The initial charge separation step in oxygenic photosynthesis

Abstract

Photosystem II is crucial for life on Earth as it provides oxygen as a result of photoinduced electron transfer and water splitting reactions. The excited state dynamics of the photosystem II-reaction center (PSII-RC) has been a matter of vivid debate because the absorption spectra of the embedded chromophores significantly overlap and hence it is extremely difficult to distinguish transients. Here, we report the two-dimensional electronic-vibrational spectroscopic study of the PSII-RC. The simultaneous resolution along both the visible excitation and infrared detection axis is crucial in allowing for the character of the excitonic states and interplay between them to be clearly distinguished. In particular, this work demonstrates that the mixed exciton-charge transfer state, previously proposed to be responsible for the far-red light operation of photosynthesis, is characterized by the ChlD1+Phe radical pair and can be directly prepared upon photoexcitation. Further, we find that the initial electron acceptor in the PSII-RC is Phe, rather than PD1, regardless of excitation wavelength.

Quasiparticle Self-Consistent GW-Bethe–Salpeter Equation Calculations for Large Chromophoric Systems

“…At the qs GW -BSE level, the two lowest states with pronounced CT characters can be found at 2.7 eV and these cannot directly be linked to charge separation pathways in PSII, which have been observed experimentally. 44 − 46 Only the third excited state at the qs GW -BSE level of theory at 1.91 eV contains a contribution from a Chl D1 + –Pheo D1 – particle-hole transition with a small weight, which is entirely absent in our TD-DFT and ev GW -BSE calculations. Future studies at the GW -BSE level with the inclusion of the environmental electrostatics are needed to rationalize how the Chl D1 + –Pheo D1 – CT state is influenced by the protein environment at the qs GW -BSE level.…”

“…The most complete model of the PSII RC we consider in this work comprises all six chromophores shown in Figure with 476 atoms in total. Time-resolved spectroscopic experiments − show that the primary electron transfer in the RC occurs from an exciton localized on Chl D1 to Pheo D1 , followed by a transfer of the hole to P D1 . This would point to the presence and possible mixing in of low-lying CT states with pronounced Chl D1 + –Pheo D1 – and P D1 + –Pheo D1 – characters in calculations of excitation energies.…”

“…In agreement with previous results and our own calculations on the TD-DFT/RSH level for the full hexameric complex also ev GW -BSE and qs GW -BSE only predict states with predominantly local characters in the absence of the protein environment. These states can therefore not be linked to the experimentally observed CT processes. − Recent computational studies have established that the environmental electrostatics are responsible for this type of CT. ,, Along the lines of previous GW -BSE implementations, ,, future research needs to focus on ways to explicitly account for the environmental electrostatics in large-scale GW -BSE calculations.…”

“…CC2 results are typically in good agreement with more involved methods like equation-of-motion (EOM) CC with singles and doubles (EOM-CCSD) or similarity-transformed (ST) EOM , -CCSD. , For these methods, we are aware of one study of a tetrameric model by Suomivuori et al using ADC(2) together with the spin-opposite-scaled and reduced-virtual-space (RVS) approximations. Unfortunately, they did not include the pheophytin chromophores in their calculations, which are known to play a key role in the initial charge separation immediately after photoexcitation. ,− This is potentially possible, but we note that most applications of wave function-based methods ,,, focus on single chromophores. Utilizing subsystem methods, − the applicability of these methods can be extended.…”

“…Unfortunately, they did not include the pheophytin chromophores in their calculations, which are known to play a key role in the initial charge separation immediately after photoexcitation. 14 , 44 − 46 This is potentially possible, but we note that most applications of wave function-based methods 18 , 20 , 47 , 48 focus on single chromophores. Utilizing subsystem methods, 49 − 55 the applicability of these methods can be extended.…”