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Title: Unraveling electronic absorption spectra using nuclear quantum effects: Photoactive yellow protein and green fluorescent protein chromophores in water

Abstract

Many physical phenomena must be accounted for to accurately model solution-phase optical spectra line shapes, from the sampling of chromophore-solvent configurations to the electronic-vibrational transitions leading to vibronic fine structure. Here we thoroughly explore the role of nuclear quantum effects, direct and indirect solvent effects, and vibronic effects in the computation of the optical spectrum of the aqueously solvated anionic chromophores of green fluorescent protein (GFP) and photoactive yellow protein (PYP). By analyzing the chromophore and solvent configurations, the distributions of vertical excitation energies, the absorption spectra computed within the ensemble approach, and the absorption spectra computed within the ensemble plus zero-temperature Franck-Condon approach, we introduce how solvent, nuclear quantum effects, and vibronic transitions alter the optical absorption spectra. We discover that including nuclear quantum effects in the sampling of chromophore-solvent configurations using ab initio path integral molecular dynamics simulations leads to improved spectral shapes through three mechanisms. The three mechanisms that lead to line shape broadening and a better description of the high-energy tail are softening of heavy atom bonds in the chromophore that couple to the optically bright state, widening the distribution of vertical excitation energies from more diverse solvation environments, and redistributing spectral weight from the 0-0more » vibronic transition to higher energy vibronic transitions when computing the Franck-Condon spectrum in a frozen solvent pocket. The absorption spectra computed using the combined ensemble plus zero-temperature Franck-Condon approach yield significant improvements in spectral shape and width compared to spectra computed with the ensemble approach. Using the combined approach with configurations sampled from path integral molecular dynamics trajectories presents a significant step forward in accurately modeling the absorption spectra of aqueously solvated chromophores.« less

Authors:
 [1];  [2];  [1]; ORCiD logo [2]; ORCiD logo [1]
  1. Univ. of California, Merced, CA (United States)
  2. Stanford Univ., CA (United States)
Publication Date:
Research Org.:
Stanford Univ., CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division; USDOE
OSTI Identifier:
1526765
Alternate Identifier(s):
OSTI ID: 1460130
Grant/Contract Number:  
SC0014437; AC02-05CH11231; ACI-1429830; ACI-1429783
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Journal of Chemical Physics
Additional Journal Information:
Journal Volume: 149; Journal Issue: 2; Journal ID: ISSN 0021-9606
Publisher:
American Institute of Physics (AIP)
Country of Publication:
United States
Language:
English
Subject:
71 CLASSICAL AND QUANTUM MECHANICS, GENERAL PHYSICS; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Zuehlsdorff, Tim J., Napoli, Joseph A., Milanese, Joel M., Markland, Thomas E., and Isborn, Christine M. Unraveling electronic absorption spectra using nuclear quantum effects: Photoactive yellow protein and green fluorescent protein chromophores in water. United States: N. p., 2018. Web. doi:10.1063/1.5025517.
Zuehlsdorff, Tim J., Napoli, Joseph A., Milanese, Joel M., Markland, Thomas E., & Isborn, Christine M. Unraveling electronic absorption spectra using nuclear quantum effects: Photoactive yellow protein and green fluorescent protein chromophores in water. United States. doi:10.1063/1.5025517.
Zuehlsdorff, Tim J., Napoli, Joseph A., Milanese, Joel M., Markland, Thomas E., and Isborn, Christine M. Fri . "Unraveling electronic absorption spectra using nuclear quantum effects: Photoactive yellow protein and green fluorescent protein chromophores in water". United States. doi:10.1063/1.5025517. https://www.osti.gov/servlets/purl/1526765.
@article{osti_1526765,
title = {Unraveling electronic absorption spectra using nuclear quantum effects: Photoactive yellow protein and green fluorescent protein chromophores in water},
author = {Zuehlsdorff, Tim J. and Napoli, Joseph A. and Milanese, Joel M. and Markland, Thomas E. and Isborn, Christine M.},
abstractNote = {Many physical phenomena must be accounted for to accurately model solution-phase optical spectra line shapes, from the sampling of chromophore-solvent configurations to the electronic-vibrational transitions leading to vibronic fine structure. Here we thoroughly explore the role of nuclear quantum effects, direct and indirect solvent effects, and vibronic effects in the computation of the optical spectrum of the aqueously solvated anionic chromophores of green fluorescent protein (GFP) and photoactive yellow protein (PYP). By analyzing the chromophore and solvent configurations, the distributions of vertical excitation energies, the absorption spectra computed within the ensemble approach, and the absorption spectra computed within the ensemble plus zero-temperature Franck-Condon approach, we introduce how solvent, nuclear quantum effects, and vibronic transitions alter the optical absorption spectra. We discover that including nuclear quantum effects in the sampling of chromophore-solvent configurations using ab initio path integral molecular dynamics simulations leads to improved spectral shapes through three mechanisms. The three mechanisms that lead to line shape broadening and a better description of the high-energy tail are softening of heavy atom bonds in the chromophore that couple to the optically bright state, widening the distribution of vertical excitation energies from more diverse solvation environments, and redistributing spectral weight from the 0-0 vibronic transition to higher energy vibronic transitions when computing the Franck-Condon spectrum in a frozen solvent pocket. The absorption spectra computed using the combined ensemble plus zero-temperature Franck-Condon approach yield significant improvements in spectral shape and width compared to spectra computed with the ensemble approach. Using the combined approach with configurations sampled from path integral molecular dynamics trajectories presents a significant step forward in accurately modeling the absorption spectra of aqueously solvated chromophores.},
doi = {10.1063/1.5025517},
journal = {Journal of Chemical Physics},
issn = {0021-9606},
number = 2,
volume = 149,
place = {United States},
year = {2018},
month = {7}
}

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