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

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.