Non-classicality of the molecular vibrations assisting exciton energy transfer at room temperature

Abstract

Advancing the debate on quantum effects in light-initiated reactions in biology requires clear identification of non-classical features that these processes can exhibit and utilize. Here we show that in prototype dimers present in a variety of photosynthetic antennae, efficient vibration-assisted energy transfer in the sub-picosecond timescale and at room temperature can manifest and benefit from non-classical fluctuations of collective pigment motions. Non-classicality of initially thermalized vibrations is induced via coherent exciton–vibration interactions and is unambiguously indicated by negativities in the phase–space quasi-probability distribution of the effective collective mode coupled to the electronic dynamics. These quantum effects can be prompted upon incoherent input of excitation. Our results therefore suggest that investigation of the non-classical properties of vibrational motions assisting excitation and charge transport, photoreception and chemical sensing processes could be a touchstone for revealing a role for non-trivial quantum phenomena in biology.

Scalable High-Performance Algorithm for the Simulation of Exciton Dynamics. Application to the Light-Harvesting Complex II in the Presence of Resonant Vibrational Modes

“…It has been suggested that the vibrations might be tuned in resonance in order to improve inter-band energy transfer from the energetically higher-lying Chlb sites to the Chla band. 29 An experimental assessment of the impact of specific vibrational modes by 2d-echo spectroscopy is complicated due to superposition of ground-state vibrations and excited-state absorption signals on top of the stimulated emission pathway, which for specific systems overshadow electronic coherences. 10,53 For the FMO complex, added resonant modes hardly diminish or enhance transfer efficiencies.…”

“…16,30 Previous works focus on dimer pairs as representatives for Chlb/Chla transfer-pathways in LHC II and suggest non-classical phenomena and vibration-assisted transfer in the model system. 29 A typical dimer-pair is given by Chlb 601 and Chla 602 with an energy splitting chosen close to resonance with the intra-molecular vibration peak at Ω vib = 742 cm −1 .…”

“…There is an ongoing debate if underdamped modes in LHCs are tuned to resonance to enhance the transfer efficiency. 28,29 It has been suggested that non-classical phenomena and vibration-assisted transfer through resonantly coupled underdamped modes enhances Chlb/Chla inter-band relaxation in LHC II. 29 For the Fenna-Matthews-Olson (FMO) complex and dimer models computations with HEOM and the quasi-adiabatic path integral (QUAPI) show that added underdamped modes act as additional dissipative channels, which do not alter the transfer efficiency appreciably.…”

“…28,29 It has been suggested that non-classical phenomena and vibration-assisted transfer through resonantly coupled underdamped modes enhances Chlb/Chla inter-band relaxation in LHC II. 29 For the Fenna-Matthews-Olson (FMO) complex and dimer models computations with HEOM and the quasi-adiabatic path integral (QUAPI) show that added underdamped modes act as additional dissipative channels, which do not alter the transfer efficiency appreciably. 16,30,31 However, 2d echo-spectra are more susceptible to vibrational modes and reflect both, electronic and vibrational effects.…”

Quantum modeling of ultrafast photoinduced charge separation

“…This coupling is proposed to be the source of long-lived oscillations observed in time-resolved spectroscopies in several systems (see section 4). In addition, some authors stress the ultimate quantum nature of vibration-assisted exciton transport and claim that it is achieved via non-classical fluctuations of collective pigment motions [142].…”