Journal Article

Optical control of ultrafast structural dynamics in a fluorescent protein

Garratt, Douglas, Eom, Intae, Galinis, Gediminas, Barnard, Jonathan, Ferreira, Josie L, Choi, Hyeongi, Boutet, Sebastien, Groenhof, Gerrit, Baxter, James M, Jang, Dogeun, Hyun, HyoJung, Buckup, Tiago, Morozov, Dmitry, Hutchison, Christopher D. M, Glencross, Flo, Perrett, Samuel, Boxer, Steven G, DePonte, Daniel P, Schmidt, Marius, Owada, Shigeki, Carbajo, Sergio, Taylor, Ben, Nango, Eriko, Maghlaoui, Karim, Fitzpatrick, Ann, Park, Jaehyun, Chukhutsina, Volha U, Yuan, Letong, Dorlhiac, Gabriel, Lefèvre, Salomé Bodet, Kim, Minseok, Aquila, Andrew, Marangos, Jon P, Cordon-Preciado, Violeta, Romei, Matthew G, Morgan, Rhodri M, Tanaka, Rie, Park, Sehan, Barty, Anton, Seaberg, Matt, Stockton, Sian, Chatrchyan, Viktoria, Iwata, So, Fadini, Alisia, Tono, Kensuke, Lin, Chi-Yun, Park, Gisu, van Thor, Jasper J

2023

Overview

The photoisomerization reaction of a fluorescent protein chromophore occurs on the ultrafast timescale. The structural dynamics that result from femtosecond optical excitation have contributions from vibrational and electronic processes and from reaction dynamics that involve the crossing through a conical intersection. The creation and progression of the ultrafast structural dynamics strongly depends on optical and molecular parameters. When using X-ray crystallography as a probe of ultrafast dynamics, the origin of the observed nuclear motions is not known. Now, high-resolution pump–probe X-ray crystallography reveals complex sub-ångström, ultrafast motions and hydrogen-bonding rearrangements in the active site of a fluorescent protein. However, we demonstrate that the measured motions are not part of the photoisomerization reaction but instead arise from impulsively driven coherent vibrational processes in the electronic ground state. A coherent-control experiment using a two-colour and two-pulse optical excitation strongly amplifies the X-ray crystallographic difference density, while it fully depletes the photoisomerization process. A coherent control mechanism was tested and confirmed the wave packets assignment.Pump–probe measurements conventionally achieve femtosecond time resolution for X-ray crystallography of reactive processes, but the measured structural dynamics are complex. Using coherent control techniques, we show that the ultrafast crystallographic differences of a fluorescent protein are dominated by ground-state vibrational processes that are unconnected to the photoisomerization reaction of the chromophore.

• Publisher: Nature Publishing Group
• Subject: Chromophores / Coherence / Crystallography / Dynamics / Excitation / Fluorescence / Hydrogen bonding / Optical control / Proteins / Wave packets / X-ray crystallography