Normal mode analysis of spectral density of FMO trimers: Intra- and intermonomer energy transfer.

Alexander Klinger,Dominik Lindorfer,Thomas Renger,Frank Müh

doi:10.1063/5.0027994

Alexander Klinger, Dominik Lindorfer + Show 2 more

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https://doi.org/10.1063/5.0027994

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Abstract

The intermolecular contribution to the spectral density of the exciton-vibrational coupling of the homotrimeric Fenna-Matthews-Olson (FMO) light-harvesting protein of green sulfur bacteria P. aestuarii is analyzed by combining a normal mode analysis of the protein with the charge density coupling method for the calculation of local transition energies of the pigments. Correlations in site energy fluctuations across the whole FMO trimer are found at low vibrational frequencies. Including, additionally, the high-frequency intrapigment part of the spectral density, extracted from line-narrowing spectra, we study intra- and intermonomer exciton transfer. Whereas the intrapigment part of the spectral density is important for fast intramonomer exciton relaxation, the intermolecular contributions (due to pigment-environment coupling) determine the intermonomer exciton transfer. Neither the variations of the local Huang-Rhys factors nor the correlations in site energy fluctuations have a critical influence on energy transfer. At room temperature, the intermonomer transfer in the FMO protein occurs on a 10 ps time scale, whereas intramonomer exciton equilibration is roughly two orders of magnitude faster. At cryogenic temperatures, intermonomer transfer limits the lifetimes of the lowest exciton band. The lifetimes are found to increase between 20 ps in the center of this band up to 100 ps toward lower energies, which is in very good agreement with the estimates from hole burning data. Interestingly, exciton delocalization in the FMO monomers is found to slow down intermonomer energy transfer, at both physiological and cryogenic temperatures.

Highlights

The Fenna–Matthews–Olson (FMO) protein mediates energy transfer between an outer antenna system in green sulfur bacteria, termed a chlorosome, and the reaction center complex
The intermolecular contribution to the spectral density of the exciton-vibrational coupling of the homotrimeric Fenna–Matthews–Olson (FMO) light-harvesting protein of green sulfur bacteria P. aestuarii is analyzed by combining a normal mode analysis of the protein with the charge density coupling method for the calculation of local transition energies of the pigments
The excitons become partially localized over just a few pigments, exciton relaxation corresponds to a spatially directed energy transfer toward the low-energy pigments, and the excess energy of excitons can be well dissipated by the vibrations

Summary

Introduction

The Fenna–Matthews–Olson (FMO) protein mediates energy transfer between an outer antenna system in green sulfur bacteria, termed a chlorosome, and the reaction center complex. The FMO protein is one of the first systems to which the newly developed 2D electronic spectroscopy was applied, revealing long-lived coherent oscillations that founded the field of quantum biology and brought this protein into the attention of a general audience from many different fields It is becoming more and more clear that the origin of the long-lived part of the oscillations is due to vibrational rather than electronic coherences.. It is becoming more and more clear that the origin of the long-lived part of the oscillations is due to vibrational rather than electronic coherences.21–23,26,27 It is not the protection of inter-exciton state coherences, but the equal strength of nearest neighbor pigment–pigment and local pigment–protein coupling that holds the key for efficient excitation energy transfer.. It is becoming more and more clear that the origin of the long-lived part of the oscillations is due to vibrational rather than electronic coherences. It is not the protection of inter-exciton state coherences, but the equal strength of nearest neighbor pigment–pigment and local pigment–protein coupling that holds the key for efficient excitation energy transfer. In this way, the excitons become partially localized over just a few pigments, exciton relaxation corresponds to a spatially directed energy transfer toward the low-energy pigments, and the excess energy of excitons can be well dissipated by the vibrations. A protection of inter-exciton state coherences would be detrimental for exciton relaxation.

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