Resolving the ultrafast dynamics of the anionic green fluorescent protein chromophore in water

Jones, Chey M.; List, Nanna H.; Martínez, Todd J.

doi:10.1039/D1SC02508B

Title: Resolving the ultrafast dynamics of the anionic green fluorescent protein chromophore in water

Journal Article · Wed Sep 01 00:00:00 EDT 2021 · Chemical Science

DOI:https://doi.org/10.1039/D1SC02508B· OSTI ID:1810989

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Department of Chemistry and the PULSE Institute, Stanford University, Stanford, CA 94305, USA, SLAC National Accelerator Laboratory, 2575 Sand Hill Road, Menlo Park, CA 94025, USA

The chromophore of the green fluorescent protein (GFP) is critical for probing environmental influences on fluorescent protein behavior. Using the aqueous system as a bridge between the unconfined vacuum system and a constricting protein scaffold, we investigate the steric and electronic effects of the environment on the photodynamical behavior of the chromophore. Specifically, we apply ab initio multiple spawning to simulate five picoseconds of nonadiabatic dynamics after photoexcitation, resolving the excited-state pathways responsible for internal conversion in the aqueous chromophore. We identify an ultrafast pathway that proceeds through a short-lived (sub-picosecond) imidazolinone-twisted (I-twisted) species and a slower (several picoseconds) channel that proceeds through a long-lived phenolate-twisted (P-twisted) intermediate. The molecule navigates the non-equilibrium energy landscape via an aborted hula-twist-like motion toward the one-bond-flip dominated conical intersection seams, as opposed to following the pure one-bond-flip paths proposed by the excited-state equilibrium picture. We interpret our simulations in the context of time-resolved fluorescence experiments, which use short- and long-time components to describe the fluorescence decay of the aqueous GFP chromophore. Our results suggest that the longer time component is caused by an energetically uphill approach to the P-twisted intersection seam rather than an excited-state barrier to reach the twisted intramolecular charge-transfer species. Irrespective of the location of the nonadiabatic population events, the twisted intersection seams are inefficient at facilitating isomerization in aqueous solution. The disordered and homogeneous nature of the aqueous solvent environment facilitates non-selective stabilization with respect to I- and P-twisted species, offering an important foundation for understanding the consequences of selective stabilization in heterogeneous and rigid protein environments.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AMOS Program; AC02-76SF00515

OSTI ID:: 1810989

Alternate ID(s):: OSTI ID: 1819727

Journal Information:: Chemical Science, Journal Name: Chemical Science Vol. 12 Journal Issue: 34; ISSN 2041-6520

Publisher:: Royal Society of Chemistry (RSC)Copyright Statement

Country of Publication:: United Kingdom

Language:: English

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