Abstract
Results of Density Functional Theory (DFT) theoretical investigations, which use a model tyrosyl (Tyr) radical and tyrosyl-histidine (Tyr-His) complex to mimick the Y ·D radical in Photosystem II (PSII) are presented and compared to experimental results from 15N Electron-Nuclear Double Resonance spectroscopy (ENDOR) studies of the τ nitrogen coupling from His-189 in the PSII Tyr-His complex. The DFT calculations are performed using an optimized geometry of the tyrosine radical and Tyr-His complex. The conformational space of the Tyr-His tandem is explored by varying the relative geometry of the two components; relevant parameters, such as the spin distribution on the phenoxy-ring carbons of the Tyr radical and the EPR hyperfine tensors, are calculated at each geometry and compared with the available experimental data. The isotropic 15N-ENDOR signal arising from spin delocalization on the His hydrogen-bonded to the PSII tyrosine radical is analyzed in terms of the DFT obtained parameters. The calculations of the g tensor using the Gauge Independent Atomic Orbital (GIAO) approach are presented and the influence of the geometry of the Tyr-His complex on the deviation of the g-tensor elements from the free electron values is discussed.
Similar content being viewed by others
References
R. J. Debus, Biochim. Biophys. Acta 1503, 164 (2001).
B. A. Diner, Biochim. Biophys. Acta 1503, 147 (2001).
B. A. Diner and G. T. Babcock, Adv. Photosynth. 4, 213 (1996).
K. N. Ferreira, T. M. Iverson, K. Maghlaoui, J. Barber and S. Iwata, Science 303, 1831 (2004).
N. Kamiya and J.-R. Shen, Proc. Natl. Acad. Sci. USA 100, 98 (2003).
B. Loll, J. Kern, W. Saenger, A. Zouni and J. Biesiadka, Nature 438, 1040 (2005).
A. Zouni, H. T. Witt, J. Kern, P. Fromme, N. Krauss, W. Saenger and P. Orth, Nature 409, 739 (2001).
P. J. O’Malley and A. J. MacFarlane, Theochem 96, 293 (1992).
P. J. O’Malley, A. J. MacFarlane, S. E. J. Rigby and J. H. A. Nugent, Biochim. Biophys. Acta 1232, 175 (1995).
Y. Qin and R. A. Wheeler, J. Am. Chem. Soc. 117, 6083 (1995).
S. Un, M. Atta, M. Fontecave and A. W. Rutherford, J. Am. Chem. Soc. 117, 10713 (1995).
F. Himo, A. Graeslund and L. A. Eriksson, Biophys. J. 72, 1556 (1997).
M. J. Lundqvist and L. A. Eriksson, J. Phys. Chem. B 104, 848 (2000).
J.-P. Piquemal, J. Maddaluno, B. Silvia and C. Giessenr-Prettre, New J. Chem. 27, 909 (2003).
M. Engstroem, F. Himo, A. Graeslund, B. Minaev, O. Vahtras and H. Agren, J. Phys. Chem. A 104, 5149 (2000).
A. Ivancich, T. A. Mattioli and S. Un, J. Am. Chem. Soc. 121, 5743 (1999).
M. Kaupp, T. Gress, R. Reviakine, O. L. Malkina and V. G. Malkin, J. Phys. Chem. B 107, 331 (2003).
O. L. Malkina, J. Vaara, B. Schimmelpfennig, M. Munzarova, V. G. Malkin and M. Kaupp, J. Am. Chem. Soc. 122, 9206 (2000).
E. Langella, R. Improta and V. Barone, J. Am. Chem. Soc. 124, 11531 (2002).
Alia, B. Hulsebosch, H. J. van Gorkom, J. Raap, J. Lugtenburg, J. Matysik, H. J. M. de Groot and P. Gast, Chem. Phys. 294, 459 (2003).
C. T. Farrar, G. J. Gerfen, R. G. Griffin, D. A. Force and R. D. Britt, J. Phys. Chem. B 101, 6634 (1997).
R. J. Hulsebosch, J. S. van den Brink, S. A. M. Nieuwenhuis, P. Gast, J. Raap, J. Lugtenburg and A. J. Hoff, J. Am. Chem. Soc. 119, 8685 (1997).
I. Ayala, K. Range, D. York and B. A. Barry, J. Am. Chem. Soc. 124, 5496 (2002).
P. J. O’Malley, J. Am. Chem. Soc. 120, 11732 (1998).
Y.-N. Wang and L. A. Eriksson, Int. J. Quant. Chem. 83, 220 (2001).
P. Varnai and W. G. Richards, Int. J. Quant. Chem. 84, 276 (2001).
M. R. A. Blomberg, P. E. M. Siegbahn, S. Styring, G. T. Babcock, B. Aakermark and P. Korall, J. Am. Chem. Soc. 119, 8285 (1997).
A. M. Boulet, E. D. Walter, D. A. Schwartz, G. J. Gerfen, P. R. Callis and D. J. Singel, Chem. Phys. Lett. 331, 108 (2000).
M. Engstrom, F. Himo and H. Agren, Chem. Phys. Lett. 319, 191 (2000).
K. E. Wise, J. B. Pate and R. A. Wheeler, J. Phys. Chem. B 103, 4764 (1999).
R. G. Evelo, A. J. Hoff, S. A. Dikanov and A. M. Tyryshkin, Chem. Phys. Lett. 161, 479 (1989).
W. T. Dixon and D. Murphy, J. Chem. Soc., Faraday Trans. 2 72, 1221 (1976).
P. Coppens, Y. Abramov, M. Carducci, B. Korjov, I. Novozhilova, C. Alhambra and M. R. Pressprich, J. Am. Chem. Soc. 121, 2585 (1999).
M. J. Frisch, G. W. Trucks, H. B. Schlegel, G. E. Scuseria, M. A. Robb, J. R. Cheeseman, J. A. Montgomery Jr., T. Vreven, K. N. Kudin, J. C. Burant, J. M. Millam, S. S. Iyengar, J. Tomasi, V. Barone, B. Mennucci, M. Cossi, G. Scalmani, N. Rega, G. A. Petersson, H. Nakatsuji, M. Hada, M. Ehara, K. Toyota, R. Fukuda, J. Hasegawa, M. Ishida, T. Nakajima, Y. Honda, O. Kitao, H. Nakai, M. Klene, X. Li, J. E. Knox, H. P. Hratchian, J. B. Cross, C. Adamo, J. Jaramillo, R. Gomperts, R. E. Stratmann, O. Yazyev, A. J. Austin, R. Cammi, C. Pomelli, J. W. Ochterski, P. Y. Ayala, K. Morokuma, G. A. Voth, P. Salvador, J. J. Dannenberg, V. G. Zakrzewski, S. Dapprich, A. D. Daniels, M. C. Strain, O. Farkas, D. K. Malick, A. D. Rabuck, K. Raghavachari, J. B. Foresman, J. V. Ortiz, Q. Cui, A. G. Baboul, S. Clifford, J. Cioslowski, B. B. Stefanov, G. Liu, A. Liashenko, P. Piskorz, I. Komaromi, R. L. Martin, D. J. Fox, T. Keith, M. A. Al-Laham, C. Y. Peng, A. Nanayakkara, M. Challacombe, P. M. W. Gill, B. Johnson, W. Chen, M. W. Wong, C. Gonzalez and J. A. Pople, R. A. Gaussian 03. Gaussian, Pittsburgh, PA (2003).
P. J. O’Malley, Chem. Phys. Lett. 291, 367 (1998).
J. Gauss, K. Ruud and T. Helgaker, J. Chem. Phys. 105, 2804 (1996).
E. J. Baerends, J. A. Autschbach, A. Bérces, C. Bo, P. M. Boerrigter, L. Cavallo, D. P. Chong, L. Deng, R. M. Dickson, D. E. Ellis, L. Fan, T. H. Fischer, C. Fonseca Guerra, S. J. A. van Gisbergen, J. A. Groeneveld, O. V. Gritsenko, M. Grüning, F. E. Harris, P. van den Hoek, H. Jacobsen, G. van Kessel, F. Kootstra, E. van Lenthe, V. P. Osinga, S. Patchkovskii, P. H. T. Philipsen, D. Post, C. C. Pye, W. Ravenek, P. Ros, P. R. T. Schipper, G. Schreckenbach, J. G. Snijders, M. Sola, M. Swart, D. Swerhone, G. te Velde, P. Vernooijs, L. Versluis, O. Visser, E. van Wezenbeek, G. Wiesenekker, S. K. Wolff, T. K. Woo and T. Ziegler, ADF2002.03. Theoretical Chemistry, Vrije Universiteit, Amsterdam (2003). Available online at http://www.scm.com
B. A. Barry, M. K. el-Deeb, P. O. Sandusky and G. T. Babcock, J. Biol. Chem. 265, 20139 (1990).
S. A. M. Nieuwenhuis, R. J. Hulsebosch, J. Raap, P. Gast, J. Lugtenburg and A. J. Hoff, J. Am. Chem. Soc. 120, 829 (1998).
D. A. Svistunenko, J. Dunne, M. Fryer, P. Nicholls, B. J. Reeder, M. T. Wilson, M. G. Bigotti, F. Cutruzzola and C. E. Cooper, Biophys. J. 83, 2845 (2002).
C. Tommos, C. Madsen, S. Styring and W. Vermaas, Biochemistry 33, 11805 (1994).
R. de Wijn and H. J. van Gorkom, Biochim. Biophys. Acta 1553, 302 (2002).
R. W. Fessenden and R. H. Schuler, J. Chem. Phys. 39, 2147 (1963).
G. Bar, M. Bennati, H. H. Nguyen, J. Ge, J. A. Stubbe and R. G. Griffin, J. Am. Chem. Soc. 123, 3569 (2001).
P. Faller, C. Goussias, A. W. Rutherford and S. Un, Proc. Natl. Acad. Sci. USA 100, 8732 (2003).
F. Dole, B. A. Diner, C. W. Hoganson, G. T. Babcock and R. D. Britt, J. Am. Chem. Soc. 119, 11540 (1997).
K. Warncke, G. T. Babcock and J. McCracken, J. Am. Chem. Soc. 116, 7332 (1994).
S. E. J. Rigby, J. H. A. Nugent and P. J. O’Malley, Biochemistry 33, 1734 (1994).
C. W. Hoganson, M. Sahlin, B.-M. Sjoeberg and G. T. Babcock, J. Am. Chem. Soc. 118, 4672 (1996).
C. J. Bender, M. Sahlin, G. T. Babcock, B. A. Barry, T. K. Chandrashekar, S. P. Salowe, J. Stubbe, B. Lindstroem, L. Petersson and et al., J. Am. Chem. Soc. 111, 8076 (1989).
K. A. Campbell, J. M. Peloquin, B. A. Diner, X.-S. Tang, D. A. Chisholm and R. D. Britt, J. Am. Chem. Soc. 119, 4787 (1997).
A. J. Stone, Mol. Phys. 6, 509 (1963).
A. J. Stone, Mol. Phys. 7, 311 (1964).
E. L. Fasanella and W. Gordy, Proc. Natl. Acad. Sci. USA 62, 299 (1969).
B. A. Barry and O. Einarsdottir, J. Phys. Chem. B 109, 6972 (2005).
W. Hofbauer, A. Zouni, R. Bittl, J. Kern, P. Orth, F. Lendzian, P. Fromme, H. T. Witt and W. Lubitz, Proc. Natl. Acad. Sci. USA 98, 6623 (2001).
A. Mezzetti, A. L. Maniero, M. Brustolon, G. Giacometti and L. C. Brunel, J. Phys. Chem. A 103, 9636 (1999).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Brynda, M., David Britt, R. Density Functional Theory calculations on the magnetic properties of the model tyrosine radical-histidine complex mimicking tyrosyl radical YD · in photosystem II. Res Chem Intermed 33, 863–883 (2007). https://doi.org/10.1163/156856707782169426
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1163/156856707782169426