Assembly of a Mixture of Isomeric BChl c from Chlorobium limicola As Determined by Intermolecular ¹³C−¹³C Dipolar Correlations:  Coexistence of Dimer-Based and Pseudo-Monomer-Based Stackings

Abstract

A mixture of bacteriochlorophyll (BChl) c isomers was extracted from the cells of Chlorobium limicola that were grown in the media of 13C-enriched and natural-abundance isotopic compositions. The magic-angle spinning 13C NMR proton-driven spin-diffusion spectra were recorded with mixing times of 50, 100, and 250 ms for two different kinds of in vitro aggregates, one consisting of pure [13C]BChl c and the other consisting of a 1:1 mixture of [13C]BChl c and [12C]BChl c; those peaks whose intensities were reduced to approximately 1/4 by this dilution were assigned to intermolecular 13C-13C dipolar correlation peaks. On the other hand, the nearest-neighbor intermolecular carbon-carbon close contacts with distances of 4-6 A were simulated, to predict observed correlation peaks, for six different models of BChl c assembly. They include weakly overlapped monomers forming structure 1 and structure 2, strongly overlapped dimers forming straight and inclined columns, and weakly overlapped dimers forming aligned and displaced layers. Comparison between the observed correlation peaks and the predicted carbon-carbon close contacts, for both the macrocycles and the side chains, led us to a conclusion that the weakly overlapped dimers forming displaced layers are most likely the assembly of the BChl c molecules in the aggregate.

The supramolecular organization of self-assembling chlorosomal bacteriochlorophyll c , d , or e mimics

“…However, in these more recent models hydrogen bonding was still assumed to occur between dimers (7,12). Another very recent study by solid-state NMR on 13 C-labeled chlorosomes has discussed all previous models and favors a parallel hydrogenbonded dimer model as the most probable one (15,16). Molecular mechanics calculations and exciton theory have been applied in a very thorough theoretical investigation on the different possible geometries such as tube, lamella, or spiral-type for the chlorosomal aggregates (17).…”

Stacking of Bacteriochlorophyll c Macrocycles in Chlorosome from Chlorobium limicola As Revealed by Intermolecular 13C Magnetic-Dipole Correlation, X-Ray Diffraction, and Quadrupole Coupling in 25Mg NMR

“…In a previous investigation, we have actually determined, by the use of this method, the assembly of BChl c in the in Vitro solid aggregate of an isomeric mixture extracted from Chl. limicola (hereafter, we will call this sample simply "solid aggregate") (19). We found a unique stacking of macrocycles, as shown in Figure 1f, which we call "weakly overlapped dimers forming displaced layers".…”

“…We found a unique stacking of macrocycles, as shown in Figure 1f, which we call "weakly overlapped dimers forming displaced layers". It consisted of (i) the dimer-based stacking, (ii) the pseudo-monomerbased stacking of structure 1 type, and (iii) the pseudomonomer-based stacking of structure 2 type (see Figure 7 of ref 19).…”

On the way to biomimetic dye aggregate solar cells

“…56,57,58 A similar hydrogen-bonded dimer based model but with cylindrical geometry has been recently proposed based on solid state 13 C-NMR studies. 59,60 We favour an undulated, tubular architecture with frequent defects where the stacks are held together by hydrophobic and dispersive forces alone 33 as none of our BChl mimics, in spite of having hydroxy and carbonyl groups, show hydrogen bonds in the crystal. Recently, Linnanto and Korppi-Tommola have investigated theoretically by molecular mechanics and exciton theory various chlorosomal architectures, including tubes, lamellas and spiral-type aggregates.…”