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Title: Internal conversion of the anionic GFP chromophore: in and out of the I-twisted S 1 /S 0 conical intersection seam

Abstract

The functional diversity of the green fluorescent protein (GFP) family is intimately connected to the interplay between competing photo-induced transformations of the chromophore motif, anionic p-hydroxybenzylidene-2,3-dimethylimidazolinone (HBDI-). Its ability to undergo Z/E-isomerization is of particular importance for super-resolution microscopy and emerging opportunities in optogenetics. Yet, key dynamical features of the underlying internal conversion process in the native HBDI- chromophore remain largely elusive. We investigate the intrinsic excited-state behavior of isolated HBDI- to resolve competing decay pathways and map out the factors governing efficiency and the stereochemical outcome of photoisomerization. Based on non-adiabatic dynamics simulations, we demonstrate that non-selective progress along the two bridge-torsional (i.e., phenolate, P, or imidazolinone, I) pathways accounts for the three decay constants reported experimentally, leading to competing ultrafast relaxation primarily along the I-twisted pathway and S1 trapping along the P-torsion. The majority of the population (~70%) is transferred to S0 in the vicinity of two approximately enantiomeric minima on the I-twisted intersection seam (MECI-Is). Despite their sloped, reactant-biased topographies (suggesting low photoproduct yields), we find that decay through these intersections leads to products with a surprisingly high quantum yield of ~30%. This demonstrates that E-isomer generation results at least in part from direct isomerization on themore » excited state. A photoisomerization committor analysis reveals a difference in intrinsic photoreactivity of the two MECI-Is and that the observed photoisomerization is the combined result of two effects: early, non-statistical dynamics around the less reactive intersection followed by later, near-statistical behavior around the more reactive MECI-I. Our work offers new insight into internal conversion of HBDI- that both establishes the intrinsic properties of the chromophore and enlightens principles for the design of chromophore derivatives and protein variants with improved photoswitching properties.« less

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]
+ Show Author Affiliations
  1. 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
Publication Date:
Research Org.:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); Villum Foundation
OSTI Identifier:
1834650
Alternate Identifier(s):
OSTI ID: 1838671
Grant/Contract Number:  
AC02-76SF00515; VKR023371
Resource Type:
Published Article
Journal Name:
Chemical Science
Additional Journal Information:
Journal Name: Chemical Science Journal Volume: 13 Journal Issue: 2; Journal ID: ISSN 2041-6520
Publisher:
Royal Society of Chemistry (RSC)
Country of Publication:
United Kingdom
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

List, Nanna H., Jones, Chey M., and Martínez, Todd J. Internal conversion of the anionic GFP chromophore: in and out of the I-twisted S 1 /S 0 conical intersection seam. United Kingdom: N. p., 2022. Web. doi:10.1039/D1SC05849E.
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List, Nanna H., Jones, Chey M., & Martínez, Todd J. Internal conversion of the anionic GFP chromophore: in and out of the I-twisted S 1 /S 0 conical intersection seam. United Kingdom. https://doi.org/10.1039/D1SC05849E
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List, Nanna H., Jones, Chey M., and Martínez, Todd J. Wed . "Internal conversion of the anionic GFP chromophore: in and out of the I-twisted S 1 /S 0 conical intersection seam". United Kingdom. https://doi.org/10.1039/D1SC05849E.
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@article{osti_1834650,
title = {Internal conversion of the anionic GFP chromophore: in and out of the I-twisted S 1 /S 0 conical intersection seam},
author = {List, Nanna H. and Jones, Chey M. and Martínez, Todd J.},
abstractNote = {The functional diversity of the green fluorescent protein (GFP) family is intimately connected to the interplay between competing photo-induced transformations of the chromophore motif, anionic p-hydroxybenzylidene-2,3-dimethylimidazolinone (HBDI-). Its ability to undergo Z/E-isomerization is of particular importance for super-resolution microscopy and emerging opportunities in optogenetics. Yet, key dynamical features of the underlying internal conversion process in the native HBDI- chromophore remain largely elusive. We investigate the intrinsic excited-state behavior of isolated HBDI- to resolve competing decay pathways and map out the factors governing efficiency and the stereochemical outcome of photoisomerization. Based on non-adiabatic dynamics simulations, we demonstrate that non-selective progress along the two bridge-torsional (i.e., phenolate, P, or imidazolinone, I) pathways accounts for the three decay constants reported experimentally, leading to competing ultrafast relaxation primarily along the I-twisted pathway and S1 trapping along the P-torsion. The majority of the population (~70%) is transferred to S0 in the vicinity of two approximately enantiomeric minima on the I-twisted intersection seam (MECI-Is). Despite their sloped, reactant-biased topographies (suggesting low photoproduct yields), we find that decay through these intersections leads to products with a surprisingly high quantum yield of ~30%. This demonstrates that E-isomer generation results at least in part from direct isomerization on the excited state. A photoisomerization committor analysis reveals a difference in intrinsic photoreactivity of the two MECI-Is and that the observed photoisomerization is the combined result of two effects: early, non-statistical dynamics around the less reactive intersection followed by later, near-statistical behavior around the more reactive MECI-I. Our work offers new insight into internal conversion of HBDI- that both establishes the intrinsic properties of the chromophore and enlightens principles for the design of chromophore derivatives and protein variants with improved photoswitching properties.},
doi = {10.1039/D1SC05849E},
journal = {Chemical Science},
number = 2,
volume = 13,
place = {United Kingdom},
year = {Wed Jan 05 00:00:00 EST 2022},
month = {Wed Jan 05 00:00:00 EST 2022}
}
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