Vibronic Coherence in the Charge Separation Process of the Rhodobacter sphaeroides Reaction Center

Abstract

Two-dimensional electronic spectroscopy was applied to a variant of the reaction center (RC) of purple bacterium Rhodobacter sphaeroides lacking the primary acceptor ubiquinone in order to understand the ultrafast separation and transfer of charge between the bacteriochlorin cofactors. For the first time, characteristic 2D spectra were obtained for the participating excited and charge-transfer states, and the electron-transfer cascade (including two different channels, the P* and B* channels) was fully mapped. By analyzing quantum beats using 2D frequency maps, excited-state vibrational modes at 153 and 33 cm–1 were identified. We speculate that these modes couple to the charge separation (CS) process and collectively optimize the CS and are responsible for the superhigh efficiency.

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.…”

Theory of delocalised charge transfer​​​​​​​

“…The coupling of charge transfer states to nuclear modes was suggested to play a functional role in the efficiency of charge transfer since the 1990s 105,106 , and recent work with 2DES has detected quantum beats at a number of frequencies that correlate with charge transfer, exciton, and vibrational states at room temperature [106][107][108] . As such, vibronic coherences have been suggested to play an active role in charge separation at physiological temperatures in both bacterial and oxygenic photosynthesis 43,98,[106][107][108][109] . Although the mere presence of quantum beating doesn't mean that coherence is playing a functional role in charge separation, this is an active field study that is currently seeing much activity.…”

“…All RCs are dimeric, with two branches that only interact at a strongly coupled special pair (P) of chlorophyll (Chl) or bacteriochlorophyll (BChl) molecules. P is the dominant acceptor of excitons from antenna complexes and the primary charge donor [142][143][144] . From P, the charges are transferred down either branch in homodimeric RCs (such as heliobacteria 74,83 ) or down only one branch in heterodimers.…”

“…Analysing Explanation 6 requires understanding how the dimerisation affected the exciton-and charge-transfer functions in the RC. Intriguingly, the constituent pigments within P are the only ones in the RC close enough to influence each other, meaning that the part of the RC most affected by dimerisation is also both the ultimate acceptor of excitonic energy and the location of charge separation [142][143][144] . Therefore, to understand the role of dimerisation, we must consider how both exciton transfer to P and charge transfer out of it would have been affected by dimerisation.…”

“…We determined the limits of the parameter space by considering modern RCs. We assume that the monomer was no faster at EET or CT than modern RCs, implying that the monomer EET and CT rates are less than the natural rates: k mon EET ≤ 10 11 s −1 and k mon CT ≤ 10 12 s −1 34,143,144,154 . We also assume that these rates are larger than the recombination rate k mon rec = 10 9 s −1 , which is assumed constant, essentially setting the timescale.…”