Abstract
Exciton charge separation in photosynthetic reaction centers from purple bacteria (PbRC) and photosystem II (PSII) occurs exclusively along one of the two pseudo-symmetric branches (active branch) of pigment–protein complexes. The microscopic origin of unidirectional charge separation in photosynthesis remains controversial. Here we elucidate the essential factors leading to unidirectional charge separation in PbRC and PSII, using nonadiabatic quantum dynamics calculations in conjunction with time-dependent density functional theory (TDDFT) with the quantum mechanics/molecular mechanics/polarizable continuum model (QM/MM/PCM) method. This approach accounts for energetics, electronic coupling, and vibronic coupling of the pigment excited states under electrostatic interactions and polarization of whole protein environments. The calculated time constants of charge separation along the active branches of PbRC and PSII are similar to those observed in time-resolved spectroscopic experiments. In PbRC, Tyr-M210 near the accessary bacteriochlorophyll reduces the energy of the intermediate state and drastically accelerates charge separation overcoming the electron–hole interaction. Remarkably, even though both the active and inactive branches in PSII can accept excitons from light-harvesting complexes, charge separation in the inactive branch is prevented by a weak electronic coupling due to symmetry-breaking of the chlorophyll configurations. The exciton in the inactive branch in PSII can be transferred to the active branch via direct and indirect pathways. Subsequently, the ultrafast electron transfer to pheophytin in the active branch prevents exciton back transfer to the inactive branch, thereby achieving unidirectional charge separation.
Highlights
Light reactions of photosynthesis achieve an extremely high internal quantum efficiency from photoabsorption to separated electrons and holes[1] through ingeniously regulated pathways of energy and charge transfers in pigment–protein complexes
We address the long-standing open question as to how PbRC and Photosystem II (PSII) achieve unidirectional charge separation exclusively along the active branch, by means of nonadiabatic quantum dynamics calculations[59,60,61,62] parametrized on the basis of time-dependent density functional theory (TDDFT) in the framework of the QM/MM/PCM method.[63,64]
We show that the experimentally observed kinetics of charge separation along the active branches of PbRC and PSII are fairly well reproduced by nonadiabatic quantum dynamics calculations, which is based on the energetics and electronic coupling of the pigments, accounting for electrostatic interactions and polarization of whole protein environments from the X-ray crystal structures
Summary
Light reactions of photosynthesis achieve an extremely high internal quantum efficiency from photoabsorption to separated electrons and holes[1] through ingeniously regulated pathways of energy and charge transfers in pigment–protein complexes. We address the long-standing open question as to how PbRC and PSII achieve unidirectional charge separation exclusively along the active branch, by means of nonadiabatic quantum dynamics calculations[59,60,61,62] parametrized on the basis of TDDFT in the framework of the QM/MM/PCM method.[63,64] First, we show that the experimentally observed kinetics of charge separation along the active branches of PbRC and PSII are fairly well reproduced by nonadiabatic quantum dynamics calculations, which is based on the energetics and electronic coupling of the pigments, accounting for electrostatic interactions and polarization of whole protein environments from the X-ray crystal structures On this basis, we clarify the essential factors which regulate the charge separation pathways in the reaction centers
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