Local and Global Electric Field Asymmetry in Photosynthetic Reaction Centers

Abstract

The origin of unidirectional electron transfer in photosynthetic reaction centers (RCs) has been widely discussed. Despite the high level of structural similarity between the two branches of pigments that participate in the initial electron transfer steps of photosynthesis, electron transfer only occurs along one branch. One possible explanation for this functional asymmetry is the differences in the electrostatic environment between the active and the inactive branches arising from the charges and dipoles of the organized protein structure. We present an analysis of electric fields in the RC of the purple bacterium Rhodobacter sphaeroides using the intrinsic carbonyl groups of the pigments as vibrational reporters whose vibrational frequency shifts can be converted into electric fields based on the vibrational Stark effect and also provide Stark effect data for plant pigments that can be used in future studies. The carbonyl stretches of the isolated pigments show pronounced Stark effects. We use these data, solvatochromism, molecular dynamics simulations, and data in the literature from IR and Raman spectra to evaluate differences in fields at symmetry-related positions, in particular at the 9-keto and 2-acetyl positions of the pigments involved in primary charge separation.

Acquirement of water-splitting ability and alteration of the charge-separation mechanism in photosynthetic reaction centers

“…2 and 4 ). However, the L/M residues that stabilize H L •– with respect to H M •– (e.g., Glu-L104 ( 39 ), SI Appendix , Table S5 ) do not correspond to those that stabilize Pheo D1 •– with respect to Pheo D2 •– ( Table 5 ), which implies the difference in the protein electrostatic environment and the charge-separation mechanism between the two reaction centers.…”

Solvent tuning of photochemistry upon excited-state symmetry breaking

“…They raise the question of whether coherence in the excited state can be functionally relevant or whether it is too fragile to be utilized in realistic photochemical transformations. The local asymmetry arising from local fields is at the core of the functional asymmetry of natural photosynthetic reaction centers 68 . It also explains the lack of success in the elaboration of symmetric molecular systems that could exhibit double excitedstate proton transfer [69][70][71] .…”

The origin of unidirectional charge separation in photosynthetic reaction centers: nonadiabatic quantum dynamics of exciton and charge in pigment–protein complexes

“…[39][40][41][42][43][44][45][46][47][48][49][50] Despite the pseudo-C 2 symmetric cofactor arrangement, the difference in the amino acid sequences between the L-and M-branches leads to the difference in the redox potentials of the pigments via electrostatic interactions and polarization. [51][52][53] A previous study using time-dependent density functional theory (TDDFT) with the quantum mechanics/molecular mechanics/polarizable continuum model (QM/MM/PCM) method indicated that the intermediate states of charge separation along the L-and M-branches, i.e., [P L P M ]c + B L c À and [P L P M ]c + B M c À , are lower and higher in energy than that of (P L P M )*, respectively. 34 In contrast to PbRC, the excitation energies of P D1 and P D2 in PSII are higher than those of Chl D1 and Chl D2 , 9,34 where the exciton tends to be localized on a single pigment owing to a weak excitonic coupling.…”