Interquinone electron transfer in photosystem i as evidenced by altering the hydrogen bond strength to the phylloquinone(s)

Journal of Physical Chemistry B

Volumn 114, Issue 28, 2010, Pages 9300-9312

  Santabarbara, Stefano ^a,b,c,e   Reifschneider, Kiera ^a   Jasaitis, Audrius ^b,c   Gu, Feifei ^c   Agostini, Giancarlo ^d   Carbonera, Donatella ^d   Rappaport, Fabrice ^b   Redding, Kevin E ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

^c UNIVERSITY OF ALABAMA   (United States)

^d UNIVERSITY OF PADOVA   (Italy)

^e CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRON TRANSITIONS; HYDROGEN; HYDROGEN BONDS; KETONES; SULFUR;

CHLAMYDOMONAS REINHARDTII; CONSERVED RESIDUES; DRIVING FORCES; ELECTRON TRANSFER; ELECTRON-TRANSFER REACTIONS; GREEN ALGA; HYDROGEN BOND STRENGTH; HYDROGEN BONDINGS; IRON-SULFUR CLUSTERS; OXIDATION KINETICS; PEPTIDE NITROGEN; PHOTOSYSTEM I; PHYLLOQUINONE; REACTION CENTER; RELATIVE AMPLITUDE; WILD TYPES;

OXIDATION;

EID: 77954709177     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp1038656     Document Type: Article

References (47)

1. Brettel, K.; Leibl, W.; Electron transfer in photosystem, I. Biochim. Biophys. Acta-Bioenerg. 2001, 1507 (1-3) 100-114
2. Santabarbara, S.; Heathcote, P.; Evans, M. C. Modelling of the electron transfer reactions in Photosystem I by electron tunnelling theory: the phylloquinones bound to the PsaA and the PsaB reaction centre subunits of PS I are almost isoenergetic to the iron-sulfur cluster F(X) Biochim. Biophys. Acta 2005, 1708 (3) 283-310
3. Srinivasan, N.; Golbeck, J. H. Protein-cofactor interactions in bioenergetic complexes: the role of the A1A and A1B phylloquinones in Photosystem I Biochim. Biophys. Acta 2009, 1787 (9) 1057-88
4. Guergova-Kuras, M.; Boudreaux, B.; Joliot, A.; Joliot, P.; Redding, K. Evidence for two active branches for electron transfer in photosystem I Proc. Natl. Acad. Sci. U.S.A. 2001, 98 (8) 4437-4442
5. ̇- radical pair for photosynthetic electron transfer on both the PsaA and PsaB branches of the photosystem I reaction centre FEBS Lett. 2001, 503 (1) 56-60
6. + and A1- in spin-correlated radical pairs Biochemistry 2005, 44 (6) 2119-28
7. 1-] radical pair of photosystem I indicates that both reaction center subunits are competent in electron transfer in cyanobacteria, green algae, and higher plants Biochemistry 2006, 45 (23) 7389-403
8. Bautista, J. A.; Rappaport, F.; Guergova-Kuras, M.; Cohen, R. O.; Golbeck, J. H.; Wang, J. Y.; Beal, D.; Diner, B. A. Biochemical and biophysical characterization of photosystem I from phytoene desaturase and zeta-carotene desaturase deletion mutants of Synechocystis sp. PCC 6803: Evidence for PsaA- and PsaB-side electron transport in cyanobacteria J. Biol. Chem. 2005, 280 (20) 20030-41
9. Poluektov, O. G.; Paschenko, S. V.; Utschig, L. M.; Lakshmi, K. V.; Thurnauer, M. C. Bidirectional electron transfer in photosystem I. direct evidence from high-frequency time-resolved EPR spectroscopy J. Am. Chem. Soc. 2005, 127 (34) 11910-1
10. Li, Y.; van der Est, A.; Lucas, M. G.; Ramesh, V. M.; Gu, F.; Petrenko, A.; Lin, S.; Webber, A. N.; Rappaport, F.; Redding, K. Directing electron transfer within Photosystem I by breaking H-bonds in the cofactor branches Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (7) 2144-9
11. Byrdin, M.; Santabarbara, S.; Gu, F.; Fairclough, W. V.; Heathcote, P.; Redding, K.; Rappaport, F. Assignment of a kinetic component to electron transfer between iron-sulfur clusters F(X) and F(A/B) of Photosystem I Biochim. Biophys. Acta 2006, 1757 (11) 1529-38
12. Santabarbara, S.; Jasaitis, A.; Byrdin, M.; Gu, F.; Rappaport, F.; Redding, K. Additive effect of mutations affecting the rate of phylloquinone reoxidation and directionality of electron transfer within photosystem I Photochem. Photobiol. 2008, 84 (6) 1381-7
13. Jordan, P.; Fromme, P.; Witt, H. T.; Klukas, O.; Saenger, W.; Krauss, N. Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution Nature 2001, 411 (6840) 909-17
14. Ben-Shem, A.; Frolow, F.; Nelson, N. Crystal structure of plant photosystem I Nature 2003, 426, 630-5
15. Schlodder, E.; Falkenberg, K.; Gergeleit, M.; Brettel, K. Temperature dependence of forward and reverse electron transfer from A1l the reduced secondary electron acceptor in photosystem I Biochemistry 1998, 37 (26) 9466-76
16. Agalarov, R.; Brettel, K. Temperature dependence of biphasic forward electron transfer from the phylloquinone(s) A(1) in photosystem I: only the slower phase is activated Biochim. Biophys. Acta 2003, 1604 (1) 7-12
17. Ishikita, H.; Knapp, E. W. Redox potential of quinones in both electron transfer branches of photosystem I J. Biol. Chem. 2003
18. Karyagina, I.; Pushkar, Y.; Stehlik, D.; van der Est, A.; Ishikita, H.; Knapp, E. W.; Jagannathan, B.; Agalarov, R.; Golbeck, J. H. Contributions of the protein environment to the midpoint potentials of the A1 phylloquinones and the Fx iron-sulfur cluster in photosystem I Biochemistry 2007, 46 (38) 10804-16
19. Munge, B.; Das, S. K.; Ilagan, R.; Pendon, Z.; Yang, J.; Frank, H. A.; Rusling, J. F. Electron transfer reactions of redox cofactors in spinach photosystem I reaction center protein in lipid films on electrodes J. Am. Chem. Soc. 2003, 125 (41) 12457-63
20. Moser, C. C.; Dutton, P. L. Application of Marcus Theory to Photosystem I Electron Transfer. In Photosystem I: The Plastocyanin:Ferredoxin Oxidoreductase in Photosynthesis; Golbeck, J., Ed.; Kluwer Academic Publishers: Dordrecht, 2006; pp 583 - 594
21. Srinivasan, N.; Karyagina, I.; Bittl, R.; van der Est, A.; Golbeck, J. H. Role of the hydrogen bond from Leu722 to the A1A phylloquinone in photosystem I Biochemistry 2009, 48 (15) 3315-24
22. Li, Y.; Lucas, M.-G.; Konovalova, T.; Abbott, B.; MacMillan, F.; Petrenko, A.; Sivakumar, V.; Wang, R.; Hastings, G.; Gu, F.; van Tol, J.; Brunel, L.-C.; Timkovich, R.; Rappaport, F.; Redding, K. Mutation of the Putative Hydrogen-Bond Donor to P700 of Photosystem I Biochemistry 2004, 43 (39) 12634-12647
23. Redding, K.; MacMillan, F.; Leibl, W.; Brettel, K.; Rutherford, A. W.; Breton, J.; Rochaix, J.-D. A survey of conserved histidines in the photosystem 1: Methodology and analysis of the PsaB-H656L mutant. In Photosynthesis: Mechanisms and Effects; Garab, G., Ed.; Kluwer Academic Publishers: Dordrecht, 1998; Vol. 1; pp 591 - 594.
24. Harris, E. H. The Chlamydomonas sourcebook. A comprehensive guide to biology and laboratory use; Academic Press: San Diego, 1989; p 780.
25. Santabarbara, S.; Agostini, G.; Casazza, A. P.; Syme, C. D.; Heathcote, P.; Bohles, F.; Evans, M. C.; Jennings, R. C.; Carbonera, D. Chlorophyll triplet states associated with Photosystem I and Photosystem II in thylakoids of the green alga Chlamydomonas reinhardtii Biochim. Biophys. Acta 2007, 1767 (1) 88-105
26. Béal, D.; Rappaport, F.; Joliot, P. A new high-sensitivity 10-ns time-resolution spectrophotometric technique adapted to in vivo analysis of the photosynthetic apparatus Rev. Sci. Instrum. 1999, 70, 202-7
27. Carbonera, D.; Giacometti, G.; Agostini, G. FDMR of Carotenoids and Chlorophyll in Light-harvesting Complex II of Spinach Appl. Magn. Reson. 1992, 3, 859-872
28. Carbonera, D.; Collareta, P.; Giacometti, G. The P700 triplet state in an intact environment detected by ODMR. A well resolved triplet minus singlet spectrum Biochim. Biophys. Acta 1997, 1322 (2-3) 115-128
29. Santabarbara, S.; Bordignon, E.; Jennings, R. C.; Carbonera, D. Chlorophyll triplet states associated with photosystem II of thylakoids Biochemistry 2002, 41 (25) 8184-94
30. Marcus, R.; Sutin, N. Electron transfers in chemistry and biology Biochim. Biophys. Acta 1985, 811 (3) 265-322
31. DeVault, D. Quantum-Mechanical Tunnelling in Biological Systems; Cambridge University Press: Cambridge, 1984.
32. Hopfield, J. J. Electron Transfer Between Biological Molecules by Thermally Activated Tunneling Proc. Natl. Acad. Sci. U.S.A. 1974, 71 (9) 3640-3644
33. Moser, C. C.; Keske, J. M.; Warncke, K.; Farid, R. S.; Dutton, P. L. Nature of biological electron transfer Nature 1992, 355 (6363) 796-802
34. Redding, K.; MacMillan, F.; Leibl, W.; Brettel, K.; Hanley, J.; Rutherford, A. W.; Breton, J.; Rochaix, J. D. A systematic survey of conserved histidines in the core subunits of Photosystem I by site-directed mutagenesis reveals the likely axial ligands of P700 EMBO J. 1998, 17 (1) 50-60
35. Ramesh, V. M.; Guergova-Kuras, M.; Joliot, P.; Webber, A. N. Electron transfer from plastocyanin to the photosystem I reaction center in mutants with increased potential of the primary donor in Chlamydomonas reinhardtii Biochemistry 2002, 41 (50) 14652-14658
36. + by tightly bound plastocyanin in vivo Biochemistry 2009, 48 (43) 10457-66
37. Brettel, K. Electron transfer and arrangement of the redox cofactors in photosystem I Biochim. Biophys. Acta 1997, 1318, 322-373
38. Searle, G.; Schaafsma, T. Fluorescence Detected Magnetic Resonance of the Primary Donor and Inner Antenna Chlorophylls in Photosystem I Reaction Centres Proteins: Sign Inversion and Energy Transfer Photosyn. Res. 1992, 32, 193-206
39. Rappaport, F.; Diner, B. A.; Redding, K. Optical measurements of secondary electron transfer in Photosystem I. In Photosystem I: The Plastocyanin:Ferredoxin Oxidoreductase in Photosynthesis; Golbeck, J., Ed.; Kluwer Academic Publishers: Dordrecht, 2006; pp 223 - 244.
40. Redding, K.; van der Est, A.; The Directionality of Electron Transfer in Photosystem I In Photosystem I: The Plastocyanin:Ferredoxin Oxidoreductase in Photosynthesis; Golbeck, J., Ed.; Kluwer Academic Publishers: Dordrecht, 2006; pp 413 - 437.
41. Xu, W.; Chitnis, P. R.; Valieva, A.; van der Est, A.; Brettel, K.; Guergova-Kuras, M.; Pushkar, Y. N.; Zech, S. G.; Stehlik, D.; Shen, G.; Zybailov, B.; Golbeck, J. H. 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. 2003, 278 (30) 27876-87
42. Ali, K.; Santabarbara, S.; Heathcote, P.; Evans, M. C.; Purton, S. Bidirectional electron transfer in photosystem I replacement of the symmetry-breaking tryptophan close to the PsaB-bound phylloquinone A1B with a glycine residue alters the redox properties of A1B and blocks forward electron transfer at cryogenic temperatures Biochim. Biophys. Acta 2006, 1757 (12) 1623-33
43. Müller, M. G.; Niklas, J.; Lubitz, W.; Holzwarth, A. R. Ultrafast transient absoprtion studies on photosystem I reaction centers from Chlamydomonas reinhardtii I. A new interpretation of the energy trapping and early electron transfer steps in photosystem I Biophys. J. 2003, 85 (6) 3899-3922
44. Müller, M. G.; Slavov, C.; Luthra, R.; Redding, K. E.; Holzwarth, A. R. Independent initiation of primary electron transfer in the two branches of the photosystem I reaction center Proc. Natl. Acad. Sci. U.S.A. 2010, 107 (9) 4123-8
45. Srinivasan, N.; Karyagina, I.; Golbeck, J. H.; Stehlik, D., Structure-Function Correlations in the (A0 → A1 → FX) Electron Transfer Kinetics of the Phylloquinone (A1) Acceptor in Cyanobacterial Photosystem I. In Photosynthesis. Energy from the Sun: 14th International Congress on Photosynthesis; Allen, J. F.; Gantt, E.; Golbeck, J. H.; Osmond, B., Eds.; Springer: Dordrecht, The Netherlands, 2007; pp 207 - 210.
46. Nakamura, A.; Watanabe, T. Separation and determination of minor photosynthetic pigments by reversed-phase HPLC with minimal alteration of chlorophylls Anal. Sci. 2001, 17 (4) 503-8
47. Fairclough, W. V.; Forsyth, A.; Evans, M. C.; Rigby, S. E.; Purton, S.; Heathcote, P. Bidirectional electron transfer in photosystem I electron transfer on the PsaA side is not essential for phototrophic growth in Chlamydomonas Biochim. Biophys. Acta 2003, 1606 (1-3) 43-55