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Title: Constructing the Mechanism of Dinoflagellate Luciferin Bioluminescence Using Computation

Abstract

Dinoflagellate luciferin bioluminescence is unique since it does not rely on decarboxylation but is poorly understood compared to that of firefly, bacteria, and coelenterata luciferins. Here, in this work, we computationally investigate possible protonation states, stereoisomers, a chemical mechanism, and the dynamics of the bioluminescence intermediate that is responsible for chemiexcitation. Using semiempirical dynamics, time-dependent density functional theory static calculations, and a correlation diagram, we find that the intermediate’s functional group that is likely responsible for chemiexcitation is a 4-member ring, a dioxetanol, that undergoes [2π + 2π] cycloreversion and the biolumiphore is the cleaved structure. The simulated emission spectra and luciferase-dependent absorbance spectra agree with the experimental data, giving support to our proposed mechanism and biolumiphore. We also compute circular dichroism spectra of the intermediate’s four stereoisomers to guide future experiments in differentiating them.

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2]
+ Show Author Affiliations
  1. Univ. of California, Irvine, CA (United States)
  2. Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Publication Date:
Research Org.:
Univ. of California, Irvine, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
2281920
Grant/Contract Number:  
SC0018352; 89233218NCA000001
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Physical Chemistry Letters
Additional Journal Information:
Journal Volume: 14; Journal Issue: 26; Journal ID: ISSN 1948-7185
Publisher:
American Chemical Society
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 74 ATOMIC AND MOLECULAR PHYSICS; Bioluminescence; Bioluminescent probes; Excited states; Mathematical methods; Molecular structure

Citation Formats

Phun, Gabriel S., Rappoport, Dmitrij, Furche, Filipp, Gibson, Tammie R., and Tretiak, Sergei. Constructing the Mechanism of Dinoflagellate Luciferin Bioluminescence Using Computation. United States: N. p., 2023. Web. doi:10.1021/acs.jpclett.3c01053.
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Phun, Gabriel S., Rappoport, Dmitrij, Furche, Filipp, Gibson, Tammie R., & Tretiak, Sergei. Constructing the Mechanism of Dinoflagellate Luciferin Bioluminescence Using Computation. United States. https://doi.org/10.1021/acs.jpclett.3c01053
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Phun, Gabriel S., Rappoport, Dmitrij, Furche, Filipp, Gibson, Tammie R., and Tretiak, Sergei. Thu . "Constructing the Mechanism of Dinoflagellate Luciferin Bioluminescence Using Computation". United States. https://doi.org/10.1021/acs.jpclett.3c01053.
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@article{osti_2281920,
title = {Constructing the Mechanism of Dinoflagellate Luciferin Bioluminescence Using Computation},
author = {Phun, Gabriel S. and Rappoport, Dmitrij and Furche, Filipp and Gibson, Tammie R. and Tretiak, Sergei},
abstractNote = {Dinoflagellate luciferin bioluminescence is unique since it does not rely on decarboxylation but is poorly understood compared to that of firefly, bacteria, and coelenterata luciferins. Here, in this work, we computationally investigate possible protonation states, stereoisomers, a chemical mechanism, and the dynamics of the bioluminescence intermediate that is responsible for chemiexcitation. Using semiempirical dynamics, time-dependent density functional theory static calculations, and a correlation diagram, we find that the intermediate’s functional group that is likely responsible for chemiexcitation is a 4-member ring, a dioxetanol, that undergoes [2π + 2π] cycloreversion and the biolumiphore is the cleaved structure. The simulated emission spectra and luciferase-dependent absorbance spectra agree with the experimental data, giving support to our proposed mechanism and biolumiphore. We also compute circular dichroism spectra of the intermediate’s four stereoisomers to guide future experiments in differentiating them.},
doi = {10.1021/acs.jpclett.3c01053},
journal = {Journal of Physical Chemistry Letters},
number = 26,
volume = 14,
place = {United States},
year = {Thu Jun 22 00:00:00 EDT 2023},
month = {Thu Jun 22 00:00:00 EDT 2023}
}
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Journal Article:
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