Ultrafast Anisotropy Decay Reveals Structure and Energy Transfer in Supramolecular Aggregates

Abstract

Chlorosomes from green bacteria perform the most efficient light capture and energy transfer, as observed among natural light-harvesting antennae. Hence, their unique functional properties inspire developments in artificial light-harvesting and molecular optoelectronics. We examine two distinct organizations of the molecular building blocks as proposed in the literature, demonstrating how these organizations alter light capture and energy transfer, which can serve as a mechanism that the bacteria utilize to adapt to changes in light conditions. Spectral simulations of polarization-resolved two-dimensional electronic spectra unravel how changes in the helicity of chlorosomal aggregates alter energy transfer. We show that ultrafast anisotropy decay presents a spectral signature that reveals contrasting energy pathways in different chlorosomes.

Observation of Dark States in Two-Dimensional Electronic Spectra of Chlorosomes

“…Such a large system size allows us to estimate statistical distributions of excitonic parameters that reflect the presence of molecular-scale disorder. The agreement between the absorption spectra of these two systems shows that the chosen small model is a good candidate for performing 2DES calculations, as shown previously (Figure S4 in ref 47).…”

“…Here, the exciton states have an overall approximately isotropic distribution of the direction of transition dipole moments, i.e., the excitonic transition dipole moments span all possible angles with the long axis of the cylinder. 47 The time evolution of the exciton states is calculated using the NISE code 41,42,57 that solves the time-dependent Schrodinger equation numerically…”

“…The current work builds on a model developed and refined in multiple steps in refs ( 18 , 44 , 46 , 47 , 49 ). We will focus on the Q y band 21 arising from the strongly coupled Q y transitions of BChl c in chlorosomes and represent the excited states using a Frenkel exciton Hamiltonian accounting for both structural and energetic disorder 50 …”

“…40 Here, we will use a quantum-classical approach 41,42 to simulate the 2DES spectra of a single chlorosome cylinder up to 500 fs waiting time and compare the results to experimental observations. 29 Since we use an atomistic model 43 of chlorosomal supramolecular aggregates 18,44,45 to simulate spectroscopic observables, 46,47 we can provide information on the molecular mechanisms behind ultrafast exciton transfer in chlorosomes without relying on fitting or on a prior assumption of a specific mechanism. We identify spectral signatures in the 2DES spectra of chlorosomes that arise due to the participation of low-lying dark states 48 in the exciton dynamics.…”

Contrasting packing modes for tubular assemblies in chlorosomes

“…The BChls in chlorosomes are thought to form syn-anti parallel stacks that self-assemble in polar chiral sheets, and concentric tubes with varying curvature where the dipole moments are partially averaged over the circumference of the cylinders and a net dipole moment is established for the light harvesting function (van Rossum et al 2001;Ganapathy et al 2009;Günther et al 2016;Li et al 2018;Eric et al 2023a). Both 13 C Magic Angle Spinning (MAS) NMR and optical spectroscopy have revealed two distinct spectral fractions with remarkably small inhomogeneous linewidths approaching ~ 1 ppm in the 13 C NMR and ~ 100 cm -1 in optical data (Balaban et al 1995;Psencik et al 1994;Günther et al 2016).…”