Hydrogen bond interactions of the pheophytin electron acceptor and its radical anion in photosystem II as revealed by fourier transform infrared difference spectroscopy

Biochemistry

Volumn 49, Issue 3, 2010, Pages 493-501

  Shibuya, Yuichi ^a   Takahashi, Ryouta ^a   Okubo, Tatsunori ^a   Suzuki, Hiroyuki ^a   Sugiura, Miwa ^b   Noguchi, Takumi ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b EHIME UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIONIC STATE; D1 PROTEIN; DENSITY FUNCTIONAL THEORY CALCULATIONS; DFT CALCULATION; DIFFERENCE SPECTROSCOPY; ELECTRON ACCEPTOR; ELECTRON TRANSFER; FOURIER TRANSFORM INFRARED; FOURIER TRANSFORM INFRARED DIFFERENCE SPECTROSCOPY; FREQUENCY SHIFT; FTIR; HYDROGEN BOND DONORS; HYDROGEN BOND INTERACTION; HYDROGEN-BOND EFFECT; PHOTO-REDUCTION; PHOTOPROTECTION MECHANISMS; PHOTOSYSTEM II; POTENTIAL CONTROL; PRIMARY ELECTRONS; PSII CORE COMPLEX; RADICAL ANIONS; REDOX POTENTIALS; SIDE CHAINS; SYNECHOCYSTIS; THERMOSYNECHOCOCCUS ELONGATUS;

ACETIC ACID; ACIDS; COMPLEXATION; DENSITY FUNCTIONAL THEORY; DYES; FOURIER TRANSFORM INFRARED SPECTROSCOPY; FREE RADICAL REACTIONS; HYDROGEN BONDS; IONS; PH EFFECTS; PROBABILITY DENSITY FUNCTION; SECONDARY BATTERIES; SULFUR COMPOUNDS;

HYDROGEN;

ACETAMIDE; ACETIC ACID; ANION; CARBON; GLUTAMINE; OXYGEN; PHEOPHYTIN;

ACCLIMATIZATION; ARTICLE; COMPLEX FORMATION; CYANOBACTERIUM; DENSITY FUNCTIONAL THEORY; ELECTRON TRANSPORT; HYDROGEN BOND; INFRARED SPECTROSCOPY; MOLECULAR INTERACTION; NONHUMAN; OXIDATION REDUCTION REACTION; PHOTOSYSTEM II; PRIORITY JOURNAL; SYNECHOCYSTIS; THERMOSYNECHOCOCCUS ELONGATUS;

ANIONS; CYANOBACTERIA; ELECTRON TRANSPORT; HYDROGEN BONDING; PHEOPHYTINS; PHOTOSYSTEM II PROTEIN COMPLEX; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

CYANOBACTERIA; SPINACIA OLERACEA; SYNECHOCYSTIS; THERMOSYNECHOCOCCUS ELONGATUS;

EID: 74949118292     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi9018829     Document Type: Article

References (48)

1. Nixon, P. J., Sarcina, M., and Diner, B. A. (2005) The D1 and D2 core proteins, in Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase (Wydrzynski, T., and Satoh, K., Eds.) pp 71-94, Springer, Dordrecht, The Netherlands.
2. Renger, G., and Holzwarth, A. R. (2005) Primary electron transfer, in Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase (Wydrzynski, T., and Satoh, K., Eds.) pp 139-175, Springer, Dordrecht, The Netherlands.
3. Hillier, W., and Messinger, J. (2005) Mechanism of photosynthetic oxygen production, in Photosystem II: The Light-Driven Water: Plastoquinone Oxidoreductase (Wydrzynski, T., and Satoh, K., Eds.) pp 567-608, Springer, Dordrecht, The Netherlands.
4. Petrouleas, V., and Crofts, A. R. (2005) The quinone iron acceptor complex, in Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase (Wydrzynski, T., and Satoh, K., Eds.) pp 177-206, Springer, Dordrecht, The Netherlands.
5. Giorgi,L.B., Nixon, P. J.,Merry, S.A. P., Joseph,D.M.,Durrant, J.R., Rivas, J. D., Barber, J., Porter,G., and Klug, D. R. (1996) Comparison of primary charge separation in the photosystem II reaction center complex isolated from wild-type and D1-130 mutants of the cyanobacterium Synechocystis PCC 6803. J. Biol. Chem. 271, 2093-2101.
6. Merry, S. A. P., Nixon, P. J., Barter, L. M. C., Schilstra, M., Porter, G., Barber, J., Durrant, J. R., and Klug, D. R. (1998) Modulation of quantumyield of primary radical pair formation in photosystem II by site-directed mutagenesis affecting radical cations and anions. Biochemistry 37, 17439-17447.
7. Cuni, A., Xiong, L., Sayre, R., Rappaport, F., and Lavergne, J. (2004) Modification of the pheophytin midpoint potential in photosystem II: Modulation of the quantum yield of charge separation and of charge recombination pathways. Phys. Chem. Chem. Phys. 6, 4825-4831.
8. Cser, K., and Vass, I. (2007) Radiative and non-radiative charge recombination pathways in photosystem II studied by thermoluminescence and chlorophyll fluorescence in the cyanobacterium Synechocystis 6803. Biochim. Biophys. Acta 1767, 233-243.
9. Rappaport, F., Guergova-Kuras, M., Nixon, P. J., Diner, B. A., and Lavergne, J. (2002) Kinetics and pathways of charge recombination in photosystem II. Biochemistry 41, 8518-8527.
10. Vass, I., and Cser, K. (2009) Janus-faced charge recombinations in photosystem II photoinhibition. Trends Plant Sci. 14, 200-205.
11. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J., and Iwata, S. (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831-1838.
12. Guskov, A., Kern, J., Gabdulkhakov, A., Broser, M., Zouni, A., and Saenger, W. (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat. Struct. Mol. Biol. 16, 334-342.
13. Kawakami, K., Umena, Y., Kamiya, N., and Shen, J.-R. (2009) Location of chloride and its possible functions in oxygen-evolving photosystem II revealed by X-ray crystallography. Proc. Natl. Acad. Sci. U.S.A. 106, 8567-8572.
14. Dorlet, P., Xiong, L., Sayre, R. T., and Un, S. (2001) High field EPR study of the pheophytin anion radical in wild type and D1-E130 mutants of photosystem II in Chlamydomonas reinhardtii. J. Biol. Chem. 276, 22313-22316.
15. Cser, K., and Vass, I. (2008) Regulation of photoprotection by non-radiative charge recombination in photosystem II, in Photosynthesis. Energy from the Sun (Allen, J. F., Gantt, E., Golbeck, J. H., and Osmond, B., Eds.) pp 47-50, Springer, Dordrecht, The Netherlands.
16. Kos, P. B., Deak, Z., Cheregi, O., and Vass, I. (2008) Differential regulation of psbA and psbD gene expression, and the role of the different D1 protein copies in the cyanobacterium Thermosynechococcus elongatus BP-1. Biochim. Biophys. Acta 1777, 74-83.
17. Loll, B., Broser, M., Kos, P. B., Kern, J., Biesiadka, J., Vass, I., Saenger, W., and Zouni, A. (2008) Modeling of variant copies of subunit D1 in the structure of photosystem II from Thermosynechococcus elongatus. Biol. Chem. 389, 609-617.
18. Svensson, B., Vass, I., and Styring, S. (1991) Sequence-analysis of the D1 and D2 reaction center proteins of photosystem II. Z. Naturforsch. 46c, 765-776.
19. Clarke, A. K., Soitamo, A., Gustafsson, P., and Oquist, G. (1993) Rapid interchange between two distinct forms of cyanobacterial photosystem II reaction-center protein D1 in response to photoinhibition. Proc. Natl. Acad. Sci. U.S.A. 90, 9973-9977.
20. Golden, S. S. (1995) Light-responsive gene-expression in cyanobacteria. J. Bacteriol. 177, 1651-1654.
21. Noguchi, T., and Berthomieu, C. (2005) Molecular analysis by vibrational spectroscopy, in Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase (Wydrzynski, T., and Satoh, K., Eds.) pp 367-387, Springer, Dordrecht, The Netherlands.
22. Noguchi, T. (2007) Light-induced FTIR difference spectroscopy as a powerful tool toward understanding the molecular mechanism of photosynthetic oxygen evolution. Photosynth. Res. 91, 59-69.
23. Berthomieu, C., and Hienerwadel, R. (2009) Fourier transform infrared (FTIR) spectroscopy. Photosynth. Res. 101, 157-170.
24. Tavitian, B. A., Nabedryk, E., Mäntele, W., and Breton, J. (1986) Light-induced Fourier transform infrared spectroscopic investigations of primary reactions in photosystem I and photosystem II. FEBS Lett. 201, 151-157.
25. Nabedryk, E., Andrianambinintsoa, S., Berger, G., Leonhard, M., Mäntele, W., and Breton, J. (1990) Characterization of bonding interactions of the intermediary electron-acceptor in the reaction center of photosystem II by FTIR spectroscopy. Biochim. Biophys. Acta 1016, 49-54.
26. Sugiura, M., and Inoue, Y. (1999) Highly purified thermo-stable oxygen-evolving photosystem II core complex from the thermophilic cyanobacterium Synechococcus elongatus having His-tagged CP43. Plant Cell Physiol. 40, 1219-1231.
27. Sugiura, M., Boussac, A., Noguchi, T., and Rappaport, F. (2008) Influence of histidine-198 of the D1 subunit on the properties of the primary electron donor, P680, of photosystem II in Thermosynechococcus elongatus. Biochim. Biophys. Acta 1777, 331-342.
28. Ono, T., and Inoue, Y. (1986) Effects of removal and reconstitution of the extrinsic 33, 24 and 16 kDa proteins on flash oxygen yield in photosystem II particles. Biochim. Biophys. Acta 850, 380-389.
29. Noguchi, T., and Inoue, Y. (1995) Molecular interactions of the redox-active accessory chlorophyll on the electron-donor side of photosystem II as studied by Fourier transform infrared spectroscopy. FEBS Lett. 370, 241-244.
30. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Montgomery, J. A., Jr., Vreven, T., Kudin, K. N., Burant, J. C., Millam, J. M., Iyengar, S. S., Tomasi, J., Barone, V., Mennucci, B., Cossi, M., Scalmani, G., Rega, N., Petersson, G. A., Nakatsuji, H., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Klene, M., Li, X., Knox, J. E., Hratchian, H. P., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C., Ochterski, J. W., Ayala, P. Y., Morokuma, K., Voth, G. A., Salvador, P., Dannenberg, J. J., Zakrzewski, V. G., Dapprich, S., Daniels, A. D., Strain,M. C., Farkas, O., Malick,D.K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Ortiz, J. V., Cui, Q., Baboul, A. G., Clifford, S., Cioslowski, J., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Gonzalez, C., and Pople, J. A. (2004) Gaussian 03, Revision C.02, Gaussian, Inc., Wallingford, CT.
31. Becke, A. D. (1993) Density-functional thermochemistry. III. The role of exact exchange. J. Chem. Phys. 98, 5648-5652.
32. Lee, C., Yang, W., and Parr, R. G. (1988) Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys. Rev. B 37, 785-789.
33. Trasatti, S. (1986) The absolute electrode potential: An explanatory note. Pure Appl. Chem. 58, 955-966.
34. Reiss, H., and Heller, A. (1985) The absolute potential of the standard hydrogen electrode: A new estimate. J. Phys. Chem. 89, 4207-4213.
35. Moënne-Loccoz, P., Robert, B., and Lutz, M. (1989) A resonance Raman characterization of the primary electron-acceptor in photosystem II. Biochemistry 28, 3641-3645.
36. Germano, M., Pascal, A., Shkuropatov, A. Y., Robert, B., Hoff, A. J., and van Gorkom, H. J. (2002) Pheophytin-protein interactions in photosystem II studied by resonance Raman spectroscopy of modified reaction centers. Biochemistry 41, 11449-11455.
37. Kazakova, A. A., Kisselev, B. A., and Kozlov, Y. N. (1989) Electrochemical reduction of pheophytin and its participation in the functioning of photosystem II. Bioelectrochem. Bioenerg. 21, 367-372.
38. Watanabe, T., and Kobayashi, M. (1991) Electrochemistry of chlorophylls, in Chlorophylls (Scheer, H., Ed.) pp 287-315, CRC Press, Boca Raton, FL.
39. Hasegawa, K., and Noguchi, T. (2005) Density functional theory calculations on the dielectric-constant dependence of the oxidation potential of chlorophyll: Implication for the high potential of P680 in photosystem II. Biochemistry 44, 8865-8872.
40. Heimdal, J., Jensen, K. P., Devarajan, A., and Ryde, U. (2007) The role of axial ligands for the structure and function of chlorophylls. J. Biol. Inorg. Chem. 12, 49-61.
41. Mehta, N., and Datta, S. N. (2007) Theoretical determination of the standard reduction potentials of pheophytin-a in N,N-dimethyl formamide and membrane. J. Phys. Chem. B 111, 7210-7217.
42. O'Malley, P. J. (2000) Density functional predicted geometries and vibrational frequencies of the neutral and anion-radical form of pheophytin: Relevance to electron transfer in photosynthetic reaction centres. Chem. Phys. Lett. 331, 78-82.
43. Takei, K., Takahashi, R., and Noguchi, T. (2008) Correlation between the hydrogen-bond structures and the C=O stretching frequencies of carboxylic acids as studied by density functional theory calculations: Theoretical basis for interpretation of infrared bands of carboxylic groups in proteins. J. Phys. Chem. B 112, 6725-6731.
44. A in reaction centers from Rhodopseudomonas viridis revealed by Fourier transform infrared spectroscopy and site-directed mutagenesis. Biochemistry 38, 11541-11552.
45. Klimov, V. V., Allakhverdiev, S. I., Demeter, S., and Krasnovskii, A. A. (1979) Photoreduction of pheophytin in photosystem 2 of chloroplasts with respect to redox potential of the medium. Dokl. Akad. Nauk SSSR 249, 227-230.
46. Rutherford, A. W., Mullet, J. E., and Crofts, A. R. (1981) Measurement of the midpoint potential of the pheophytin acceptor of photosystem II. FEBS Lett. 123, 235-237.
47. Kato, Y., Sugiura, M., Oda, A., and Watanabe, T. (2009) Spectroelectrochemical determination of the redox potential of pheophytin a, the primary electron acceptor in photosystem II. Proc. Natl. Acad. Sci. U.S.A. 106, 17365-17370.
48. Ishikita, H., Biesiadka, J., Loll, B., Saenger, W., and Knapp, E. W. (2006) Cationic state of accessory chlorophyll and electron transfer through pheophytin to plastoquinone in photosystem II. Angew. Chem. 45, 1964-1965.