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 C-13 and N-15 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 Cd-113 MAS NMR signals indicate a five-coordination of the Cd metal. In particular, the combined NMR data show a (HOCd)-Cd-... coordination, very similar to the (HOMg)-Mg-... coordination in the natural system. Anomalously large H-1 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 A was defined from long-range ring-current shift calculations. In addition, our model structures confirm and validate the essential role of the [3(1)R] and [3(1)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 C-13-C-13 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