Coherent intradimer dynamics in reaction centers of photosynthetic green bacterium Chloroflexus aurantiacus

Abstract

early-time dynamics of absorbance changes (light minus dark) in the long-wavelength Q y absorption band of bacteriochlorophyll dimer p of isolated reaction centers (Rcs) from thermophilic green bacterium Chloroflexus (Cfx.) aurantiacus was studied by difference pump-probe spectroscopy with 18-fs resolution at cryogenic temperature. It was found that the stimulated emission spectrum gradually moves to the red on the ~100-fs time scale and subsequently oscillates with a major frequency of ~140 cm −1. By applying the non-secular Redfield theory and linear susceptibility theory, the coherent dynamics of the stimulated emission from the excited state of the primary electron donor, bacteriochlorophyll dimer p*, was modeled. The model showed the possibility of an extremely fast transition from the locally excited state p 1 * to the spectrally different excited state P 2 *. this transition is clearly seen in the kinetics of the stimulated emission at 880 and 945 nm, where mostly P 1 * and p 2 * states emit, respectively. These findings are similar to those obtained previously in RCs of the purple bacterium Rhodobacter (Rba.) sphaeroides. the assumption about the existence of the second excited state p 2 * helps to explain the complicated temporal behavior of the ΔA spectrum measured by pumpprobe spectroscopy. It is interesting that, in spite of the strong coupling between the P 1 * and p 2 * states assumed in our model, the form of the coherent oscillations is mainly defined by pure vibrational coherence in the excited states. A possible nature of the p 2 * state is discussed. Photosynthesis is a grandiose natural phenomenon of conversion of solar energy into stable energy of chemical compounds. Very shortly, absorption of light by pigment molecules creates an excited state, the energy of which is further used in a long sequence of biophysical and biochemical events. A first step in this sequence is charge separation occurring in special pigment-protein complexes, reaction centers (RCs). The conversion of light energy into free energy of charge-separated states occurs in RCs on a picosecond time scale. The well-studied RCs of the photosynthetic purple bacterium Rhodobacter (Rba.) sphaeroides contain two exciton-coupled bacteriochlorophylls (P A and P B), two bacteriochlorophylls (B A and B B) in monomeric form, two bacteriopheophytins (H A and H B), two quinones (Q A and Q B) and a Fe atom. A spatial arrangement of the pigments is conserved by protein matrix. According to X-ray structure analysis, the pigments form two symmetrical branches, P A

Dynamics of the Excited State in Photosynthetic Bacterial Reaction Centers

“…The sharp features illustrated at early times in Figure A,B are qualitatively similar to the features that are seen experimentally in stimulated emission from reaction centers. ,,− They depend on the number, frequencies, and Huang–Rhys parameters of the vibrational modes in the model, and they would be smoothed by convolution with lineshape and instrumental-response functions. The aim here is not to reproduce the signals from any particular experiment in detail, but just to note that, because the spectroscopic properties of P depend on coupling to multiple low-energy vibrational modes, , pure dephasing of these modes can have significant effects on stimulated emission at early times.…”

“…When it is excited by light, P transfers an electron to a neighboring bacteriochlorophyll (B L ), forming a radical pair (P + B L – ) that sends an electron on to a chain of secondary carriers. Several investigators have proposed that the initial reaction proceeds in two discrete steps. − They suggest that excitation first promotes P to its lowest exciton state (P*), after which an electron moves from P L to P M to form an internal charge-transfer (CT) state (P L + P M – ), and that the anionic radical P M – then transfers an electron to B L : …”

“…Evidence for an intermediate between P* and P + B L – has come from time-resolved pump-probe and two-dimensional (2D) electronic spectroscopy. During the first 200 fs after the reaction centers are excited in their long-wavelength absorption band, stimulated emission from the excited state weakens and shifts to the red, while the absorbance increases around 1080 nm and in IR vibrational bands between 1000 and 1600 cm –1 . − ,,− These events precede absorbance changes that signal reduction of B L and the next electron acceptor, which takes several picoseconds. Although identifications of the putative intermediate as P L + P M – have been tentative, quantum calculations indicate that a CT state mixes strongly with the P* exciton state and that electron density moves from P L to P M when the dimer is excited. ,− This movement of charge could facilitate transfer to B L because B L is closer to P M than to P L . ,− Rapid electronic relaxation from P* to P L + P M – also has been suggested as a possible explanation for the long-wavelength absorption band’s broad homogeneous width and relatively small cross sections for resonance Raman absorption. − …”