Cofactors involved in light-driven charge separation in photosystem i identified by subpicosecond infrared spectroscopy

Biochemistry

Volumn 50, Issue 4, 2011, Pages 480-490

  Donato, Mariangela Di ^a   Stahl, Andreas D ^a   Van Stokkum, Ivo H M ^a   Grondelle, Rienk Van ^a   Groot, Marie Louise ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHARGE SEPARATION PROCESS; CHARGE SEPARATIONS; CHEMICAL ENERGY; CHLOROPHYLL A; COFACTORS; ELECTRON DONORS; EXCITATION CONDITIONS; FEMTOSECONDS; HIGH SPECIFICITY; INFRARED REGIONS; IR SIGNATURES; MIDINFRARED; PHOTOSYSTEM I; PHOTOSYSTEM I TRIMER; PRIMARY ELECTRON DONOR; PRIMARY RADICALS; PROBE SPECTROSCOPY; RADICAL PAIR; RED PIGMENTS; REDOX STATE; SECONDARY ELECTRONS; SUBPICOSECOND; SUBPICOSECOND TIME SCALE; SYNECHOCOCCUS ELONGATUS; TIME CONSTANTS; TIME RESOLUTION; ULTRA-FAST;

CHARGE TRANSFER; DIMERS; INFRARED SPECTROSCOPY; IODINE; ION EXCHANGE; POSITIVE IONS; SOLAR ENERGY;

CHLOROPHYLL;

CHLOROPHYLL; PIGMENT;

ARTICLE; CHEMICAL STRUCTURE; ELECTRON TRANSPORT; INFRARED SPECTROSCOPY; MOLECULAR DYNAMICS; NONHUMAN; OXIDATION; OXIDATION REDUCTION STATE; PHOTOSYSTEM I; PRIORITY JOURNAL; SEPARATION TECHNIQUE; SYNECHOCOCCUS ELONGATUS;

BACTERIAL PROTEINS; CHLOROPHYLL; ELECTRON TRANSPORT; PHOTOSYSTEM I PROTEIN COMPLEX; PIGMENTS, BIOLOGICAL; SPECTROPHOTOMETRY, INFRARED; SPINACIA OLERACEA; STATIC ELECTRICITY; SUNLIGHT; SYNECHOCOCCUS; TIME FACTORS;

SYNECHOCOCCUS ELONGATUS;

EID: 79952095403     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101565w     Document Type: Article

References (67)

1. Fromme, P., Jordan, P., and Krauss, N. (2001) Structure of photosystem I. Biochim. Biophys. Acta 1507, 5-31. (Pubitemid 33001510)
2. Jordan, P., Fromme, P., Witt, H. T., Klukas, O., Saenger, W., and Krausz, N. (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Angstrom resolution. Nature 411, 909-917. (Pubitemid 32601481)
3. Ali, K., Santabarbara, S., Heathcote, P., Evans, M. C. W., and Purton, S. (2006) Bidirectional electron transfer in photosystem I: Replacement of the symmetry-breaking tryptophan close to the PsaBbound phylloquinone (A1B) with a glycine residue alters the redox properties of A1B and blocks forward electron transfer at cryogenic temperatures. Biochim. Biophys. Acta 1757, 1623-1633. (Pubitemid 44838475)
4. Brettel, K., and Leibl, W. (2001) Electron transfer in photosystem I. Biochim. Biophys. Acta 1507, 100-114. (Pubitemid 33001515)
5. Dashdorj, N., Xu, W., Cohen, R. O., Golbeck, J. H., and Savikhin, S. (2005) Asymmetric Electron Transfer in Cyanobacterial Photosystem I: Charge Separation and Secondary Electron Transfer Dynamics of Mutations Near the Primary Electron Acceptor A0. Biophys. J. 88, 1238-1249. (Pubitemid 40975951)
6. Fairclough, W. V., Forsyth, A., Evans, M. C. W., Rigby, S. E. J., Purton, S., and Heathcote, P. (2003) Bidirectional electron transfer in photosystem I: Electron transfer on the PsaA side is not essential for phototrophic growth in Chlamydomonas. Biochim. Biophys. Acta 1606, 43-55. (Pubitemid 37267869)
7. 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. U.S.A. 98, 4437-4442. (Pubitemid 32294995)
8. Ivashin, N., and Larsson, S. (2003) Electron transfer pathways in photosystem I reaction centers. Chem. Phys. Lett. 375, 383-387. (Pubitemid 36776861)
9. Poluektov, O. G., Paschenko, S. V., Utschig, L. M., Lakshmi, K. V., and Thurnauer, M. C. (2005) Bidirectional Electron Transfer in Photosystem I: Direct Evidence from High-Frequency Time-Resolved EPR Spectroscopy. J. Am. Chem. Soc. 127, 11910-11911. (Pubitemid 41233696)
10. 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., and Golbeck, J. H. (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, 27876-27887. (Pubitemid 36899980)
11. Müller, M. G., Slavov, C., Luthra, R., Redding, K. E., and Holzwarth, A. R. (2010) Independent initiation of primary electron transfer in the two branches of the photosystem I reaction center. Proc. Natl. Acad. Sci. U.S.A. 107, 4123-4128.
12. Hastings, G., Reed, L. J., Lin, S., and Blankenship, R. E. (1995) Excited state dynamics in photosystem I: Effects of detergent and excitation wavelength. Biophys. J. 69, 2044-2055.
13. Bender, S. L., and Barry, B. A. (2008) Light-Induced Dynamics in Photosystem I Electron Transfer. Biophys. J. 95, 3927-3934.
14. Damjanovic, A., Vaswani, H. M., Fromme, P., and Fleming, G. R. (2002) Chlorophyll Excitations in Photosystem I of Synechococcus elongatus. J. Phys. Chem. B 106, 10251-10262. (Pubitemid 35382730)
15. Gobets, B., and van Grondelle, R. (2001) Energy transfer and trapping in photosystem I. Biochim. Biophys. Acta 1507, 80-99. (Pubitemid 33001514)
16. Gobets, B., van Stokkum, I.H. M., Ruogner, M., Kruip, J., Schlodder, E., Karapetyan, N. V., Dekker, J. P., and van Grondelle, R. (2001) Time-Resolved Fluorescence Emission Measurements of Photosystem I Particles of Various Cyanobacteria: A Unified Compartmental Model. Biophys. J. 81, 407-424. (Pubitemid 32605980)
17. Holzwarth, A. R., Muller, M. G., Niklas, J., and Lubitz, W. (2006) Ultrafast Transient Absorption Studies on Photosystem I Reaction Centers from Chlamydomonas reinhardtii. 2: Mutations near the P700 Reaction Center Chlorophylls Provide New Insight into the Nature of the Primary Electron Donor. Biophys. J. 90, 552-565.
18. Kumazaki, S., Ikegami, I., Furusawa, H., Yasuda, S., and Yoshihara, K. (2001) Observation of the Excited State of the Primary Electron Donor Chlorophyll (P700) and the Ultrafast Charge Separation in the Spinach Photosystem I Reaction Center. J. Phys. Chem. B 105, 1093-1099.
19. Slavov, C., El-Mohsnawy, E., Rogner, M., and Holzwarth, A. R. (2009) Trapping kinetics in isolated cyanobacterial PS I complexes. Chem. Phys. 357, 163-170.
20. Vaswani, H. M., Stenger, J., Fromme, P., and Fleming, G. R. (2006) One- and Two-Color Photon Echo Peak Shift Studies of Photosystem I. J. Phys. Chem. B 110, 26303-26312. (Pubitemid 46133352)
21. Muller, M. G., Niklas, J., Lubitz, W., and Holzwarth, A. R. (2003) Ultrafast Transient Absorption Studies on Photosystem I Reaction Centers from Chlamydomonas reinhardtii. 1. A New Interpretation of the Energy Trapping and Early Electron Transfer Steps in Photosystem I. Biophys. J. 85, 3899-3922. (Pubitemid 37490299)
22. Gibasiewicz, K., Ramesh, V. M., Melkozernov, A. N., Lin, S., Woodbury, N. W., Blankenship, R. E., and Webber, A. N. (2001) Excitation Dynamics in the Core Antenna of PS I from Chlamydomonas reinhardtii CC 2696 at Room Temperature. J. Phys. Chem. B 105, 11498-11506. (Pubitemid 35338451)
23. Melkozernov, A. N., Lin, S., and Blankenship, R. E. (2000) Excitation Dynamics and Heterogeneity of Energy Equilibration in the Core Antenna of Photosystem I from the Cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 39, 1489-1498. (Pubitemid 30090719)
24. Melkozernov, A. N., Schmid, V. H. R., Lin, S., Paulsen, H., and Blankenship, R. E. (2002) Excitation Energy Transfer in the Lhca1 Subunit of LHC I-730 Peripheral Antenna of Photosystem I. J. Phys. Chem. B 106, 4313-4317. (Pubitemid 35290167)
25. Savikhin, S., Xu, W., Martinsson, P., Chitnis, P. R., and Struve, W. S. (2001) Kinetics of Charge Separation and A0 to A1 Electron Transfer in Photosystem I Reaction Centers. Biochemistry 40, 9282-9290. (Pubitemid 32730049)
26. Gobets, B., van Stokkum, I.H. M., van Mourik, F., Dekker, J. P., and van Grondelle, R. (2003) Excitation Wavelength Dependence of the Fluorescence Kinetics in Photosystem I Particles from Synechocystis PCC 6803 and Synechococcus elongatus. Biophys. J. 85, 3883-3898. (Pubitemid 37490298)
27. Croce, R., Dorra, D., Holzwarth, A. R., and Jennings, R. C. (2000) Fluorescence Decay and Spectral Evolution in Intact Photosystem I of Higher Plants. Biochemistry 39, 6341-6348. (Pubitemid 30347138)
28. Nabedryk, E., Allen, J. P., Taguchi, A. K. W., Williams, J. C., Woodbury, N. W., and Breton, J. (1993) Fourier transform infrared study of the primary electron donor in chromatophores of Rhodobacter sphaeroides with reaction centers genetically modified at residues M160 and L131. Biochemistry 32, 13879-13885. (Pubitemid 24018239)
29. Pawlowicz, N. P., van Grondelle, R., van Stokkum, I. H. M., Breton, J., Jones, M. R., and Groot, M. L. (2008) Identification of the First Steps in Charge Separation in Bacterial Photosynthetic Reaction Centers of Rhodobacter sphaeroides by Ultrafast Mid-Infrared Spectroscopy: Electron Transfer and Protein Dynamics. Biophys. J. 95, 1268-1284.
30. Maiti, S., Walker, G. C., Cowen, B. R., Pippenger, R., Moser, C. C., Dutton, P. L., and Hochstrasser, R. M. (1994) Femtosecond coherent transient infrared spectroscopy of reaction centers from Rhodobacter sphaeroides. Proc. Natl. Acad. Sci. U.S.A. 91, 10360-10364. (Pubitemid 24328996)
31. Hamm, P., and Zinth, W. (1995) Ultrafast initial reaction in bacterial photosynthesis revealed by femtosecond infrared spectroscopy. J. Phys. Chem. 99, 13537-13544.
32. Groot, M. L., Pawlowicz, N. P., van Wilderen, L. J. G. W., Breton, J., van Stokkum, I. H. M., and van Grondelle, R. (2005) Initial electron donor and acceptor in isolated Photosystem II reaction centers identified with femtosecond mid-IR spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 102, 13087-13092. (Pubitemid 41324983)
33. Di Donato, M., Cohen, R. O., Diner, B. A., Breton, J., van Grondelle, R., and Groot, M. L. (2008) Primary Charge Separation in the Photosystem II Core from Synechocystis: A Comparison of Femtosecond Visible/Midinfrared Pump-Probe Spectra of Wild-Type and Two P680 Mutants. Biophys. J. 94, 4783-4795.
34. Romero, E., Mozzo, M., van Stokkum, I. H. M., Dekker, J. P., van Grondelle, R., and Croce, R. (2009) The Origin of the Low-Energy Form of Photosystem I Light-Harvesting Complex Lhca4: Mixing of the Lowest Exciton with a Charge-Transfer State. Biophys. J. 96, L35- L37.
35. Frese, R. N., Palacios, M. A., Azzizi, A., van Stokkum, I. H. M., Kruip, J., Rogner, M., Karapetyan, N. V., Schlodder, E., van Grondelle, R., and Dekker, J. P. (2002) Electric field effects on red chlorophylls, β-carotenes and P700 in cyanobacterial Photosystem I complexes. Biochim. Biophys. Acta 1554, 180-191. (Pubitemid 34874934)
36. Giera, W., Ramesh, V. M., Webber, A. N., van Stokkum, I., van Grondelle, R., and Gibasiewicz, K. (2010) Effect of the P700 preoxidation and point mutations near A0 on the reversibility of the primary charge separation in Photosystem I from Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1797, 106-112.
37. Fromme, P., and Witt, H. T. (1998) Improved isolation and crystallization of photosystem I for structural analysis. Biochim. Biophys. Acta 1365, 175-184. (Pubitemid 29359255)
38. van Stokkum, I. H. M., Larsen, D. S., and van Grondelle, R. (2004) Global and target analysis of time-resolved spectra. Biochim. Biophys. Acta 1657, 82-104. (Pubitemid 38952870)
39. Closs, G. L., Katz, J. J., Pennington, F. C., Thomas, M. R., and Strain, H. H. (1963) Nuclear Magnetic Resonance Spectra and Molecular Association of Chlorophylls a and b, Methyl Chlorophyllides, Pheophytins, and Methyl Pheophorbides. J. Am. Chem. Soc. 85, 3809-3821.
40. Groot, M. L., Breton, J., van Wilderen, L. J. G. W., Dekker, J. P., and van Grondelle, R. (2004) Femtosecond Visible/Visible and Visible/ Mid-IR Pump-Probe Study of the Photosystem II Core Antenna Complex CP47. J. Phys. Chem. B 108, 8001-8006.
41. Di Donato, M., van Grondelle, R., van Stokkum, I. H. M., and Groot, M. L. (2007) Excitation Energy Transfer in the Photosystem II Core Antenna Complex CP43 Studied by Femtosecond Visible/ Visible and Visible/Mid-Infrared Pump Probe Spectroscopy. J. Phys. Chem. B 111, 7345-7352. (Pubitemid 47152522)
42. Noguchi, T., Tomo, T., and Inoue, Y. (1998) Fourier Transform Infrared Study of the Cation Radical of P680 in the Photosystem II Reaction Center: Evidence for Charge Delocalization on the Chlorophyll Dimer. Biochemistry 37, 13614-13625. (Pubitemid 28455536)
43. Barth, A. (2007) Infrared spectroscopy of proteins. Biochim. Biophys. Acta 1767, 1073-1101. (Pubitemid 47313388)
44. Noguchi, T., Mitsuka, T., and Inoue, Y. (1994) Fourier transform infrared spectrum of the radical cation of Β-carotene photoinduced in photosystem II. FEBS Lett. 356, 179-182. (Pubitemid 24376966)
45. Mantele, W. G., Wollenweber, A. M., Nabedryk, E., and Breton, J. (1988) Infrared spectroelectrochemistry of bacteriochlorophylls and bacteriopheophytins: Implications for the binding of the pigments in the reaction center from photosynthetic bacteria. Proc. Natl. Acad. Sci. U.S.A. 85, 8468-8472.
46. Hartwich, G., Geskes, C., Scheer, H., Heinze, J., and Maentele, W. (1995) Fourier transform infrared spectroscopy of electrogenerated anions and cations of metal-substituted bacteriochlorophyll a. J. Am. Chem. Soc. 117, 7784-7790.
47. Shelaev, I. V., Gostev, F. E., Mamedov, M. D., Sarkisov, O. M., Nadtochenko, V. A., Shuvalov, V. A., and Semenov, A. Y. (2010) Femtosecond primary charge separation in Synechocystis sp. PCC 6803 photosystem I. Biochim. Biophys. Acta 1797, 1410-1420.
48. Nabedryk, E., Robles, S. J., Goldman, E., Youvan, D. C., and Breton, J. (1992) Probing the primary donor environment in the histidineM200 to leucine and histidineL173 to leucine heterodimer mutants of Rhodobacter capsulatus by light-induced Fourier transform infrared difference spectroscopy. Biochemistry 31, 10852-10858.
49. Pawlowicz, N. P., Groot, M. L., van Stokkum, I. H. M., Breton, J., and van Grondelle, R. (2007) Charge Separation and Energy Transfer in the Photosystem II Core Complex Studied by Femtosecond Midinfrared Spectroscopy. Biophys. J. 93, 2732-2742. (Pubitemid 47607810)
50. Groot, M. L., Peterman, E. J., van Kan, P. J., van Stokkum, I. H., Dekker, J. P., and van Grondelle, R. (1994) Temperature-dependent triplet and fluorescence quantum yields of the photosystem II reaction center described in a thermodynamic model. Biophys. J. 67, 318-330. (Pubitemid 24197897)
51. Woodbury, N. W. T., and Parson, W. W. (1984) Nanosecond fluorescence from isolated photosynthetic reaction centers of Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta 767, 345-361. (Pubitemid 15218680)
52. Breton, J. (2001) Fourier transform infrared spectroscopy of primary electron donors in type I photosynthetic reaction centers. Biochim. Biophys. Acta 1507, 180-193. (Pubitemid 33001519)
53. Palsson, L.-O., Flemming, C., Gobets, B., van Grondelle, R., Dekker, J. P., and Schlodder, E. (1998) Energy Transfer and Charge Separation in Photosystem I: P700 Oxidation Upon Selective Excitation of the Long-Wavelength Antenna Chlorophylls of Synechococcus elongatus. Biophys. J. 74, 2611-2622. (Pubitemid 28225255)
54. de Weerd, F. L., Dekker, J. P., and van Grondelle, R. (2003) Dynamics of β-Carotene-to-Chlorophyll Singlet Energy Transfer in the Core of Photosystem II. J. Phys. Chem. B 107, 6214-6220.
55. de Weerd, F. L., Kennis, J. T. M., Dekker, J. P., and van Grondelle, R. (2003) β-Carotene to Chlorophyll Singlet Energy Transfer in the Photosystem I Core of Synechococcus elongatus Proceeds via the β-Carotene S2 and S1 States. J. Phys. Chem. B 107, 5995-6002.
56. Croce, R., Chojnicka, A., Morosinotto, T., Ihalainen, J. A., van Mourik, F., Dekker, J. P., Bassi, R., and van Grondelle, R. (2007) The Low-Energy Forms of Photosystem I Light-Harvesting Complexes: Spectroscopic Properties and Pigment-Pigment Interaction Characteristics. Biophys. J. 93, 2418-2428. (Pubitemid 47511142)
57. Sytina, O. A., van Stokkum, I. H. M., Heyes, D. J., Hunter, C. N., van Grondelle, R., and Groot, M. L. (2010) Protochlorophyllide Excited- State Dynamics in Organic Solvents Studied by Time-Resolved Visible and Mid-Infrared Spectroscopy. J. Phys. Chem. B 114, 4335-4344.
58. Wilson, A. L., Punginelli, C., Gall, A., Bonetti, C., Alexandre, M., Routaboul, J.-M., Kerfeld, C. A., van Grondelle, R., Robert, B., Kennis, J. T. M., and Kirilovsky, D. (2008) A photoactive carotenoid protein acting as light intensity sensor. Proc. Natl. Acad. Sci. U.S.A. 105, 12075-12080.
59. Hughes, J. L., Smith, P., Pace, R., and Krausz, E. (2006) Charge separation in photosystem II core complexes induced by 690-730 nm excitation at 1.7 K. Biochim. Biophys. Acta 1757, 841-851. (Pubitemid 44142424)
60. Van Brederode, M. E., Jones, M. R., Van Mourik, F., Van Stokkum, I. H. M., and Van Grondelle, R. (1997) A New Pathway for Transmembrane Electron Transfer in Photosynthetic Reaction Centers of Rhodobacter sphaeroides Not Involving the Excited Special Pair. Biochemistry 36, 6855-6861. (Pubitemid 27258097)
61. van Brederode, M. E., van Mourik, F., van Stokkum, I. H. M., Jones, M. R., and van Grondelle, R. (1999) Multiple pathways for ultrafast transduction of light energy in the photosynthetic reaction center of Rhodobacter sphaeroides. Proc. Natl. Acad. Sci. U.S.A. 96, 2054-2059. (Pubitemid 29117866)
62. Holzwarth, A. R., Muller, M. G., Reus, M., Nowaczyk, M., Sander, J., and Ragner, M. (2006) Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: Pheophytin is the primary electron acceptor. Proc. Natl. Acad. Sci. U.S.A. 103, 6895-6900.
63. Sivakumar, V., Wang, R., and Hastings, G. (2005) A1 Reduction in Intact Cyanobacterial Photosystem I Particles Studied by Time- Resolved Step-Scan Fourier Transform Infrared Difference Spectroscopy and Isotope Labeling. Biochemistry 44, 1880-1893. (Pubitemid 40223619)
64. Groot, M. L., Pawlowicz, N. P., van Wilderen, L. J. G. W., Breton, J., van Stokkum, I. H. M., and van Grondelle, R. (2005) Initial electron donor and acceptor in isolated Photosystem II reaction centers identified with femtosecond mid-IR spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 102, 13087-13092. (Pubitemid 41324983)
65. Burie, J.-R., Boussac, A., Boullais, C., Berger, G., Mattioli, T., Mioskowski, C., Nabedryk, E., and Breton, J. (1995) FTIR Spectroscopy of UV-Generated Quinone Radicals: Evidence for an Intramolecular Hydrogen Atom Transfer in Ubiquinone, Naphthoquinone, and Plastoquinone. J. Phys. Chem. 99, 4059-4070.
66. 13C-Labeled Ubiquinones and Vitamin K1. Biochemistry 33, 4953-4965. (Pubitemid 24158447)
67. Renger, T., and Schlodder, E. (2010) Primary Photophysical Processes in Photosystem II: Bridging the Gap between Crystal Structure and Optical Spectra. ChemPhysChem 11, 1141-1153.