A Refined Model of the Chlorosomal Antennae of the Green Bacterium Chlorobium tepidum from Proton Chemical Shift Constraints Obtained with High-Field 2-D and 3-D MAS NMR Dipolar Correlation Spectroscopy

Abstract

Heteronuclear 2-D and 3-D magic-angle spinning NMR dipolar correlation spectroscopy was applied to determine solid-state (1)H shifts for aggregated bacteriochlorophyll c (BChl c) in uniformly (13)C-enriched light harvesting chlorosomes of the green photosynthetic bacterium Chlorobium tepidum. A complete assignment of 29 different observable resonances of the 61 protons of the aggregated BChl c in the intact chlorosomes is obtained. Aggregation shifts relative to monomeric BChl c in solution are detected for protons attached to rings I, II, and III/V and to their side chains. The 2(1)-H(3), 3(2)-H(3), and 3(1)-H resonances are shifted upfield by -2.2, -1, and -3.3 ppm, respectively, relative to monomeric BChl c in solution. Although the resonances are inhomogeneously broadened and reveal considerable global structural heterogeneity, the 5-CH and the 7-Me responses are doubled, which provides evidence for the existence of at least two relatively well-defined structurally different arrangements. Ab initio quantum chemical modeling studies were performed to refine a model for the self-assembled BChl c with two different types of BChl stacks. The BChl in the stacks can adopt either anti- or syn-configuration of the coordinative bond, where anti and syn designate the relative orientation of the Mg-OH bond relative to the direction of the 17-17(1) bond. The analogy between aggregation shifts for BChl c in the chlorosome and for self-assembled chlorophyll a/H(2)O is explored, and a bilayer model for the tubular supra-structure of sheets of BChl c is proposed, from a homology modeling approach.

Zinc chlorins for artificial light-harvesting self-assemble into antiparallel stacks forming a microcrystalline solid-state material

“…2 A-D. A single set of peaks without significant broadening is detected for 1 and 2, which implies a local packing order with unique structural environments for every molecule. The 3 1 -OH and 3 1 -OCH 3 resonances for chlorins 1 and 2 respectively, were not observed even at lower contour levels, possibly because of some form of dynamics and inefficient cross-polarization (11,17). The solidstate proton shift values have been listed in Table 1 Table 1.…”

The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium

“…All Chlorobia possess unique light-harvesting antennae known as chlorosomes (26), which contain bacteriochlorophyll c (BChl c) aggregates (27,28) and are surrounded by a protein-stabilized, galactolipid monolayer. Genes had been identified for most of the 10 known chlorosome proteins (29) and for the BChl a binding protein FMO (CT1499), which likely attaches the chlorosome to the underlying RCs ( Fig.…”

Bacteriochlorophyllide c C-8 2 and C-12 1 Methyltransferases Are Essential for Adaptation to Low Light in Chlorobaculum tepidum

“…The larger aggregates could assemble a larger chlorosome containing a greater number of BChl c molecules, which would in turn allow an organism to increase its relative BChl c content. Another possibility is that these modifications of the BChl c molecule increase disorder in the BChl aggregates and allow a much higher packing density of BChl c in the chlorosomes without causing crystallization (33). While some evidence suggests that the absence of these physical interactions in the mutants would contribute to the reduced BChl c content in the cells, both cases would cause a dramatic change in the relative composition of the chlorosomes.…”

“…This methyl-carboxyl group would interfere with the hydrogenbonding network between the keto group of one molecule and the C-3 1 hydroxyl of a neighboring molecule in a BChl aggregate (19,33). These modifications contribute to the formation of the large aggregates that make up the core of the chlorosome (13).…”