Spin Density Asymmetry Research Articles

Electronic Structure of the Primary Electron Donor P700+• in Photosystem I Studied by Multifrequency HYSCORE Spectroscopy at X- and Q-Band.

The primary electron donor P700 of the photosystem I (PSI) is a heterodimer consisting of two chlorophyll molecules. A series of electron-transfer events immediately following the initial light excitation leads to a stabilization of the positive charge by its cation radical form, P700+•. The electronic structure of P700+• and, in particular, its asymmetry with respect to the two chlorophyll monomers is of fundamental interest and is not fully understood up to this date. Here, we apply multifrequency X- (9 GHz) and Q-band (35 GHz) hyperfine sublevel correlation (HYSCORE) spectroscopy to investigate the electron spin density distribution in the cation radical P700+• of PSI from a thermophilic cyanobacterium Thermosynechococcus elongatus. Six 14N and two 1H distinct nuclei have been resolved in the HYSCORE spectra and parameters of the corresponding nuclear hyperfine and quadrupolar hyperfine interactions were obtained by combining the analysis of HYSCORE spectral features with direct numerical simulations. Based on a close similarity of the nuclear quadrupole tensor parameters, all of the resolved 14N nuclei were assigned to six out of total eight available pyrrole ring nitrogen atoms (i.e., four in each of the chlorophylls), providing direct evidence of spin density delocalization over the both monomers in the heterodimer. Using the obtained experimental values of the 14N electron-nuclear hyperfine interaction parameters, the upper limit of the electron spin density asymmetry parameter is estimated as RA/Bupper = 7.7 ± 0.5, while a tentative assignment of 14N observed in the HYSCORE spectra yields RB/A = 3.1 ± 0.5.

Computational Investigation of the Spin-Density Asymmetry in Photosynthetic Reaction Center Models from First Principles.

We present a computational analysis of the spin-density asymmetry in cation radical states of reaction center models from photosystem I, photosystem II, and bacteria from Synechococcus elongatus, Thermococcus vulcanus, and Rhodobacter sphaeroides, respectively. The recently developed frozen-density embedding (FDE)-diab methodology [J. Chem. Phys., 2018, 148, 214104] allowed us to effectively avoid the spin-density overdelocalization error characteristic for the standard Kohn-Sham density functional theory and to reliably calculate spin-density distributions and electronic couplings for a number of molecular systems ranging from inner pairs of (bacterio)chlorophyll a molecules in vacuum to large proteins including up to about 2000 atoms. The calculated spin densities show a good agreement with available experimental results and were used to validate reaction center models reported in the literature. Here, we demonstrate that the applied theoretical approach is very sensitive to changes in molecular structures and the relative orientation of molecules. This makes FDE-diab a valuable tool for electronic structure calculations of large photosynthetic models effectively complementing the existing experimental techniques.

Spin densities from subsystem density-functional theory: Assessment and application to a photosynthetic reaction center complex model

Subsystem density-functional theory (DFT) is a powerful and efficient alternative to Kohn-Sham DFT for large systems composed of several weakly interacting subunits. Here, we provide a systematic investigation of the spin-density distributions obtained in subsystem DFT calculations for radicals in explicit environments. This includes a small radical in a solvent shell, a π-stacked guanine-thymine radical cation, and a benchmark application to a model for the special pair radical cation, which is a dimer of bacteriochlorophyll pigments, from the photosynthetic reaction center of purple bacteria. We investigate the differences in the spin densities resulting from subsystem DFT and Kohn-Sham DFT calculations. In these comparisons, we focus on the problem of overdelocalization of spin densities due to the self-interaction error in DFT. It is demonstrated that subsystem DFT can reduce this problem, while it still allows to describe spin-polarization effects crossing the boundaries of the subsystems. In practical calculations of spin densities for radicals in a given environment, it may thus be a pragmatic alternative to Kohn-Sham DFT calculations. In our calculation on the special pair radical cation, we show that the coordinating histidine residues reduce the spin-density asymmetry between the two halves of this system, while inclusion of a larger binding pocket model increases this asymmetry. The unidirectional energy transfer in photosynthetic reaction centers is related to the asymmetry introduced by the protein environment.

Density Functional Studies of the Spin Density Distribution of the P865 Cation Radical in the Reaction Center of Rb sphaeroides

Density functional calculations are used to calculate the spin density distribution for the P865 dimer cation radical in the Rb sphaeroides reaction center. Comparison between calculated and experimental hyperfine couplings is performed where good agreement is found for the four nitrogen and 121 proton methyl group hyperfine couplings. Overall, the spin density ratio between the two halves is in agreement with experimental determinations, although the calculations suggest that significant differences in this ratio exists for different regions of the bacteriochlorophyll macrocycles. Calculated spin density asymmetry changes brought about by mutational changes in the immediate amino acid environment agree with experimental interpretations.

An ONIOM study of the Q A site semiquinone in the Rhodobacter sphaeroides photosynthetic reaction centre

ONIOM (QM/MM) calculations are performed to investigate the spin density distribution for the ubisemiquinone anion radical in the Q A binding site of the photosynthetic bacterium Rhodobacter sphaeroides. The calculated spin density in the Q A site model suggests that differential hydrogen bonding strength to the O1 and O4 oxygen atoms of the radical results in an asymmetric spin density distribution in the semiquinone anion free radical form. The origin of the spin density asymmetry is attributed to the presence of the divalent iron or zinc ion situated between the Q A and Q B sites.

A DFT STUDY ON THE ELECTRONIC CHARACTER OF P700+

This density functional study is devoted to the long debated electronic nature of P700+. We found that P700+ is intrinsically a dimer of chlorophyll molecules. The unpaired electron spin distributes equally over two chlorophyll molecule halves in the bare P700+, while the dressed P700+ shows the spin density asymmetry mainly coming from the H-bond donated to 131-keto-O of one half. The experimental contradictions on the electronic nature of P700+ are also discussed.

The origin of the spin density asymmetry at the Q A binding site of type II photosynthetic reaction centres

Hybrid density functional calculations are used to calculate the spin density distribution for the ubisemiquinone anion radical in the Q A binding site of the photosynthetic bacterium Rb sphaeroides. The calculated spin density in the Q A site model suggests that differential hydrogen-bonding strength to the O1 and O4 oxygen atoms of the radical results in an asymmetric spin density distribution in the semiquinone anion free radical form. Good agreement is found between calculated and experimental 13C and 17O hyperfine couplings lending support to the calculation. The origin of the spin density asymmetry is attributed to the presence of the divalent iron or zinc ion situated between the Q A and Q B sites. The asymmetry is proposed to play a role in the unique one-electron reduction mechanism of the Q A site quinone and also in redirecting electron transfer parallel to the membrane plane.

Molecular orbital study of the primary electron donor P700 of photosystem I based on a recent X-ray single crystal structure analysis

Abstract 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.

Spin-density asymmetry in NiV alloy at various temperatures

Polarised neutron diffraction has been used to determine the neutron magnetic form factors of a Ni0.959V0.041 random alloy at 4.2, 290 and 378 K. From the analysis of the form factors it is concluded that within experimental accuracy the spatial distribution of the spin density remains unaltered up to 0.9 Tc for this alloy.

Temperature dependence of the spin-density asymmetry in Ni

Temperature dependence of the spin-density asymmetry in Ni