Two-dimensional electronic spectroscopy of bacteriochlorophyll a in solution: Elucidating the coherence dynamics of the Fenna-Matthews-Olson complex using its chromophore as a control

Abstract

Following the observation of long-lived coherences in the two-dimensional (2D) electronic spectra of the Fenna-Matthews-Olson (FMO) complex, many theoretical works suggest that coherences between excitons may play a role in the efficient energy transfer that occurs in photosynthetic antennae. This interpretation of the dynamics depends on the assignment of quantum beating signals to superpositions of excitons, which is complicated by the possibility of observing both electronic and vibrational coherences in 2D spectra. Here, we explore 2D spectra of bacteriochlorophyll a (BChla) in solution in an attempt to isolate vibrational beating signals in the absence of excitonic signals to identify the origin of the quantum beats in 2D spectra of FMO. Even at high laser power, our BChla spectra show strong beating only from the nonresonant response of the solvent. The beating signals that we can conclusively assign to vibrational modes of BChla are only slightly above the noise and at higher frequencies than those previously observed in spectra of FMO. Our results suggest that the beating observed in spectra of FMO is of a radically different character than the signals observed here and can therefore be attributed to electronic coherences or intermolecular degrees of freedom.

Impact of environmentally induced fluctuations on quantum mechanically mixed electronic and vibrational pigment states in photosynthetic energy transfer and 2D electronic spectra

“…27 In general, the Huang-Rhys factors of BChl are small, 45 and the factor associated with the vibrational mode in this work is set to S = 0.025, 27 which is within the range of the experimentally measured values.…”

“…Indeed, the recent 2D electronic experiments on BChl molecules in solution did not find significant vibrational coherence. 45 In relation to this, Christensson et al 21 proposed that resonance be- …”

Vibration-assisted resonance in photosynthetic excitation-energy transfer

“…The primary effect of the resonance is an enhancement of the energy transfer efficiency, which was not addressed in that particular experiment. Another experiment designed to compare the 2D spectra of Bchl a in solution with the spectra of FMO was unable to resolve more than two vibrational modes, which had frequencies well above those relevant for our model [34]. Neither of these experiments would seem to rule out a vibrationassisted resonance mechanism.…”

Electronic energy transfer through non-adiabatic vibrational-electronic resonance. I. Theory for a dimer

“…The proposed explanation was that the antenna protein holding the pigments somehow preserves electronic coherence. 11 Several investigations of these oscillations reported signatures consistent with hypotheses of purely electronic coherence between different excitons spanning more than one pigment 13,14 and reversible energy flow between pigments and bath, termed quantum energy transport. 19 Parallel theoretical studies 20,21 on several different antennas have proposed a modified hypothesis that vibrational-electronic mixing allows coherence between excited states of the antenna to generate oscillations with amplitudes characteristic of electronic coherence and picosecond decays characteristic of vibrational coherence.…”

“…8,9 In this regime, a pioneering paper by Womick energy transfer and increase the energy transfer rate by an order of magnitude. 10 Over the last several years, experiments on photosynthetic antennas [11][12][13][14][15] and reaction centers 16,17 using femtosecond two-dimensional (2D) electronic spectroscopy 18 have revealed that energy transfer in these systems is associated with oscillations in 2D peak amplitude, shape, and phase which last for picoseconds. 12 The first 2D study reporting these oscillations 11 raised the puzzle that they had an amplitude too strong for the Franck-Condon excitation of vibrations in the isolated pigments but a decay time significantly longer than usual for electronic coherence in the condensed phase.…”