Vibronic coupling explains the ultrafast carotenoid-to-bacteriochlorophyll energy transfer in natural and artificial light harvesters

Abstract

The initial energy transfer steps in photosynthesis occur on ultrafast timescales. We analyze the carotenoid to bacteriochlorophyll energy transfer in LH2 Marichromatium purpuratum as well as in an artificial light-harvesting dyad system by using transient grating and two-dimensional electronic spectroscopy with 10 fs time resolution. We find that Förster-type models reproduce the experimentally observed 60 fs transfer times, but overestimate coupling constants, which lead to a disagreement with both linear absorption and electronic 2D-spectra. We show that a vibronic model, which treats carotenoid vibrations on both electronic ground and excited states as part of the system's Hamiltonian, reproduces all measured quantities. Importantly, the vibronic model presented here can explain the fast energy transfer rates with only moderate coupling constants, which are in agreement with structure based calculations. Counterintuitively, the vibrational levels on the carotenoid electronic ground state play the central role in the excited state population transfer to bacteriochlorophyll; resonance between the donor-acceptor energy gap and the vibrational ground state energies is the physical basis of the ultrafast energy transfer rates in these systems.

Ultrafast energy transfer with competing channels: Non-equilibrium Förster and Modified Redfield theories

“…In this section we calculate transfer rates for a model donor-acceptor system motivated by previously studied carotenoid-chlorophyll and carotenoid-purpurin dyads [47]. The dyads in Ref.…”

“…We are motivated by our recent study of ultrafast energy transfer between the bright S 2 state of a carotenoid molecule and the second lowest excited state, the socalled Q x state, of (bacterio)chlorophyll ((B)Chl) and related molecules [47]. By means of an explicit nonperturbative treatment of carotenoid vibrational modes, it was possible to show in Ref.…”

Vibrational relaxation beyond the linear damping limit in two-dimensional optical spectra of molecular aggregates

“…We have studied relative oscillatory phase between diagonal and cross peaks of 2D spectra and its temperature sensitivity for a generic vibronic dimer (P-model) and monomer (V-model) [14]. Vibronic dimer was next used as a model for transient grating (TG) studies of exciton transfer from carotenoid's S2 to bacteriochlorophyll Qx [4] and similar study for perylene complexes is in preparation [16]. The code was also used to look into the electronic vibrational dynamics of (monomers of) hypericin [15] Details of the application are summarized in the following …”

“…Two dimensional optical spectra [1][2][3] of molecular aggregates shows almost invariantly important role of vibrations on relaxation and electronic transport [4] within organic dyes, light harvesters and similar molecular systems of intensive interest. Interplay of vibrational and electronic dynamics is a computational challenge which has been approached on the various level of theory [5].…”

“…In the present communication we report a dynamical model of vibronic dynamics affordable for small (dimers, trimers) molecular aggregates with resolved vibrational structure which we have implemented recently to inquire phase relation in vibronic systems [14], and further used it for simulation of 2D spectra of carotenoid-chlorophyll dyad [4], and transient grating on hypericin [15]. Few others applications (perylene dimers) are yet in preparation [16].…”