MAS NMR Structures of Aggregated Cadmium Chlorins Reveal Molecular Control of Self-Assembly of Chlorosomal Bacteriochlorophylls

Magic angle spinning NMR spectroscopy has been used to investigate the self-organization of bacteriochlorophylls in chlorosomal light-harvesting antennae. Two model cadmium chlorins were studied that were uniformly 13C and 15N enriched in the ring moieties. The chlorin models differ from the natural BChl c in the central metal and the 3-, 12-, 17-, and 20-side chains. One model system has the farnesyl tail replaced by a methyl, whereas the other has a stearyl tail. The 113Cd MAS NMR signals indicate a five-coordination of the Cd metal. In particular, the combined NMR data show a HO···Cd coordination, very similar to the HO···Mg coordination in the natural system. Anomalously large 1H ring-current shifts of up to 10 ppm reveal a dense orderly stacking of the molecules in planar layers, for which a correlation length of at least 24 Å was defined from long-range ring-current shift calculations. In addition, our model structures confirm and validate the essential role of the [3 R] and [31 S] stereoisomers in the formation of the chlorosomal antennae, as tubular structures are not formed without this chirality. The 3D arrangement of the layers is revealed by intermolecular 13C−13C correlations obtained from CP3 CHHC experiments. With the tail truncated to methyl, a microcrystalline solid is formed with favorable interactions between the planar sheets in a head-to-tail orientation. The stearyl tails lead to a considerably disordered aggregate consisting of both syn and anti layers similar to the chlorosomes, as indicated by a doubling of the N−D signal. These results reveal a balance between relatively strong local interactions and contributions to the free energy of the system associated with a longer length scale. This leads to a robust chlorosome structure, stable against thermodynamic noise, and allows for fine-tuning of the structure.