Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes

Abstract

Chlorosomes are the largest and most efficient light-harvesting antennae found in nature, and they are constructed from hundreds of thousands of self-assembled bacteriochlorophyll (BChl) c, d, or e pigments. Because they form very large and compositionally heterogeneous organelles, they had been the only photosynthetic antenna system for which no detailed structural information was available. In our approach, the structure of a member of the chlorosome class was determined and compared with the wild type (WT) to resolve how the biological light-harvesting function of the chlorosome is established. By constructing a triple mutant, the heterogeneous BChl c pigment composition of chlorosomes of the green sulfur bacteria Chlorobaculum tepidum was simplified to nearly homogeneous BChl d. Computational integration of two different bioimaging techniques, solid-state NMR and cryoEM, revealed an undescribed syn-anti stacking mode and showed how ligated BChl c and d self-assemble into coaxial cylinders to form tubular-shaped elements. A close packing of BChls via pi-pi stacking and helical H-bonding networks present in both the mutant and in the WT forms the basis for ultrafast, long-distance transmission of excitation energy. The structural framework is robust and can accommodate extensive chemical heterogeneity in the BChl side chains for adaptive optimization of the light-harvesting functionality in low-light environments. In addition, syn-anti BChl stacks form sheets that allow for strong exciton overlap in two dimensions enabling triplet exciton formation for efficient photoprotection.

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

“…Our CD spectrum agrees with the one reported by Saga et al [24] and the recently measured spectra for the three-point mutant [25]. Our simulated result further supports the supramolecular structure proposed by Ganapathy et al [19] Figure 4b shows the peak positions of the absorption maximum and the LES as a function of σ. The peak positions are overestimated compared with the experiments [25].…”

“…Therefore, the first component reflecting the coherent energy transfer may be similar for the wild type and the three-point mutant. We also expect that the second component describing the inter-layer EET is similar for the wild type and the three-point mutant, because the same 2.1 nm spacing was observed for both the wild type and the three-point mutant [3,19]. The third component describing the energy equilibration over the roll is sensitive to a radius of the roll.…”

“…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]. We utilize the aggregate model from [19] to calculate excitation dynamics and optical response of C. tepidum assuming that the structural dissimilarity between the mutant and the wild type of bacteria is small and its influence on EET within the chlorosome is negligible.…”

“…Additionally, the aggregate structure proposed in [19] have been supported by two-dimensional polarization fluorescence microscopy experiments [21]. We utilize the aggregate model from [19] to calculate excitation dynamics and optical response of C. tepidum assuming that the structural dissimilarity between the mutant and the wild type of bacteria is small and its influence on EET within the chlorosome is negligible. In the model of Ganapathy et al [19] (Figure 1a) syn-anti monomer stacks ( Figure 1b) are basic building blocks of the aggregate.…”

“…We utilize the aggregate model from [19] to calculate excitation dynamics and optical response of C. tepidum assuming that the structural dissimilarity between the mutant and the wild type of bacteria is small and its influence on EET within the chlorosome is negligible. In the model of Ganapathy et al [19] (Figure 1a) syn-anti monomer stacks ( Figure 1b) are basic building blocks of the aggregate. The stacks form rings that are organized into helical cylinders.…”