First-Principles Characterization of the Elusive I Fluorescent State and the Structural Evolution of Retinal Protonated Schiff Base in Bacteriorhodopsin

Yu, Jimmy K.; Liang, Ruibin; Liu, Fang; Martínez, Todd J.

doi:10.1021/jacs.9b08941

Title: First-Principles Characterization of the Elusive I Fluorescent State and the Structural Evolution of Retinal Protonated Schiff Base in Bacteriorhodopsin

Journal Article · Thu Oct 17 00:00:00 EDT 2019 · Journal of the American Chemical Society

DOI:https://doi.org/10.1021/jacs.9b08941· OSTI ID:1597903

Yu, Jimmy K. ^[1];

^[1];

^[2];

^[3]

Department of Chemistry and The PULSE Institute, Stanford University, Stanford, California 94305 (United States)
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Stanford Univ., CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)

The conversion of light energy into work is essential to life on earth. Bacteriorhodopsin (bR), a light-activated proton pump in Archae, has served for many years as a model system for the study of this process in photoactive proteins. Upon absorption of a photon, its chromophore, the retinal protonated Schiff base (RPSB), isomerizes from its native all-trans form to a 13-cis form and pumps a proton out of the cell in a process that is coupled to eventual ATP synthesis. Despite numerous time-resolved spectroscopic studies over the years, the details of the photodynamics of bR on the excited state, particularly the characterization of the I fluorescent state, the time-resolved reaction mechanism, and the role of the counterion cluster of RPSB, remain uncertain. Here, in this work, we use ab initio multiple spawning (AIMS) with spin-restricted ensemble Kohn–Sham (REKS) theory to simulate the nonadiabatic dynamics of the ultrafast photoreaction in bR. The excited state dynamics can be partitioned into three distinct phases: (1) relaxation away from the Franck–Condon region dominated by changes in retinal bond length alternation, (2) dwell time on the excited state in the I fluorescent state featuring an untwisted, bond length inverted RPSB, and (3) rapid torsional evolution to the conical intersection after overcoming a small excited state barrier. We fully characterize the I fluorescent state and the excited state barrier that hinders direct evolution to the conical intersection following photoexcitation. We also find that photoisomerization is accompanied by weakening of the interaction between RPSB and its counterion cluster. However, in contradiction with a recent time-resolved X-ray experiment, hydrogen bond cleavage is not necessary to reproduce the observed photoisomerization dynamics.

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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). Chemical Sciences, Geosciences, and Biosciences Division; National Science Foundation (NSF)

Grant/Contract Number:: AC02-76SF00515; CHE-1740645

OSTI ID:: 1597903

Journal Information:: Journal of the American Chemical Society, Vol. 141, Issue 45; ISSN 0002-7863

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 36 works

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37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Counterions
Fluorescence
Crystal structure
Quantum mechanics
Excited states

Title: First-Principles Characterization of the Elusive I Fluorescent State and the Structural Evolution of Retinal Protonated Schiff Base in Bacteriorhodopsin

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