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

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, 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.