TY - JOUR
T1 - Molecular orbital study of the primary electron donor P700 of photosystem I based on a recent X-ray single crystal structure analysis
AU - Plato, Martin
AU - Krauß, Norbert
AU - Fromme, Petra
AU - Lubitz, Wolfgang
N1 - Funding Information:
Arnold Hoff was one of the first researchers to work on the dimer problem in photosynthesis. When working with George Feher at UC San Diego as a postdoc in the early seventies, he showed the existence of the bacteriochlorophyll dimer in bacterial reaction centers using ENDOR spectroscopy. He later also worked on the donors in plant RCs. We enjoyed many fruitful discussions with Arnold that helped in the analysis of our data. We also owe special thanks to Sebastian Sinnecker (Max Planck Institute for Bioinorganic Chemistry) for various DFT trial calculations on different P700 structures, and to Friedhelm Lendzian and Heike Witt (both TU Berlin) and Patrick Jordan (FU Berlin) are gratefully acknowledged for helpful discussions. This work was supported by the Deutsche Forschungsgemeinschaft (SFB 498, TP Al, A4 and C5), Fonds der Chemischen Industrie (W.L.) and the EU (FMRX-CT98-0214).
PY - 2003/11/1
Y1 - 2003/11/1
N2 - The X-ray structure analysis of photosystem (PS) I single crystals showed that the primary electron donor P700 is a heterodimer formed by one chlorophyll (Chl) a and one Chl a′ [Nature 411 (2001) 909]. The electronic structure of the cation radical P700+· of the primary donor, which is created in the charge separation process, has been probed by semiempirical molecular orbital calculations including spin polarization effects (RHF-INDO/SP). The calculations, which were based on the X-ray structure, clearly show that P700 is a supermolecule formed by two chlorophyll species. They furthermore predict an asymmetrical charge and spin density distribution in favor of the monomeric Chl a half of this dimer in accordance with results from earlier EPR and ENDOR studies [J. Phys. Chem. B 105 (2000) 1225]. The stepwise inclusion of various electrostatic interactions of the dimer with its nearest surrounding (one threonine forming a hydrogen bond to the keto group of Chl a′ and two histidines liganding the Mg atoms of the two chlorophylls) leads to a systematic enhancement of this electronic asymmetry yielding a spin density ratio of almost 5:1 as also found experimentally. A large part of this value is caused by spin polarization effects. This result is only weakly affected by the electrostatic field of more remote amino acid residues and other pigment molecules ('accessory' Chl a molecules) present in PS I. A separate group of calculations involving local geometry optimizations by energy minimization techniques yields a further enhancement of the spin density asymmetry. A particularly strong effect is obtained by allowing for variations of the geometry of the vinyl groups on both chlorophylls of the P700 dimer. Theoretical results for individual isotropic proton and nitrogen hyperfine coupling constants, showing a satisfactory agreement with experimental findings, are also presented.
AB - The X-ray structure analysis of photosystem (PS) I single crystals showed that the primary electron donor P700 is a heterodimer formed by one chlorophyll (Chl) a and one Chl a′ [Nature 411 (2001) 909]. The electronic structure of the cation radical P700+· of the primary donor, which is created in the charge separation process, has been probed by semiempirical molecular orbital calculations including spin polarization effects (RHF-INDO/SP). The calculations, which were based on the X-ray structure, clearly show that P700 is a supermolecule formed by two chlorophyll species. They furthermore predict an asymmetrical charge and spin density distribution in favor of the monomeric Chl a half of this dimer in accordance with results from earlier EPR and ENDOR studies [J. Phys. Chem. B 105 (2000) 1225]. The stepwise inclusion of various electrostatic interactions of the dimer with its nearest surrounding (one threonine forming a hydrogen bond to the keto group of Chl a′ and two histidines liganding the Mg atoms of the two chlorophylls) leads to a systematic enhancement of this electronic asymmetry yielding a spin density ratio of almost 5:1 as also found experimentally. A large part of this value is caused by spin polarization effects. This result is only weakly affected by the electrostatic field of more remote amino acid residues and other pigment molecules ('accessory' Chl a molecules) present in PS I. A separate group of calculations involving local geometry optimizations by energy minimization techniques yields a further enhancement of the spin density asymmetry. A particularly strong effect is obtained by allowing for variations of the geometry of the vinyl groups on both chlorophylls of the P700 dimer. Theoretical results for individual isotropic proton and nitrogen hyperfine coupling constants, showing a satisfactory agreement with experimental findings, are also presented.
KW - Photosystem I
KW - Primary donor cation radical P700
KW - Semiempirical INDO calculations
KW - Spin density distribution
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U2 - 10.1016/S0301-0104(03)00378-1
DO - 10.1016/S0301-0104(03)00378-1
M3 - Article
AN - SCOPUS:1642310311
SN - 0301-0104
VL - 294
SP - 483
EP - 499
JO - Chemical Physics
JF - Chemical Physics
IS - 3
ER -