Non-radiative relaxation of photoexcited chlorophylls: theoretical and experimental study.

William P Bricker,Yang Zhao,Cynthia S Lo,Howe-Siang Tan,Prathamesh M Shenai,Sebastian Fernandez-Alberti,Petar H Lambrev,Miriam Grace M Enriquez,Zhengtang Liu,Sergei Tretiak,Avishek Ghosh

doi:10.1038/srep13625

Abstract

Nonradiative relaxation of high-energy excited states to the lowest excited state in chlorophylls marks the first step in the process of photosynthesis. We perform ultrafast transient absorption spectroscopy measurements, that reveal this internal conversion dynamics to be slightly slower in chlorophyll B than in chlorophyll A. Modeling this process with non-adiabatic excited state molecular dynamics simulations uncovers a critical role played by the different side groups in the two molecules in governing the intramolecular redistribution of excited state wavefunction, leading, in turn, to different time-scales. Even given smaller electron-vibrational couplings compared to common organic conjugated chromophores, these molecules are able to efficiently dissipate about 1 eV of electronic energy into heat on the timescale of around 200 fs. This is achieved via selective participation of specific atomic groups and complex global migration of the wavefunction from the outer to inner ring, which may have important implications for biological light-harvesting function.

Highlights

The process of light-harvesting that marks the beginning of photosynthesis in different photosynthetic organisms is carried out by a variety of pigment molecules including chlorophylls, bacteriochlorophylls and carotenoids[1]
As described later in the text, in this work we have studied the internal conversion in monomeric chlorophyll molecules, the computational approach used can be readily extended in future to probe features of non-photochemical quenching (NPQ) by studying systems such as homodimers of chlorophylls or heterodimers of chlorophylls and carotenoids, which are speculated to act as excitation quenching sites in natural light-harvesting complexes
The dynamics of internal conversion in chlorophyll a (ChlA) and chlorophyll b (ChlB) solutions after excitation in the high energy B band was probed by femtosecond transient absorption (TA) spectroscopy

Summary

Introduction

The process of light-harvesting that marks the beginning of photosynthesis in different photosynthetic organisms is carried out by a variety of pigment molecules including chlorophylls, bacteriochlorophylls and carotenoids[1]. In secondary photosynthetic pigments such as carotenoids, significant efforts have revealed many interesting features of the internal conversion processes, which are perceived to be important in understanding their dual role in transferring the excitation energy absorbed in the blue region to the chlorophylls, and in participating in the photoprotective mechanisms of NPQ23–28. A recent computational study employing density functional theory based calculations on chlorophyll-carotenoid aggregates has proposed possible involvement of vibrational relaxation of carotenoid excited states in enhancing B to Q-band internal conversion in chlorophyll molecules[35]. We have systematically investigated the B to Q-band internal conversion processes in these two molecules by employing Non-Adiabatic Excited State Molecular Dynamics (NA-ESMD) simulations This methodology has been successfully used to simulate the ultrafast intramolecular redistribution and relaxation of the excess of electronic energy after photoexcitation in many large organic conjugated chromophores[36,37,38]. The role played by relatively minor structural differences between these molecules in the dynamics of relaxation of high-energy excited states has been revealed via analysis based on evolution of transition density localization

Methods

Results

Conclusion