Ultrafast energy transfer within the photosystem II core complex

Abstract

We report 2D electronic spectroscopy on the photosystem II core complex (PSII CC) at 77 K under different polarization conditions. A global analysis of the high time-resolution 2D data shows rapid, sub-100 fs energy transfer within the PSII CC. It also reveals the 2D spectral signatures of slower energy equilibration processes occurring on several to hundreds of picosecond time scales that are consistent with previous work. Using a recent structure-based model of the PSII CC [Y. Shibata, S. Nishi, K. Kawakami, J. R. Shen and T. Renger, J. Am. Chem. Soc., 2013, 135, 6903], we simulate the energy transfer in the PSII CC by calculating auxiliary time-resolved fluorescence spectra. We obtain the observed sub-100 fs evolution, even though the calculated electronic energy shows almost no dynamics at early times. On the other hand, the electronic-vibrational interaction energy increases considerably over the same time period. We conclude that interactions with vibrational degrees of freedom not only induce population transfer between the excitonic states in the PSII CC, but also reshape the energy landscape of the system. We suggest that the experimentally observed ultrafast energy transfer is a signature of excitonic-polaron formation.

The origin of unidirectional charge separation in photosynthetic reaction centers: nonadiabatic quantum dynamics of exciton and charge in pigment–protein complexes

“…exciton. [1][2][3][4][5][6][7] Exciton charge separation necessitates a sufficient potential difference between the donor and acceptor of electrons for overcoming the electron-hole Coulomb binding energy.…”

“…Photosystem II (PSII) consists of core antenna complexes (CP43 and CP47) and a reaction center (RC). [1][2][3][4] Chlorophyll a (Chl) molecules in CP43 and CP47 mediate exciton transfers to the RC consisting of Chls (P D1 , P D2 , Chl D1 , and Chl D2 ), pheophytin a (Pheo D1 and Pheo D2 ), and plastoquinone (Q A and Q B ) (Fig. 1).…”

“…The charge separation pathways in pigment-protein complexes can be determined by various factors including energetics, electronic coupling, vibronic coupling, and quantum effects. [2][3][4][18][19][20][21]31,[44][45][46] In this study, 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.…”

Vibronic mixing enables ultrafast energy flow in light-harvesting complex II

“…The commonly employed technique of twodimensional electronic spectroscopy (2DES) often lacks the spectral resolution to untangle the complex, congested spectra of relevant systems-making it challenging to discern whether or not an oscillatory feature is electronic, vibrational, or vibronic in nature 21 . Although recent work has successfully unveiled the presence of vibronic coupling in natural and artificial lightharvesting systems [28][29][30][31][32][33][34] , the newly developed technique of twodimensional electronic-vibrational (2DEV) spectroscopy 7,[35][36][37][38][39][40][41][42][43][44] , by focusing on vibrational transitions in the final light-matter interaction, has the potential to provide significantly improved experimental input into the interplay of electronic and nuclear dynamics in ultrafast energy (and charge) transfer. Several aspects of 2DEV spectroscopy are significant in this regard.…”

Revealing a full quantum ladder by nonlinear spectroscopy

“…In the visible optical regime, the 4WM measurements mainly demonstrate the properties of the single exciton manifold in -k 1 + k 2 + k 3 and k 1 -k 2 + k 3 configurations. The single excitation manifold is very important in physical chemistry as the single excitations are the main players in excitation transport, charge separation, charge transport processes in molecular and biological functional systems [17][18][19][20][21][22][23][24].…”