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

Abstract

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 FDE-diab methodology [J. Chem. Phys., 148 (2018), 214104] allowed us to effectively avoid the spin-density overdelocalization error characteristic for 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 protein 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 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. File list (2) download file view on ChemRxiv main_text.pdf (4.00 MiB) download file view on ChemRxiv supplementary_information.pdf (1.27 MiB)

Theoretical Assessment of Hinge-Type Models for Electron Donors in Reaction Centers of Photosystems I and II as Well as of Purple Bacteria

“…[28] and for inner pairs of (B)Chl molecules in RCs of PSI, PSII, and puple bacteria in Ref. [29] showing good agreements with both accurate theoretical and experimental results.…”

“…It was tested on model molecular clusters featuring different degrees of spin-density delocalizations and compared to accurate ab initio computations [28]. More recently, it was also applied to inner pair co-factors in RCs of PSI, PSII, and purple bacteria, and verified against previously available experimental measurements [29]. In both cases, a good agreement with theoretical and experimental results was found proving that the suggested approach is robust and effective.…”

“…[29]: First, positions of hydrogen atoms only were optimized and subsequently intramolecular bond lengths were relaxed, while keeping all the remaining degrees of freedom fixed (for more details, see Ref. [29]). To this end, the BP86 XC functional [45,46] and the def2-TZVP basis set [47,48] were used.…”

“…Binding pockets were initially optimized in a similar fashion as described in Ref. [29]. To this end, we first optimized the positions of hydrogens and then relaxed the atoms of (B)Chl a and Third-Order Parametrization for Organic and Biological Systems (3ob) [52,53], and the dispersion D3BJ correction [49,50] were applied in all three steps.…”

Theoretical Assessment of Hinge-Type Models for Electron Donors in Reaction Centers of Photosystems I and II as Well as of Purple Bacteria

“…that FDE-diab essentially avoids the consequences of the self-interaction-error, as far as intermolecular phenomena are concerned (as has already been highlighted in Refs. [28] and [29]). In addition, FDE-diab does not lead to overestimated areas of negative spin density, in contrast to conventional KS-DFT calculations with hybrid functionals.…”