Vibronic mixing enables ultrafast energy flow in light-harvesting complex II

Eric A Arsenault,Krishna K Niyogi,Graham R Fleming,Yusuke Yoneda,Masakazu Iwai

doi:10.1038/s41467-020-14970-1

Abstract

Since the discovery of quantum beats in the two-dimensional electronic spectra of photosynthetic pigment-protein complexes over a decade ago, the origin and mechanistic function of these beats in photosynthetic light-harvesting has been extensively debated. The current consensus is that these long-lived oscillatory features likely result from electronic-vibrational mixing, however, it remains uncertain if such mixing significantly influences energy transport. Here, we examine the interplay between the electronic and nuclear degrees of freedom (DoF) during the excitation energy transfer (EET) dynamics of light-harvesting complex II (LHCII) with two-dimensional electronic-vibrational spectroscopy. Particularly, we show the involvement of the nuclear DoF during EET through the participation of higher-lying vibronic chlorophyll states and assign observed oscillatory features to specific EET pathways, demonstrating a significant step in mapping evolution from energy to physical space. These frequencies correspond to known vibrational modes of chlorophyll, suggesting that electronic-vibrational mixing facilitates rapid EET over moderately size energy gaps.

Highlights

Since the discovery of quantum beats in the two-dimensional electronic spectra of photosynthetic pigment-protein complexes over a decade ago, the origin and mechanistic function of these beats in photosynthetic light-harvesting has been extensively debated
One major advantage of probing in this region, as opposed to the lower frequency region, which is energetically closer to the exciton energy gaps, is that since there is no anharmonic coupling between low and high frequency vibrational modes, the dynamics observed via probing the higher frequency modes are free from the modulation effects caused by the creation of low(er) frequency vibrational wavepackets
Concluding comments. 2DEV spectroscopy provides a powerful way to untangle the connection between congested electronic spectra and complex ultrafast dynamics, such as energy transfer (EET)

Summary

Introduction

Since the discovery of quantum beats in the two-dimensional electronic spectra of photosynthetic pigment-protein complexes over a decade ago, the origin and mechanistic function of these beats in photosynthetic light-harvesting has been extensively debated. We examine the interplay between the electronic and nuclear degrees of freedom (DoF) during the excitation energy transfer (EET) dynamics of light-harvesting complex II (LHCII) with two-dimensional electronic-vibrational spectroscopy. The assignment of beats as vibronic in origin does not necessarily demonstrate that electronic-vibrational mixing influences energy transport In response to such a question, the mechanistic role of vibronic coupling in facilitating EET has received significant theoretical attention, the conclusions can vary widely as there remains no uniform treatment of electronic-vibrational mixing[19–27]. Recent work has successfully unveiled the presence of vibronic coupling in natural and artificial lightharvesting systems[28–34], the newly developed technique of twodimensional electronic-vibrational (2DEV) spectroscopy[7,35–44], 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. The center line slopes (CLSs) of the spectral features being related to a cross correlation of vibrational and electronic dipoles, as opposed to the autocorrelation relationship of conventional, degenerate a b

Methods

Results

Discussion

Conclusion