Absorption Linear Dichroism Measured Directly on a Single Light-Harvesting System: The Role of Disorder in Chlorosomes of Green Photosynthetic Bacteria

Abstract

Chlorosomes are light-harvesting antennae of photosynthetic bacteria containing large numbers of self-aggregated bacteriochlorophyll (BChl) molecules. They have developed unique photophysical properties that enable them to absorb light and transfer the excitation energy with very high efficiency. However, the molecular-level organization, that produces the photophysical properties of BChl molecules in the aggregates, is still not fully understood. One of the reasons is heterogeneity in the chlorosome structure which gives rise to a hierarchy of structural and energy disorder. In this report, we for the first time directly measure absorption linear dichroism (LD) on individual, isolated chlorosomes. Together with fluorescence-detected three-dimensional LD, these experiments reveal a large amount of disorder on the single-chlorosome level in the form of distributions of LD observables in chlorosomes from wild-type bacterium Chlorobaculum tepidum . Fluorescence spectral parameters, such as peak wavelength and bandwidth, are measures of the aggregate excitonic properties. These parameters obtained on individual chlorosomes are uncorrelated with the observed LD distributions and indicate that the observed disorder is due to inner structural disorder along the chlorosome long axis. The excitonic disorder that is also present is not manifested in the LD distributions. Limiting values of the LD parameter distributions, which are relatively free of the effect of structural disorder, define a range of angles at which the excitonic dipole moment is oriented with respect to the surface of the two-dimensional aggregate of BChl molecules. Experiments on chlorosomes of a triple mutant of Chlorobaculum tepidum show that the mutant chlorosomes have significantly less inner structural disorder and higher symmetry, compatible with a model of well-ordered concentric cylinders. Different values of the transition dipole moment orientations are consistent with a different molecular level organization of BChl's in the mutant and wild-type chlorosomes.

Strong coupling between chlorosomes of photosynthetic bacteria and a confined optical cavity mode

“…57), and the average angle between the transition dipoles and the chlorosome's main axis is about 28°( ref. 58). It is likely that the spin-coating process does result in some preferential orientation of chlorosomes in the plane of the film.…”

Theoretical characterization of excitation energy transfer in chlorosome light-harvesting antennae from green sulfur bacteria

“…In order to reveal molecular alignment in BChl aggregates the authors utilized a solid-state nuclear magnetic resonance technique combined with cryo-EM imaging. Linear dichroism spectra of individual chlorosomes [20] confirm that the chlorosomes from the mutant bacteria are less disordered than those from the wild type. Additionally, the aggregate structure proposed in [19] have been supported by two-dimensional polarization fluorescence microscopy experiments [21].…”

Exciton Transport in Molecular Aggregates – From Natural Antennas to Synthetic Chromophore Systems

“…[180,181,[183][184][185][186] This has recently been applied to the bchR mutant from Cba. Tepidum, [187] see Figure 9c.…”