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

Soichiro Ogi,Frank Würthner,Charlotte Grzeszkiewicz

doi:10.1039/c7sc03725b

Abstract

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.

Highlights

Despite the vast amount of research accomplished in the last few decades on self-assembly,[1] there is still an apparent gap between the mechanistic understanding of self-assembly processes of synthetic systems so far achieved[2] and those that occur in nature, e.g. the formation of tobacco mosaic virus,[3] amyloid bers[4] or biological bilayer membranes.[5]
A prime example where chemistry and biology meet is that of chlorosomes.[6]. These are light-harvesting antenna systems of green bacteria composed of self-assembled metallochlorin dyes, in particular bacteriochlorophylls (BChls) c, d, and e that possess a chlorophyll scaffold bearing a hydroxyl group at the 31-position and a metal ion at the center (Fig. 1a).6c,7 The hydroxyl group is responsible for the slipped p-stacking arrangement aUniversitat Wurzburg, Institut fur Organische Chemie, Am Hubland, 97074 Wurzburg, Germany
zinc chlorin (ZnChl) 1 was dissolved in methanol and deionized water was added to the monomer solution in methanol until the water content reached 50–80 vol% with a total concentration of 1 Â 10À5 M

Summary

Introduction

Despite the vast amount of research accomplished in the last few decades on self-assembly,[1] there is still an apparent gap between the mechanistic understanding of self-assembly processes of synthetic systems so far achieved[2] and those that occur in nature, e.g. the formation of tobacco mosaic virus,[3] amyloid bers[4] or biological bilayer membranes.[5]. Motivated by signi cant recent progress in the mechanistic understanding of aggregation processes,[2] we here elucidate the self-assembly mechanism of a semi-synthetic zinc chlorin model compound (ZnChl 1)11d (Fig. 1a) by kinetic and thermodynamic studies.

Results

Conclusion