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, 87 (2), 1165-72

Lamellar Organization of Pigments in Chlorosomes, the Light Harvesting Complexes of Green Photosynthetic Bacteria

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Lamellar Organization of Pigments in Chlorosomes, the Light Harvesting Complexes of Green Photosynthetic Bacteria

J Psencík et al. Biophys J.

Abstract

Chlorosomes of green photosynthetic bacteria constitute the most efficient light harvesting complexes found in nature. In addition, the chlorosome is the only known photosynthetic system where the majority of pigments (BChl) is not organized in pigment-protein complexes but instead is assembled into aggregates. Because of the unusual organization, the chlorosome structure has not been resolved and only models, in which BChl pigments were organized into large rods, were proposed on the basis of freeze-fracture electron microscopy and spectroscopic constraints. We have obtained the first high-resolution images of chlorosomes from the green sulfur bacterium Chlorobium tepidum by cryoelectron microscopy. Cryoelectron microscopy images revealed dense striations approximately 20 A apart. X-ray scattering from chlorosomes exhibited a feature with the same approximately 20 A spacing. No evidence for the rod models was obtained. The observed spacing and tilt-series cryoelectron microscopy projections are compatible with a lamellar model, in which BChl molecules aggregate into semicrystalline lateral arrays. The diffraction data further indicate that arrays are built from BChl dimers. The arrays form undulating lamellae, which, in turn, are held together by interdigitated esterifying alcohol tails, carotenoids, and lipids. The lamellar model is consistent with earlier spectroscopic data and provides insight into chlorosome self-assembly.

Figures

FIGURE 1
FIGURE 1
EM analysis of chlorosomes. Image of four representative chlorosomes embedded in vitreous ice. The bottom panels show power spectra of the boxed areas and the corresponding striation spacings. Bar, 500 Å. The defocus value for panels a, b, and d was 2.5 μm and 2.55 μm for panel c.
FIGURE 2
FIGURE 2
(Upper panels) Tilted series images (−15, 0, and 30°) of a representative chlorosome. Bar, 500 Å. The defocus value was 1.6 μm. The tilt axis is oriented almost parallel to the striae and intersects through the middle of the chlorosome. Lower panels show the power spectra computed from the boxed regions (shown as a square in each upper panel), which were selected to correspond to the same volume of the chlorosome throughout the tilt.
FIGURE 3
FIGURE 3
X-ray scattering curves measured from a concentrated chlorosome solution combined from four individual measurements. The dashed curve shows scattering calculated from an analytical model containing 1000 Å long hollow cylinders of inner radius of 40 Å and outer radius of 50 Å in a 5 × 2 hexagonal lattice with a lattice constant of 100 Å (Prokhorenko et al., 2000), plus an exponentially decaying background. (Inset) X-ray scattering from a dry chlorosome sample. The positions of the diffraction maxima and corresponding monoclinic lattice indices are indicated by arrows.
FIGURE 4
FIGURE 4
Schematic model of the BChl aggregates in the chlorosome. (A) Arrangement of lamellae inside the chlorosome. Each undulated plane (thick green line) extends in the long axis of the chlorosome (z), and through the height of the chlorosome (y). Planes are arranged into lamellae throughout the chlorosome (x). Only a few lamellae are depicted for clarity. Model of one plane of BChl aggregate with parallel (B) or antiparallel (C) pigment configuration. Coordinate system as in panel A. The monoclinic unit cell projection and lattice constants are shown in red. (D) Top view of chlorin (green) planes (antiparallel configuration) associated via interdigitated esterifying alcohol tails (black). An underlying layer of BChl molecules is shown dotted whereas carotenoids (orange) are interspersed between the alcohol tails.

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