Energetics and Kinetics of Primary Charge Separation in Bacterial Photosynthesis

TL;DR

This study uses molecular dynamics simulations and formal modeling to investigate the energetics and kinetics of primary charge separation in bacterial photosynthesis, revealing large electrostatic fluctuations and non-ergodic effects that align with experimental data.

Contribution

It introduces two simulation protocols, including a polarizable special pair model, to accurately capture electrostatic fluctuations and charge separation kinetics in bacterial photosynthesis.

Findings

Electrostatic fluctuations are larger than previously estimated.

Most electrostatic fluctuations become frozen on the charge separation timescale.

The model reproduces temperature dependence and non-exponential decay observed experimentally.

Abstract

We report the results of Molecular Dynamics (MD) simulations and formal modeling of the free energy surfaces and reaction rates of primary charge separation in the reaction center of \textit{Rhodobacter sphaeroides}. Two simulation protocols were used to produce MD trajectories. Standard force field potentials were employed in the first protocol. In the second protocol, the special pair was made polarizable to reproduce a high polarizability of its photoexcited state observed by Stark spectroscopy. The charge distribution between covalent and charge-transfer states of the special pair was dynamically adjusted during the simulation run. We found from both protocols that the breadth of electrostatic fluctuations of the protein/water environment far exceeds previous estimates resulting in about 1.6 eV reorganization energy of electron transfer in the first protocol and 2.5 eV in the second protocol. Most of these electrostatic fluctuations become dynamically frozen on the time-scale of primary charge separation resulting in much smaller solvation contributions to the activation barrier. A non-ergodic formulation of the diffusion-reaction electron transfer kinetics has allowed us to reproduce the experimental results for both the temperature dependence of the rate and the non-exponential decay of the population of the photoexcited special pair.