Identification of residues potentially involved in optical shifts in the water-soluble chlorophyll-a binding protein through molecular dynamics simulations

Abstract

Photosynthesis is the process responsible for nearly all life on Earth. It has been the subject of many studies aimed to better understand this process and develop novel approaches to harvesting light energy. The first, light-induced steps of photosynthesis include light harvesting, energy transfer and charge transfer; they occur in trans-membrane pigment-protein complexes. These primary processes of photosynthesis are particularly well-suited to be explored by means of optical spectroscopy. Of particular interest are high-resolution frequency-domain techniques such as non-photochemical spectral hole burning (NPHB) and single complex spectroscopy. The very existence of NPHB and observations of line shifts in the single-molecule optical spectra of pigment-protein complexes indicate the occurrence of small structural changes in the pigment environment, even at cryogenic temperatures. Nonetheless, the specific molecular elements responsible for the observed spectral dynamics remain largely unknown, leaving the traditional double-well / two-level-system (TLS) model without molecular-level evidence supporting it. In this work, we have studied the Water-Soluble Chlorophyll-binding Protein to elucidate some of these molecular-level mechanisms. From large-scale molecular dynamics simulations of the complex, we identified potential molecular drivers for experimental observations, including long hydrogen bonds and side chain rotations of certain amino acid residues. The protein free energy landscapes associated with side chain rotations demonstrated energy barriers of around 1100-1600 cm-1, in agreement with experimental results, with the most promising residue type associated with experimental signatures being serine. Overall, we have demonstrated new evidence of the molecular-level origins of optical spectroscopy results and provided important support for the TLS/MLS model.