title: Molecular dynamics study of the primary charge separation reactions in Photosystem I: effect of the replacement of the axial ligands to the electron acceptor A₀.
abstract: Molecular dynamics (MD) calculations, a semi-continuum (SC) approach, and quantum chemistry (QC) calculations were employed together to investigate the molecular mechanics of ultrafast charge separation reactions in Photosystem I (PS I) of Thermosynechococcus elongatus. A molecular model of PS I was developed with the aim to relate the atomic structure with electron transfer events in the two branches of cofactors. A structural flexibility map of PS I was constructed based on MD simulations, which demonstrated its rigid hydrophobic core and more flexible peripheral regions. The MD model permitted the study of atomic movements (dielectric polarization) in response to primary and secondary charge separations, while QC calculations were used to estimate the direct chemical effect of the A(0A)/A(0B) ligands (Met or Asn in the 688/668 position) on the redox potential of chlorophylls A(0A)/A(0B) and phylloquinones A(1A)/A(1B). A combination of MD and SC approaches was used to estimate reorganization energies λ of the primary (λ₁) and secondary (λ₂ ) charge separation reactions, which were found to be independent of the active branch of electron transfer; in PS I from the wild type, λ₁ was estimated to be 390 ± 20mV, while λ₂ was estimated to be higher at 445 ± 15mV. MD and QC approaches were used to describe the effect of substituting Met688(PsaA)/Met668(PsaB) by Asn688(PsaA)/Asn668(PsaB) on the energetics of electron transfer. Unlike Met, which has limited degrees of freedom in the site, Asn was found to switch between two relatively stable conformations depending on cofactor charge. The introduction of Asn and its conformation flexibility significantly affected the reorganization energy of charge separation and the redox potentials of chlorophylls A(0A)/A(0B) and phylloquinones A(1A)/A(1B), which may explain the experimentally observed slowdown of secondary electron transfer in the M688N(PsaA) variant. This article is part of a special issue entitled: photosynthesis research for sustainability: keys to produce clean energy.
authors.affiliation: A.N. Belozersky Institute of Physical-Chemical Biology, Moscow State University, Moscow, Russia; Faculty of Bioengineering and Bioinformatics, Moscow State University, Moscow, Russia.
authors.forename: Georgy E
authors.initials: GE
authors.lastname: Milanovsky
authors.affiliation: A.N. Belozersky Institute of Physical-Chemical Biology, Moscow State University, Moscow, Russia.
authors.forename: Vasily V
authors.initials: VV
authors.lastname: Ptushenko
authors.affiliation: Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, PA, USA; Department of Chemistry, The Pennsylvania State University, University Park, PA, USA.
authors.forename: John H
authors.initials: JH
authors.lastname: Golbeck
authors.affiliation: A.N. Belozersky Institute of Physical-Chemical Biology, Moscow State University, Moscow, Russia. Electronic address: semenov@genebee.msu.ru.
authors.forename: Alexey Yu
authors.initials: AY
authors.lastname: Semenov
authors.affiliation: A.N. Frumkin Institute of Physical Chemistry and Electrochemistry, Russian Academy of Sciences, Moscow, Russia. Electronic address: tscherepanov@gmail.com.
authors.forename: Dmitry A
authors.initials: DA
authors.lastname: Cherepanov
mesh_terms: D002734:Chlorophyll / Q000737:chemistry; D000077194:Chlorophyll A; D004579:Electron Transport; D008024:Ligands; D056004:Molecular Dynamics Simulation; D010084:Oxidation-Reduction; D045331:Photosystem I Protein Complex / Q000737:chemistry*; D011487:Protein Conformation; D012399:Rotation; D010837:Vitamin K 1 / Q000737:chemistry
chemical_list: D008024:Ligands; D045331:Photosystem I Protein Complex; D002734:Chlorophyll; D010837:Vitamin K 1; D000077194:Chlorophyll A
keywords: Charge separation; Molecular dynamics; Photosystem I; Primary reactions; Quantum chemistry; Reorganization energy