The Role of Pigments of Photosystem II Reaction Center, a Computational Study

Palenčár P.¹, Vácha F.^2,3, Kutý M.¹

¹ Laboratory of High Performance Computing, Institute of Physical Biology,

University of South Bohemia, and Institute of Landscape Ecology, AS CR,

Zámek 136, 37333 Nové Hrady, Czech Republic

² Institute of Plant Molecular Biology, AS CR, Branišovská 31, 370 05

České Budějovice, Czech Republic

³ Institute of Physical Biology,University of South Bohemia,

Zámek 136, 373 33 Nové Hrady, Czech Republic

Photosystem II (PSII) is a pigment-protein complex located in thylakoid membrane of cyanobacteria, algae and higher plants. It performs series of light driven reactions, which result in a separation of charge and subsequently in a reduction of an electron-transport chain and water oxidation. Primary site of the light to chemical energy conversion is located in so-called reaction center (RC). Recently, light induced absorption and circular dichroism spectra from PSII RC, in presence of artificial electron donor dithionite, were obtained [1]. At room temperature the reduced pheophytin a (PHO) induces a conformational changes of the RC protein environment which affects the excitonic interaction of the RC chlorophylls.

Classical simulation methods such as molecular dynamics (MD) of PSII RC could be a powerful tool for better understanding and interpreting mention spectra. First, the distribution of negative charge over the molecule of PHO alone was needed to be calculated. Charges were derived by fitting HF/6-31G* ab initio electrostatic potential on a set of grid points around the molecule and subsequently rescaling them according to the restrained ESP (RESP) methodology [2] widely applied in AMBER Force Field (FF) [3]. Similarly also Mulliken charges applied in CHARMM FF [4] were computed. Due to computational demanding size of the whole PS II complex found in recent experimental crystal structure from Thermosynechococcus elongatus (PDB code: 1S5L) [5], smaller-size system including the most important parts of PSII RC was constructed.

Various studies have been recently performed in order to collect a complete set of parameters for the cofactors of PS II RC. [6, 7, 8, 9, 10]. Different methodologies were used to obtain FF parameters for the cofactors of PSII complex, namely fitting ab initio calculated data to observed vibrational frequencies of nickel octamethylporphyrin [9], performing normal mode analyses based on vibrational spectra of model compounds [9], using ab initio methods based on the density functional theory (DFT) [11]. It has been found that the current CHARMM27 FF parameters for the reduced heme group without ligands could represent the geometries obtained by QM calculations but are in partial disagreement with spectroscopic data [12, 13].

In this work we primarily focus on obtaining a charge set for both charged and neutral forms of PHO as well as on developing new CHARMM FF parameters [6]. The departure points of our force field development have been the existing CHARMM27 FF potential parameters for the unligated reduced form of heme prosthetic group [9] and quinines incorporated in the PSII RC.

The most characteristic feature of chlorophylls and pheophytins is their tertapyrrolic architecture related directly to metalloporphyrin (a magnesium-porphyrin system). Unfortunately, the PSII RC cofactors are in part composed of some unique molecular fragments not included in the present distributions of CHARMM27 FF [4], AMBER99 FF [3] and other [7, 6, 8] databases for which an ex novo ab initio-based modelization was performed. Following the scheme detail depicted in reference [7] we started to develop FF parameters (compatible with the CHARMM27 FF) for PSII RC cofactors based on a reliable set of ab initio calculations and reference data for chlorophyll a, pheophytin a, and a derivate of ubiquinone. In building the FF parameters we have limited the new types of atoms added to CHARMM27 FF to the bare minimum. In this study we only present the bond stretching parameters, the equilibrium bond lengths and subsistent force constants. The rest of parameters for bonded interactions are in progress.

[1] Vacha, F.; Psencik, J.; Kuty, M.; Durchan, M.; Siffel, P.: Evidence for localisation of accumulated chlorophyll cation on the D1-accessory chlorophyll in reaction centre of photosystem II., Photosynth. Res., (2005), In press

[2] Bayly, C. I.; Cieplak, P.; Cornell, W. D.; Kollman, P. A., J Phys Chem (1993), 97, 10269

[3] Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R., Jr.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Cladwell, J. W.; Kollmann, P. A., J Am Chem Soc (1995), 117, 5179

[4] MacKerell, A. D.; Bashford, D.; Bellot, M.; Dunbrack, R. L.; Evansec, J. D.; Field, M. J.; Fisher, S.; Gao, J.; Guo, H.; Ha, S.; Joseph, D.; Kuchnir, L.; Kuczera, K. K.; Lau, F. T. K.; Mattos, C.; Michnick, S.; Ngo, T.; Nguyen, D. T.; Prodhom, B.; Reiher, I. W. E.; Roux, B.; Schlenkrich, M.; Smith, J.; Stote, R.; Straub, J.; Watanabe, M.; Wiorkiewicz–Kuczera, J.; Yin, D.; Karplus, M., J Phys Chem B (1998), 102, 3586

[5] Ferreira, K. N.;Iverson, T. M.; Maghlaoui K.; Barber, J.; Iwata, S.: Architecture of the Photosynthetic Oxygen-Evolving Center, Science (2004), 303, 1831-1838

[6] Autenrieth, F.; Tajkhorshid, E.; Baudry, J.; Luthey-Schulten, Z.: Classical Force Field Parameters for the Heme Prosthetic Group of Cytochrome c, Wiley Periodicals, Inc., J Comput Chem (2004), 25, 1613-1622

[7] Ceccarelli, M.; Procacci, P.; Marchi, M.: An Ab initio Force Field for the Cofactors of Bacterial Photosynthesis, Wiley Periodicals, Inc., J Comput Chem (2003), 24, 129-142

[8] Tsai, Hui-Hsu.G.; Simpson, M. C.: HBFF-SVD Force Field Treatment of Ni(II) Porphine: Important Long Range Cross Terms, American Chemical Society (2003), 107, 526-541

[9] Kuczera, K.; Kuriyan, J.; Karplus, M.: Temperature Dependence of the Structure and Dynamics of Myoglobin. A Simulation Approach, Academic Press Limited, J Mol. Biol. (1990), 213, 351-373

[10] Foloppe, N.; Ferrand, M.; Breton, J.; Smith, J. C.: Structural Model of the Photosynthetic Reaction Centre of Rhodobacter capsulatus., Wiley Periodicals, Inc., Proteins: Structure, Function, and Genetics (1995), 226-244

[11] Ceccarelli, M.; Lutz, M.; Marchi, M. J Am Chem Soc (1996), 118, 7847

[12] Rush, T. S.; Kozlowski, P. M.; Piffat, C. A.; Kumble, R.; Zgierski, M. Z.; Spiro, T. G., J Phys Chem B (2000), 104, 5020

[13] Rai, B. K.; Durbin, S. M.; Prohofsky, E. W.; Sage, J. T.; Ellison, M. K.; Roth, A.; Scheidt, W. R.; Sturhahn, W.; Alp, E. E., J Am Chem Soc (2003), 125, 6927