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.

Department of Chemical Physics and Optics Faculty of Mathematics and Physics Charles University Prague Czech Republic

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Balaban, T. S., A. R. Holzwarth, K. Schaffner, G. J. Boender, and H. J. de Groot. 1995. CP-MAS PubMed

Blankenship, R. E., J. M. Olson, and M. Miller. 1995. Antenna complexes from green photosynthetic bacteria.

Borrego, C. M., P. G. Gerola, M. Miller, and R. P. Cox. 1999. Light intensity effects on pigment composition and organisation in the green sulfur bacterium

Brune, D. C., G. H. King, and R. E. Blankenship. 1988. Interactions between bacteriochlorophyll

Chiefari, J., K. Griebenow, F. Fages, N. Griebenow, T. S. Balaban, A. R. Holzwarth, and K. Schaffner. 1995. Models for the pigment organization in the chlorosomes of photosynthetic bacteria: Diastereoselective control of in vivo bacteriochlorophyll

Cohen-Bazire, G., N. Pfennig, and R. Kunisawa. 1964. The fine structure of green bacteria. J. Cell Biol. 22:207–225. PubMed PMC

Dubochet, J., M. Adrian, J. J. Chang, J. C. Homo, J. Lepault, A. W. McDowall, and P. Schultz. 1988. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21:129–228. PubMed

Frese, R., U. Oberheide, I. H. M. van Stokkum, R. van Grondelle, M. Foidl, J. Oelze, and H. van Amerongen. 1997. The organization of bacteriochlorophyll

Frigaard, N. U., A. G. M. Chew, H. Li, J. A. Maresca, and D. A. Bryant. 2003. PubMed

Gandini, S. C. M., E. L. Gelamo, R. Itri, and M. Tabak. 2003. Small angle x-ray scattering study of meso-tetrakis (4-Sulfonatophenyl) porphyrin in aqueous solution: a self-aggregation model. Biophys. J. 85:1259–1268. PubMed PMC

Gehrke, R. 1992. An ultrasmall angle scattering instrument for the doris-III bypass. Rev. Sci. Instrum. 63:455–458.

Gerola, P. D., and J. M. Olson. 1986. A new bacteriochlorophyll PubMed

Grigorieff, N. 1998. Three-dimensional structure of bovine NADH: Ubiquinone oxidoreductase (Complex I) at 22 angstrom in ice. J. Mol. Biol. 277:1033–1046. PubMed

Hildebrandt, P., K. Griebenow, A. R. Holzwarth, and K. Schaffner. 1991. Resonance Raman spectroscopic evidence for the identity of the bacteriochlorophyll

Holzwarth, A. R., and K. Schaffner. 1994. On the structure of bacteriochlorophyll molecular aggregates in the chlorosomes of green bacteria. A molecular modelling study. Photosynth. Res. 41:225–233. PubMed

Mizoguchi, T., K. Hara, H. Nagae, and Y. Koyama. 2000. Structural transformation among the aggregate forms of bacteriochlorophyll PubMed

Montano, G. A., B. P. Bowen, J. T. LaBelle, N. W. Woodbury, V. B. Pizziconi, and R. Blankenship. 2003. Characterization of PubMed PMC

Nozawa, T., K. Ohtomo, M. Suzuki, H. Nakagawa, Y. Shikama, H. Konami, and Z. Y. Wang. 1994. Structures of chlorosomes and aggregated BChl PubMed

Oelze, J., and J. R. Golecki. 1995. Membranes and chlorosomes of green bacteria: structure, composition, and development.

Overmann, J., H. Cypionka, and N. Pfennig. 1992. An extremely low-light-adapted phototrophic sulfur bacterium from the Black sea. Limnol. Oceanog. 37:150–155.

Prokhorenko, V. I., D. B. Steensgaard, and A. R. Holzwarth. 2000. Exciton dynamics in the chlorosomal antennae of the green bacteria PubMed PMC

Psencik, J., Y. Z. Ma, J. B. Arellano, J. Hala, and T. Gillbro. 2003. Excitation energy transfer dynamics and excited-state structure in chlorosomes of PubMed PMC

Smith, K. M., F. W. Bobe, D. A. Goff, and R. J. Abraham. 1986. NMR spectra of porphyrins. 28. Detailed solution structure of bacteriochlorophyllide

Staehelin, L. A., J. R. Golecki, R. C. Fuller, and G. Drews. 1978. Visualization of the supramolecular architecture of chlorosome (Chlorobium type vesicles) in freeze-fractured cells of

Staehelin, L. A., J. R. Golecki, and G. Drews. 1980. Supramolecular organization of chlorosome (Chlorobium vesicles) and of their membrane attachment site in PubMed

Umetsu, M., Z. Y. Wang, J. Zhang, T. Ishii, K. Uehara, Y. Inoko, M. Kobayashi, and T. Nozawa. 1999. How the formation process influences the structure of BChl c aggregates. Photosynth. Res. 60:229–239.

Umetsu, M., R. Seki, Z. Y. Wang, I. Kumagai, and T. Nozawa. 2002. Circular and magnetic circular dichroism studies of bacteriochlorophyll

van Rossum, B. J., D. B. Steensgaard, F. M. Mulder, G. J. Boender, K. Schaffner, A. R. Holzwarth, and H. M. de Groot. 2001. A refined model of the chlorosomal antennae of the green bacterium PubMed

Wahlund, T. M., C. R. Woese, R. W. Castenholz, and M. T. Madigan. 1991. A thermophilic green sulfur bacterium from new-zealand hot-springs, chlorobium-tepidum sp-nov. Arch. Microbiol. 156:81–90.

Wang, Z. Y., M. Umetsu, M. Kobayashi, and T. Nozawa. 1999a. Complete assignment of H

Wang, Z. Y., M. Umetsu, M. Kobayashi, and T. Nozawa. 1999b. C-13- and N-15-NMR studies on the intact bacteriochlorophyll

Wullink, W., and E. F. J. van Bruggen. 1988. Structural studies on chlorosomes from

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