Abstract
In the primary step of natural light-harvesting, the energy of a solar photon is captured in antenna chlorophyll as a photoexcited electron-hole pair, or an exciton. Its efficient conversion to stored chemical potential occurs in the special pair reaction center, which has to be reached by down-hill ultrafast excited state energy transport. Key to this process is the degree of interaction between the chlorophyll chromophores that can lead to spatial delocalization and quantum coherence effects. The importance of quantum contributions to energy transport depends on the relative coupling between the chlorophylls in relation to the intensity of the fluctuations and reorganization dynamics of the surrounding protein matrix, or bath. The latter induce uncorrelated modulations of the site energies, resulting in quantum decoherence, and localization of the spatial extent of the exciton. The current consensus is that under physiological conditions quantum decoherence occurs on the 10 fs time scale, and quantum coherence plays little role for the observed picosecond energy transfer dynamics. In this work, we reaffirm this from a different point of view by finding that the true onset of important electronic quantum coherence only occurs at extremely low temperatures of ~20 K. We have directly determined the exciton coherence times using two-dimensional (2D) electronic spectroscopy of the Fenna-Matthew-Olson (FMO) complex over an extensive temperature range. At 20 K, we show that electronic coherences persist out to 200 fs (close to the antenna) and marginally up to 500 fs at the reaction-center side. The electronic coherence is found to decay markedly faster with modest increases in temperature to become irrelevant above 150 K. This temperature dependence also allows disentangling the previously reported long-lived beatings thought to be evidence for electronic quantum coherence contributions. We show that they result from mixing vibrational coherences in the electronic ground state. We also uncover the relevant electronic coherence between excited electronic states and examine the temperature-dependent non-Markovianity of the transfer dynamics to show that the bath involves uncorrelated motions even to low temperatures. The observed temperature dependence allows a clear separation of the fragile electronic coherence from the robust vibrational coherence. The specific details of the critical bath interaction are treated through a theoretical model based on measured bath parameters that reproduces the temperature dependent dynamics. By this, we provide a complete picture of the bath interaction which places these systems in the regime of strong bath coupling. We believe this main conclusion to be generically valid for light harvesting systems. This principle makes the systems robust against otherwise fragile quantum effects as evidenced by the strong temperature dependence. We conclude that nature explicitly exploits decoherence or dissipation in engineering site energies to yield downhill energy gradients to unerringly direct energy, even on the fastest time scales of biological processes.
Temperature dependence of free volume distributions in polymers studied by positron lifetime spectroscopy
