Manifestation of Hydrogen Bonding and Exciton Delocalization on the Absorption and Two-Dimensional Electronic Spectra of Chlorosomes

Abstract

Chlorosomes are supramolecular aggregates that contain thousands of bacteriochlorophyll molecules. They perform the most efficient ultrafast excitation energy transfer of all natural light-harvesting complexes. Their broad absorption band optimizes light capture. In this study, we identify the microscopic sources of the disorder causing the spectral width and reveal how it affects the excited state properties and the optical response of the system. We combine molecular dynamics, quantum chemical calculations, and response function calculations to achieve this goal. The predicted linear and twodimensional electronic spectra are found to compare well with experimental data reproducing all key spectral features. Our analysis of the microscopic model reveals the interplay of static and dynamic disorder from the molecular perspective. We find that hydrogen bonding motifs are essential for a correct description of the spectral line shape. Furthermore, we find that exciton delocalization over tens to hundreds of molecules is consistent with the twodimensional electronic spectra.

Ultrafast Anisotropy Decay Reveals Structure and Energy Transfer in Supramolecular Aggregates

“…The ground and excited state partial charges were determined using the CHELPG scheme, as described in ref . The excitonic couplings J mn ( t ), i.e., the interactions that are responsible for the formation of the delocalized excitonic states, are calculated using the point dipole approximation. , However, it represents a good choice due to the restrictions coming from the computational cost connected with the large system size. Additionally, previous studies of helical cylindrical aggregates proved the utility and accuracy of this coupling scheme. ,,, The molecular transition dipole moment vectors μ⃗, responsible for excitonic coupling, are mapped onto the conformation of the BChl c molecules along the connection of the nitrogen atoms conventionally denoted N A and N C , as shown in Figure .…”

“…The high-temperature limit is a suitable approximation to describe the ultrafast processes that are of our interest . We calculate the linear and nonlinear optical responses in the perturbative regime using the response function formalism as implemented in NISE 2017 program. , The high computational cost of the 2D ES calculations, due to their scalingas N 3 with the number of molecules, restricts these simulations to smaller subsystems (see also ref . ), containing 2639 and 2675 molecules for System 1 and System 2, respectively.…”

“…The anisotropy is defined as the difference of the signal intensity I ⊥ obtained using the perpendicular, compared to the signal intensity I ∥ from the parallel pulse scheme, as given in eq r ( t ) = I ∥ ( t ) − I ⊥ ( t ) I ∥ ( t ) + 2 I ⊥ ( t ) Our simulations are in the impulsive limit, so we neglect pulse shape effects . We included effects of homogeneous and inhomogeneous broadening, caused by the presence of mesoscale disorder on the linear absorption and 2D ES spectra by weighting simulated response functions with exponential (τ homo = 300 fs) and Gaussian (τ inhomo = 166 fs) apodization functions, as reported previously in ref . The time scale responsible for inhomogeneous broadening is based on estimates from hole-burning studies …”

“…30 All of this supports our aim to create a more realistic description of chlorosomes that includes the effects of molecular scale disorder. 31 Previously, we established the connection between structural disorder on the scale of individual BChl c molecules and found that differences in hydrogen bonding result in a significant broadening of the spectra of individual chlorosomes. 31 Here, we aim to extend our investigations and show how the helical arrangements of BChl molecules within the chlorosome aggregates alter the spectral response and affect the exciton dynamics in the system, as probed in steady and time-resolved spectroscopy experiments.…”

“…31 Previously, we established the connection between structural disorder on the scale of individual BChl c molecules and found that differences in hydrogen bonding result in a significant broadening of the spectra of individual chlorosomes. 31 Here, we aim to extend our investigations and show how the helical arrangements of BChl molecules within the chlorosome aggregates alter the spectral response and affect the exciton dynamics in the system, as probed in steady and time-resolved spectroscopy experiments. 9,28,29,32−35 Our approach will be based on the simulation of linear and two-dimensional electronic spectra (2D ES) of two chlorosome model systems characterized with different macroscopic helicity.…”