Coherent nuclear dynamics at room temperature in bacterial reaction centers.

Abstract

A room-temperature study is reported of the femtosecond spectral evolution of the stimulated emission band of the primary electron-transfer precursor P* in bacterial photosynthesis. The study was performed with membranes of the antenna-deficient RCO1 mutant of Rhodobacter sphaeroides. A time-dependent red shift, reflecting nuclear motion out of the Franck-Condon region of the excited state, is resolved. Analysis of oscillatory features persisting for >1 ps in the kinetics revealed main frequencies of the activated motions at 30, 84, 145, and 192 cm-'. The oscillations occur on the time scale of primary electron transfer. Our results set a lower limit for the vibrational dephasing time in P* that is not compatible with the usual assumption in theoretical treatments of complete vibrational relaxation prior to electron transfer, even at room temperature.The primary charge separation in photosynthetic reaction centers (see refs. 1 and 2 for reviews) takes place between a donor (a bacteriochlorophyll dimer, P) and an acceptor (a bacteriopheophytin, HL) at a center-to-center distance of "17 A. The time scale of this reaction, about 3 ps at room temperature (3, 4), is extremely fast for a direct reaction spanning such a distance. As an additional monomeric bacteriochlorophyll (BL) is located in a configuration more or less bridging P and HL (5, 6), it has been put forward by many workers that the presence of BL may be the key to the extreme speed and efficiency of the reaction. In particular, it has been proposed that the state P+BL-is a real intermediate that is shorter lived than the P* precursor excited state (7,8) or, alternatively, that it is a virtual intermediate that mediates the reaction in a superexchange mechanism (9-11). Combinations of both mechanisms have also been proposed (12, 13). Very detailed analyses of short-lived transient absorption kinetics in terms of rate constants are at the center of the ongoing debate on the experimental basis for these models.From a theoretical point of view, these models are based on the conventional description of nonadiabatic electron transfer (ET), in which nuclear and electronic factors can be separated and contribute as independent factors to the ET rate (14-16). A crucial assumption in this description is that the vibrational modes of the precursor state of ET are thermally populated on the time scale of the reaction, which implies that vibrational relaxation and, if relaxation occurs via inelastic interactions with the bath, vibrational dephasing take place prior to ET.In this paper we will address the question of whether the hypothesis of vibrational dephasing prior to electron transfer is justified at room temperature and whether parameters other than a linear combination of exponentials may interfere in the analysis of ultrafast optical kinetics. Previous reports concerned the observation, at low temperature, of oscillatory features in bacterial reaction centers reflecting coherent motions in the P* state (17, 18). These specific low-frequency motions p...

Dynamical Theory of Primary Processes of Charge Separation in the Photosynthetic Reaction Center

“…The use of differential spectroscopy (in which absorption spectra with various delays are measured) has revealed a decisive role of oscillations of atomic nuclei in the ultrafast processes under discussion. This method has enabled one to observe activated coherent motions and oscillations in a bacterial reaction center and unambiguously related the occurrence of coherent motions with arising of a singlet excited P * state [19][20][21][22][23]29]. In [17], the arising of such oscillations was shown to be caused by energy modulation of an excited electron (making fast reversible transitions in the P * BH system) by nuclear dynamics.…”

“…In the modern view [1][2][3], monomeric bacteriochlorophyll B and bacteriopheophytin H also take part in the transfer ( Figure 1). Super-fast initial stages of the transfer were studied in detail in a number of RCs where the donor of an electron was a light-excited dimeric bacteriochlorophyll P * with a lifetime of the excited state of approximately ∼3×10 −10 s and the primary acceptor was bacteriopheophytin H [19][20][21][22][23]. The short lifetime of an excited dimeric P * necessitates the transfer to the monomer to be two orders of magnitude faster.…”

Ultrafast time-resolved vibrational spectroscopies of carotenoids in photosynthesis

“…As shown here spectral density includes meaningful information, however, there are scant reports on carotenoids bound to pigment-protein complexes [69]. On the other hand, many studies have already been performed on the coherent vibrations that directly reflect the effect of coupling with surrounding environment in bacteriochlorophyll [70][71][72][73][74][75][76][77]. To reveal the correlation among these coherent vibrations as well as the role of coherent vibration in excitation energy transfer is going to be important from now on.…”

Pump-Probe Spectroscopy, Photon Echoes and Vibrational Wavepackets

“…11.7A; [120,[122][123][124]), and also in photosynthetic bacterial reaction centers [27,125,126]. They typically damp out over the course of several picoseconds as a result of vibrational relaxations and dephasing.…”