Pathway complexity in the self-assembly of a zinc chlorin model system of natural bacteriochlorophyll J-aggregates

Whilst bacteriochlorophyll c, d, and e dyes self-assemble into the most efficient light harvesting J-aggregate systems found in nature, their supramolecular packing arrangements are still a matter of debate and a significant number of models have been suggested for their local and long-range ordering. Here we reveal for a synthetic model system based on a zinc chlorin (ZnChl) dye an intriguing interplay of two competing aggregation pathways by kinetic and thermodynamic studies in MeOH/water solvent mixtures: the formation of kinetically controlled off-pathway nanoparticles consisting of excitonically coupled J-dimers versus the formation of thermodynamically more stable one-dimensional helical fibers consisting of J-coupled extended aggregates. The higher order of the latter is evidenced by atomic force microscopy and a more narrow absorption spectrum of the J-aggregates. Based on a recently developed thermodynamic model that combines the cooperative K₂-K growth model with a competing dimerization model, an energy landscape could be derived that describes the pathway complexity of this biomimetic system. Our studies reveal that the kinetic stability of the off-pathway nanoparticles increases with increasing concentration of ZnChl or water content in a MeOH/water solvent mixture. For a water content >90% deeply trapped off-pathway nanoparticle products are formed that do not transform anymore to the more ordered thermodynamic product within reasonable time scales. Based on these observations, we hypothesize that out-of-equilibrium aggregate structures of natural BChl dyes may also exist in the natural chlorosomes of green bacteria.