Contrasting Modes of Self-Assembly and Hydrogen-Bonding Heterogeneity in Chlorosomes of Chlorobaculum tepidum

[Image: see text] Chlorosome antennae form an interesting class of materials for studying the role of structural motifs and dynamics in nonadiabatic energy transfer. They perform robust and highly quantum-efficient transfer of excitonic energy while allowing for compositional variation and completely lacking the usual regulatory proteins. Here, we first cast the geometrical analysis for ideal tubular scaffolding models into a formal framework, to relate effective helical properties of the assembly structures to established characterization data for various types of chlorosomes. This analysis shows that helicity is uniquely defined for chlorosomes composed of bacteriochlorophyll (BChl) d and that three chiral angles are consistent with the nuclear magnetic resonance (NMR) and electron microscope data for BChl c, including two novel ones that are at variance with current interpretations of optical data based on perfect cylindrical symmetry. We use this information as a starting point for investigating dynamic and static heterogeneity at the molecular level by unconstrained molecular dynamics. We first identify a rotational degree of freedom, along the Mg–OH coordination bond, that alternates along the syn–anti stacks and underlies the (flexible) curvature on a larger scale. Because rotation directly relates to the formation or breaking of interstack hydrogen bonds of the O–H···O=C structural motif along the syn–anti stacks, we analyzed the relative fractions of hydrogen-bonded and the nonbonded regions, forming stripe domains in otherwise spectroscopically homogeneous curved slabs. The ratios 7:3 for BChl c and 9:1 for BChl d for the two distinct structural components agree well with the signal intensities determined by NMR. In addition, rotation with curvature-independent formation of stripe domains offers a viable explanation for the localization and dispersion of exciton states over two fractions, as observed in single chlorosome fluorescence decay studies.