CrossRefGoogle Scholar
  8. Deprez J, Trissl HW and Breton J (1986) Excitation trapping and primary charge stabilization in Rhodopseudomonas viridis cells, measured electrically with picosecond resolution. Proc Natl Acad Sci USA 83: 1699–1703PubMedCrossRefGoogle Scholar
  9. Diaz-Quintana A, Leibl W, Bottin H and Sétif P (1998) Electron transfer in photosystem I reaction centers follows a linear pathway in which iron-sulfur cluster FB is the immediate electron donor to soluble ferredoxin. Biochemistry 37: 3429–3439PubMedCrossRefGoogle Scholar
  10. Drachev LA, Jasaitis AA, Kaulen AD, Kondrashin AA, Liberman EA, Nemecek IB, Ostroumov SA, Semenov AY and Skulachev VP (1974) Direct measurement of electric current generation by cytochrome oxidase, H+-ATPase and bacteriorhodopsin. Nature 249: 321–324PubMedCrossRefGoogle Scholar
  11. Drachev LA, Frolov VN, Kaulen AD, Kondrashin AA, Samuilov VD, Semenov AY and Skulachev VP (1976) Generation of electric current by chromatophores of Rhodospirillum rubrum and reconstitution of electrogenic function in subchromatophore pigment–protein complexes. Biochim Biophys Acta 440: 637–660PubMedCrossRefGoogle Scholar
  12. Drachev LA, Kaulen AD, Semenov AY, Severina II and Skulachev VP (1979) Lipid-impregnated filters as a tool for studying the electric current-generating proteins. Analyt Biochem 96: 250–262PubMedCrossRefGoogle Scholar
  13. Drachev LA, Kaulen AD, Khitrina LV and Skulachev VP (1981a) Fast stages of photoelectric processes in biological membranes. I. Bacteriorhodopsin. Eur J Biochem 117: 461–470CrossRefGoogle Scholar
  14. Drachev LA, Semenov AY, Skulachev VP, Smirnova IA, Chamorovsky SK, Kononenko AA, Rubin AB and Uspenskaya NYa (1981b) Fast stages of photoelectric processes in biological membranes. III. Bacterial photosynthetic redox system. Eur J Biochem 117: 483–489CrossRefGoogle Scholar
  15. Drachev LA, Kaminskaya OP, Konstantinov AA, Semenov AY, Skulachev VP (1985) Electrogenic reduction of Rhodospirillum rubrum reaction centre bacteriochlorophyll P870+ by redox dyes. Indication of intraprotein electron transfer. FEBS Lett 189: 45–49CrossRefGoogle Scholar
  16. Dracheva SM, Drachev LA, Konstantinov AA, Semenov AY, Skulachev VP, Arutyunian AM, Shuvalov VA and Zaberezhnaya SM (1988) Electrogenic steps in the redox reactions catalyzed by photosynthetic reaction-centre complex from Rhodopseudomonas viridis. Eur J Biochem 171: 253–264PubMedCrossRefGoogle Scholar
  17. Ermler U, Fritzsch G, Buchanan SK and Michel H (1994) Structure of the photosynthetic reaction center from Rhodobacter sphaeroides at 2.65 Å resolution: cofactors and protein-cofactor interactions. Structure 2: 925–936PubMedCrossRefGoogle Scholar
  18. Fersht A (1999) Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding. WH Freeman, New YorkGoogle Scholar
  19. Fowler CF and Kok B (1974) Direct observation of a light-induced electric field in chloroplasts. Biochim Biophys Acta 357: 308–318PubMedCrossRefGoogle Scholar
  20. Fromme P, Schubert WD and Krauß N (1994) Structure of photosystem I: suggestions on the docking sites for plastocyanin, ferredoxin and the coordination of P700. Biochim Biophys Acta 1187: 99–105CrossRefGoogle Scholar
  21. Golbeck JH (1999) A comparative analysis of the spin state distributions of in vitro and in vivo mutants of PsaC. A biochemical argument for the sequence of electron transfer as FX/→ F A/→ F B/to ferredoxin. Photosynth Res 61: 107–144CrossRefGoogle Scholar
  22. Golbeck JH and Bryant DA (1991) Photosystem I. In: Lee CP (ed) Light-Driven Reactions in Bioenergetics. Current Topics in Bioenergetics, Vol 16, pp 83–177. Academic Press, New YorkGoogle Scholar
  23. Gourovskaya KN, Mamedov MD, Vassiliev IR, Golbeck JH and Semenov AY (1997) Electrogenic reduction of the primary electron donor P700+ in photosystem I by redox dyes. FEBS Lett 414: 193–196PubMedCrossRefGoogle Scholar
  24. Gräber P (1987) Primary charge separation and energy transduction in photosynthesis. In: Milazzo G and Blanks M (eds) Bioelectrochemistry II, pp 381–429. Plenum Publishing Corporation, New YorkGoogle Scholar
  25. Guergova-Kuras M, Boudreaux B, Joliot A, Joliot P and Redding K (2001) Evidence for two active branches for electron transfer in photosystem I. Proc Natl Acad Sci USA 98: 4437–4442PubMedCrossRefGoogle Scholar
  26. Haumann M, Mulkidjanian A and Junge W (1997) Electrogenicity of electron and proton transfer at the oxidizing side of photosystem II. Biochemistry 36: 9304–9315PubMedCrossRefGoogle Scholar
  27. Hecks B, Wulf K, Breton J, Leibl W and Trissl HW (1994) Primary charge separation in photosystem I: a two-step electrogenic charge separation connected with P700+ A 0 - and P700+ A 1 - formation. Biochemistry 33: 8619–8624PubMedCrossRefGoogle Scholar
  28. Hervas M, Ortega JM, Navarro JA, De la Rosa MA and Bottin H (1994) Laser flash kinetic analysis of Synechocystis PCC 6803 cytochrome c6 and plastocyanin oxidation by photosystem I. Biochim Biophys Acta 1184: 235–241CrossRefGoogle Scholar
  29. Hervas M, Navarro JA, Diaz A, Bottin H and De la Rosa MA (1995) Laser-flash kinetic analysis of the fast electron transfer from plastocyanin and cytochrome c6 to photosystem I. Experimental evidence on the evolution of the reaction mechanism. Biochemistry 34: 11321–11326PubMedCrossRefGoogle Scholar
  30. Hillmann B, Brettel K, van Mieghem F, Kamlowski A, Rutherford AW and Schlodder E (1995) Charge recombination reactions in photosystem II. 2. Transient absorbance difference spectra and their temperature dependence. Biochemistry 34: 4814–4827PubMedCrossRefGoogle Scholar
  31. Holzwarth AR and Muller MG (1996) Energetics and kinetics of radical pairs in reaction centers from Rhodobacter sphaeroides. A femtosecond transient absorption study. Biochemistry 35: 11820–11831PubMedCrossRefGoogle Scholar
  32. Hook F and Brzezinski P (1994) Light-induced voltage changes associated with electron and proton transfer in photosystem II core complexes reconstituted in phospholipid monolayers. Biophys J 66: 2066–2072PubMedGoogle Scholar
  33. Jackson JB and Crofts AR (1969) The high energy state in chromatophores from Rhodopseudomonas sphaeroides. FEBS Lett 4: 185–189PubMedCrossRefGoogle Scholar
  34. Joliot P and Joliot A (1984) Electron transfer between the two photosystems. I. Flash excitation under oxidizing conditions. Biochim Biophys Acta 765: 210–218CrossRefGoogle Scholar
  35. Joliot P and Joliot A (1999) In vivo analysis of the electron transfer within photosystem I: are the two phylloquinones involved? Biochemistry 38: 11130–11136PubMedCrossRefGoogle Scholar
  36. Jordan P (2001) Rontgenstrukturanalyse des Trimeren Photosystems I aus dem Cyanobakterium Synechococcus elongatus bei 2.5 A Auflosung. PhD Thesis. Free University, BerlinGoogle Scholar
  37. Jordan P, Fromme P, Witt HT, Klukas O, Saenger W and Krauß N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411: 909–917PubMedCrossRefGoogle Scholar
  38. Jung Y-S, Yu L and Golbeck JH (1995) Reconstitution of iron–sulfur center FB results in complete restoration of NADP+ photoreduction in Hg-treated Photosystem I complexes from Synechococcus sp. PCC 6301. Photosynth Res 46: 249–255CrossRefGoogle Scholar
  39. Junge W and Witt HT (1968) On the ion transport system of photosynthesis. Investigations on a molecular level. Z Naturforsch 23b: 244–246Google Scholar
  40. Kaminskaya OP, Drachev LA, Konstantinov AA, Semenov AY and Skulachev VP (1986) Electrogenic reduction of the secondary quinone acceptor in chromatophores of Rhodospirillum rubrum. Rapid kinetic measurements. FEBS Lett 2: 224–228CrossRefGoogle Scholar
  41. Kamiya N and Shen JR (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynecoccus vulcanus at 3.7 Å resolution. Proc Natl Acad Sci USA 100: 98–103PubMedCrossRefGoogle Scholar
  42. Karapetyan NV, Holzwarth AR and Rögner M (1999) The photosystem I trimer of cyanobacteria: molecular organization, excitation dynamics and physiological significance. FEBS Lett 460: 395–400PubMedCrossRefGoogle Scholar
  43. Kojima Y, Niinomi Y, Tsuboi S, Hiyama T and Sakurai H (1987) Destruction of photosystem I iron-sulfur centers of spinach and Anacystis nidulans by mercurials. Bot Mag 100: 243–253CrossRefGoogle Scholar
  44. Krishtalik LI (1996) Intramembrane electron transfer: processes in the photosynthetic reaction center. Biochim Biophys Acta 1273: 139–149CrossRefGoogle Scholar
  45. Krishtalik LI and Topolev VV (2000) Effects of medium polarization and pre-existing field on activation energy of enzymatic charge-transfer reactions. Biochim Biophys Acta 1459: 88–105PubMedCrossRefGoogle Scholar
  46. Leibl W, Toupance B and Breton J (1995) Photoelectric characterization of forward electron transfer to iron-sulfur centers in photosystem I. Biochemistry 34: 10237–10244PubMedCrossRefGoogle Scholar
  47. Mamedov MD, Beshta OE, Samuilov VD and Semenov AY (1994) Electrogenicity at the secondary quinone acceptor site of cyanobacterial photosystem II. FEBS Lett 350: 96–98PubMedCrossRefGoogle Scholar
  48. Mamedov MD, Lovyagina EP, Verkhovsky MI, Semenov AY, Cherepanov DA and Shinkarev VP (1995) Generation of the electrical potential difference by photosystem II from thermophilic cyanobacteria. Biochemistry (Moscow) 59: 327–341Google Scholar
  49. Mamedov MD, Gadjieva RM, Gourovskaya KN, Drachev LA and Semenov AY (1996) Electrogenicity at the donor/acceptor sides of cyanobacterial photosystem I. J Bioenerg Biomembr 28: 517–522PubMedCrossRefGoogle Scholar
  50. Mamedov MD, Gourovskaya KN, Vassiliev IR, Golbeck JH and Semenov AY (1998) Electrogenicity accompanies photoreduction of the iron-sulfur clusters FA and FB in photosystem I. FEBS Lett 431: 219–223PubMedCrossRefGoogle Scholar
  51. Mamedov MD, Beshta OE, Gourovskaya KN, Mamedova AA, Neverov KD, Samuilov VD and Semenov AY (1999) Photoelectric responses of oxygen-evolving complexes of photosystem II. Biochemistry (Moscow) 64: 606–611Google Scholar
  52. Mamedov MD, Mamedova AA, Chamorovsky SK, Semenov AY (2001) Electrogenic reduction of the primary electron donor P700+ by plastocyanin in photosystem I complexes. FEBS Lett 500: 172–176PubMedCrossRefGoogle Scholar
  53. Mamedov MD, Tyunyatkina AA and Semenov AY (2005) Electrogenic protonation of the secondary quinone acceptor QB in spinach photosystem II complexes incorporated into lipid vesicles. Biochemistry (Moscow) 70: 1639–1645CrossRefGoogle Scholar
  54. Mamedova AA, Mamedov MD, Gourovskaya KN, Vassiliev IR, Golbeck JH and Semenov AY (1999) Electrometrical study of electron transfer from the terminal FA/FB iron-sulfur clusters to external acceptors in photosystem I. FEBS Lett 462: 421–424PubMedCrossRefGoogle Scholar
  55. Marcus R (1996) Electron transfer reactions in chemistry. Theory and experiment. In: Bendall DS (ed) Protein Electron Transfer, pp 249–272. Bios Scientific Publishers, OxfordGoogle Scholar
  56. Mertz EL and Krishtalik LI (2000) Low dielectric response in enzyme active site. Proc Natl Acad Sci USA 97: 2081–2086PubMedCrossRefGoogle Scholar
  57. Mitchell P and Pasternak CA (eds) (1992) Perspectives in Vectorial Metabolism and Osmochemistry. Glynn Research Foundation, Glynn, U.K.Google Scholar
  58. Myshkin E, Leontis NB and Bullerjahn S (2002) Computational simulation of the docking of Prochlorothrix hollandica plastocyanin to photosystem I: modeling the electron transfer complex. Biophys J 82: 3305–3313PubMedCrossRefGoogle Scholar
  59. Okamura MY and Feher G (1992) Proton transfer in reaction centers from photosynthetic bacteria. Annu Rev Biochem 61: 861–896PubMedCrossRefGoogle Scholar
  60. Parson WW, Chu ZT and Warshel A (1998) Reorganization energy of the initial electron-transfer step in photosynthetic bacterial reaction centers. Biophys J 74: 182–191PubMedGoogle Scholar
  61. Peloquin JM, Williams JC, Lin XM, Alden RG, Taguchi AKW, Allen JP and Woodbury NW (1994) Time-dependent thermodynamics during early electron transfer in reaction centers from Rhodobacter sphaeroides. Biochemistry 33: 8089–8100PubMedCrossRefGoogle Scholar
  62. Pokorny A, Wulf K and Trissl H-W (1994) An electrogenic reaction associated with the re-reduction of P680 by Tyr Z in photosystem II. Biochim Biophys Acta 1184: 65–70CrossRefGoogle Scholar
  63. Semenov AY (1991) Electrogenic reactions in photosynthetic reaction centres of purple bacteria. In: Skulachev VP (ed) Soviet Scientific Reviews/Section D, Vol 10, pp 45–75. Harwood Academic Publishers, U.K.Google Scholar
  64. Semenov AY, Mamedov MD and Chamorovsky SK (2003) Photoelectric studies of the transmembrane charge transfer reactions in photosystem I pigment-protein complexes. FEBS Lett 553: 223–228PubMedCrossRefGoogle Scholar
  65. Shinkarev VP, Drachev LA, Mamedov MD, Mulkidjanian AYa, Semenov AY and Verkhovsky MI (1993) Effect of pH and surface potential on the rate of electric potential generation due to proton uptake by secondary quinone acceptor of reaction centers in Rhodobacter sphaeroides chromatophores. Biochim Biophys Acta 1144: 285–294CrossRefGoogle Scholar
  66. Steffen MA, Lao K and Boxer SG (1994) Dielectric asymmetry in the photosynthetic reaction center. Science 264: 810–815CrossRefPubMedGoogle Scholar
  67. Stowell MHB, McPhillips TM, Rees DC, Soltis SM, Abresch E and Feher G (1997) Light-induced structural changes in photosynthetic reaction center: implications for mechanism of electron-proton transfer. Science 276: 812–816PubMedCrossRefGoogle Scholar
  68. Trissl HW and Gräber P (1980) II. Electrical measurements in the nanosecond range of the charge separation from chloroplasts spread at a heptane-water interface. Application of a novel capacitive electrode. Biochim Biophys Acta 595: 96–108PubMedCrossRefGoogle Scholar
  69. Trissl HW and Leibl W (1989) Primary charge separation in photosystem II involves two electrogenic steps. FEBS Lett 244: 85–88CrossRefGoogle Scholar
  70. Trissl HW, Leibl W, Deprez J, Dobek A and Breton J (1987) Trapping and annihilation in the antenna system of photosystem I. Biochim Biophys Acta 893: 320–332CrossRefGoogle Scholar
  71. Trissl HW, Bernhardt K and Lapin M (2001) Evidence for protein dielectric relaxations in reaction centers associated with the primary charge separation detected from Rhodospirillum rubrum chromatophores by combined photovoltage and absorption measurements in the 1–15 ns time range. Biochemistry 40: 5290–5298PubMedGoogle Scholar
  72. Vassiliev IR, Jung Y-S, Mamedov MD, Semenov AY and Golbeck JH (1997) Near-IR absorbance changes and electrogenic reactions in the microsecond-to-second time domain in photosystem I. Biophys J 72: 301–315PubMedGoogle Scholar
  73. Vassiliev IR, Jung Y-S, Yang F and Golbeck JH (1998) PsaC subunit of photosystem I is oriented with iron-sulfur cluster FB as the immediate electron donor to ferredoxin and flavodoxin. Biophys J 74: 2029–2035PubMedGoogle Scholar
  74. Witt HT and Zickler A (1973) Vectorial electron flow across the thylakoid membrane. Further evidence by kinetic measurements with an electrochromic and electrical method. FEBS Lett 37: 307–310PubMedCrossRefGoogle Scholar
  75. Woodbury NW and Parson WW (1984) Nanosecond fluorescence from isolated photosynthetic reaction centers of Rhodopseudomonas sphaeroides. Biochim Biophys Acta 767: 345–361PubMedCrossRefGoogle Scholar
  76. Xu W, Chitnis P, Valieva A, van der Est A, Brettel K, Guergova-Kuras M, Pushkar J, Zech SG, Stehlik D, Shen G, Zybailov B and Golbeck JH (2003) Electron transfer in cyanobacterial photosystem I: II. Determination of forward electron transfer rates of site-directed mutants in a putative electron transfer pathway from A0 through A1 to FX. J Biol Chem 278: 27876–27887PubMedCrossRefGoogle Scholar
  77. Zouni A, Witt H-T, Kern J, Fromme P, Krauß N, Saenger W and Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409: 739–743PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Alexey Yu. Semenov
    • 1
  • Mahir D. Mamedov
    • 1
  • Sergey K. Chamorovsky
    • 2
  1. 1.A.N. Belozersky Institute of Physico-Chemical BiologyMoscow State UniversityMoscowRussia
  2. 2.Department of Biophysics, Faculty of BiologyMoscow State UniversityMoscowRussia

Personalised recommendations