Atomic structure of the bacteriochlorophyll c assembly in intact chlorosomes from Chlorobium limicola determined by solid-state NMR

Abstract

Green sulfur photosynthetic bacteria optimize their antennas, chlorosomes, especially for harvesting weak light by organizing bacteriochlorophyll (BChl) assembly without any support of proteins. As it is difficult to crystallize the organelles, a high-resolution structure of the light-harvesting devices in the chlorosomes has not been clarified. We have determined the structure of BChl c assembly in the intact chlorosomes from Chlorobium limicola on the basis of (13)C dipolar spin-diffusion solid-state NMR analysis of uniformly (13)C-labeled chlorosomes. About 90 intermolecular C-C distances were obtained by the simultaneous assignment of distance correlations and the structure optimization preceded by the polarization-transfer matrix analysis. An atomic structure was obtained, using these distance constraints. The determined structure of the chlorosomal BChl c assembly is built with the parallel layers of piggyback-dimers. This supramolecular structure would provide insights into the mechanism of weak-light capturing.

Self‐Assemblies of Zinc Bacteriochlorophyll‐d Analogues Having Amide, Ester, and Urea Groups as Substituents at 17‐Position and Observation of Lamellar Supramolecular Nanostructures

“…tepidum lacking methyl transferases BchQ/R [60] and BchQ/R/U, [61] the major pigments of which are farnesyl 8-ethyl-12-methyl-BChl-c and -d,r espectively. Supramolecular structures of BChl-c and -d self-assemblies in natural and modified chlorosomes have also been investigated by NMR spectroscopy, [18,51,[60][61][62][63][64][65][66][67][68][69][70][71] and 5a nd 10 nm tube-shaped and lamellar supramolecular nanostructures werem odeled by computational studies. [72][73][74][75][76] ChlorosomalB Chl-c,-d,-e,a nd -f molecules are magnesium complexes of 3 1 -hydroxy-13 1 -oxo-chlorins, the C13 2 atom of which lacks the methoxycarbonyl group found in the other natural Chls and BChls (Figure 1, left).…”

“…tepidum lacking methyl transferases BchQ/R and BchQ/R/U, the major pigments of which are farnesyl 8‐ethyl‐12‐methyl‐BChl‐ c and ‐ d , respectively. Supramolecular structures of BChl‐ c and ‐ d self‐assemblies in natural and modified chlorosomes have also been investigated by NMR spectroscopy, and 5 and 10 nm tube‐shaped and lamellar supramolecular nanostructures were modeled by computational studies …”

Solid-State NMR Study of the Charge-Transfer Complex between Ubiquinone-8 and Disulfide Bond Generating Membrane Protein DsbB

“…Solid-state NMR (SSNMR) has been shown to be an effective and versatile tool for studying function-related cofactors in large protein systems, such as UQ-10, 4,5 chlorophyll, 6 bacteriochlorophyll, 7,8 and retinal. 9-14 Resonance assignments of isotopically labeled cofactors are often facilitated by cofactor reincorporation into the binding sites of proteins.…”

De novo synthesis and properties of analogues of the self-assembling chlorosomal bacteriochlorophylls

“…The chlorosomal bacteriochlorophylls (bacteriochlorophylls c, d, and e) are structurally heterogeneous (i.e., not pure compounds) yet differ only slightly from the plant photosynthetic pigments chlorophylls a and b (Chart 1). Key structural differences include the presence of a mixture of stereoisomeric 3-(1-hydroxyethyl) groups rather than the 3-vinyl unit; the absence of the 13 2 -methoxycarbonyl substituent in the isocyclic ring; diverse substituents at the R 8 , R 12 , and propionate ester positions; and the presence of a methyl group at position 20 (bacteriochlorophyll c and e). 4 The structure of chlorosomes has been investigated by diverse methods including cryoelectron microscopy, [5][6][7] X-ray scattering, 5,7,8 absorption linear dichroism spectroscopy, 9 resonance Raman spectroscopy, 10 and solid-state NMR spectroscopy.…”

“…4 The structure of chlorosomes has been investigated by diverse methods including cryoelectron microscopy, [5][6][7] X-ray scattering, 5,7,8 absorption linear dichroism spectroscopy, 9 resonance Raman spectroscopy, 10 and solid-state NMR spectroscopy. 8,11,12 The pattern of self-assembly of chlorosomal bacteriochlorophyll molecules-which may differ across diverse organisms-remains a subject of intense debate. One of the longstanding models proposed for the self-assembled architecture is illustrated in Fig.…”