Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin

TL;DR

This study employs time-resolved crystallography and spectroscopy to reveal the ultrafast structural and vibrational dynamics of photoexcited bacteriorhodopsin, highlighting a multi-photon excitation process and complex conformational changes within femtoseconds to picoseconds.

Contribution

It provides the first detailed 3D view of ultrafast dynamics in bacteriorhodopsin, uncovering multi-photon effects and coupled vibrational motions in retinal proteins.

Findings

Identification of a sequential two-photon absorption process.

Observation of a transition to a twisted 13-cis retinal conformation.

Detection of correlated vibrational motions among retinal, amino acids, and water molecules.

Abstract

Bacteriorhodopsin (bR) is a light-driven proton pump. We use time-resolved crystallography at an X-ray free-electron laser to follow the structural changes in multiphoton-excited bR from 250 femtoseconds to 10 picoseconds. Quantum chemistry and ultrafast spectroscopy allow identifying a sequential two-photon absorption process, leading to excitation of a tryptophan residue flanking the retinal chromophore, as a first manifestation of multi-photon effects. We resolve distinct stages in the structural dynamics of the all-trans retinal in photoexcited bR to a highly twisted 13-cis conformation. Other active site sub-picosecond rearrangements include correlated vibrational motions of the electronically excited retinal chromophore, the surrounding amino acids and water molecules as well as their hydrogen bonding network. These results show that this extended photo-active network forms an electronically and vibrationally coupled system in bR, and most likely in all retinal proteins.