Glassy protein dynamics and gigantic solvent reorganization energy of plastocyanin

TL;DR

This study uses Molecular Dynamics simulations to reveal that slow protein and water fluctuations cause a broad energy gap distribution in plastocyanin, significantly affecting electron transfer dynamics and reorganization energy.

Contribution

It uncovers the role of non-ergodic protein-water fluctuations in broadening energy gaps and breaking the link between Stokes shift and reorganization energy in electron transfer.

Findings

Broad distribution of donor-acceptor energy gaps due to protein-water fluctuations

Non-ergodic fluctuations decouple Stokes shift from reorganization energy

Implications for low activation barriers in natural electron transfer proteins

Abstract

We report the results of Molecular Dynamics simulations of electron transfer activation parameters of plastocyanin metalloprotein involved as electron carrier in natural photosynthesis. We have discovered that slow, non-ergodic conformational fluctuations of the protein, coupled to hydrating water, result in a very broad distribution of donor-acceptor energy gaps far exceeding that observed for commonly studied inorganic and organic donor-acceptor complexes. The Stokes shift is not affected by these fluctuations and can be calculated from solvation models in terms of the response of the solvent dipolar polarization. The non-ergodic character of large-amplitude protein/water mobility breaks the strong link between the Stokes shift and reorganization energy characteristic of equilibrium (ergodic) theories of electron transfer. This mechanism might be responsible for low activation barriers in natural electron transfer proteins characterized by low reaction free energy.