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

Zobrazit více v PubMed

Balaban, T. S., A. R. Holzwarth, K. Schaffner, G. J. Boender, and H. J. de Groot. 1995. CP-MAS 13C-NMR dipolar correlation spectroscopy of 13C-enriched chlorosomes and isolated bacteriochlorophyll c aggregates of Chlorobium tepidum: The self organization of pigments is the main structural feature of chlorosomes. Biochemistry. 34:15259–15266. PubMed

Blankenship, R. E., J. M. Olson, and M. Miller. 1995. Antenna complexes from green photosynthetic bacteria. In Anoxygenic Photosynthetic Bacteria. R. E. Blankenship, M. T. Madigan, and C. E. Bauer, editors. Kluwer Academic Publisher, Dordrecht, The Netherlands. 399–435.

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 Chlorobium tepidum. Photosynth. Res. 59:159–166.

Brune, D. C., G. H. King, and R. E. Blankenship. 1988. Interactions between bacteriochlorophyll c molecules in oligomers and in chlorosomes of green photosynthetic bacteria. In Photosynthetic Light-Harvesting Systems. H. Scheer,and S. Schneider, editors. Walter de Gruyter, Berlin. 141–151.

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 cs aggregation. J. Phys. Chem. 99:1357–1365.

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 c in chlorosomes from Chloroflexus aurantiacus and the structural role of carotenoids and protein—an absorption, linear dichroism, circular dichroism and Stark spectroscopy study. Photosynth. Res. 54:115–126.

Frigaard, N. U., A. G. M. Chew, H. Li, J. A. Maresca, and D. A. Bryant. 2003. Chlorobium tepidum: insights into the structure, physiology, and metabolism of a green sulfur bacterium derived from a complete genome sequence. Photosynth. Res. 78:93–117. 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 a-protein complex associated with the chlorosomes of green sulfur bacteria. Biochim. Biophys. Acta. 848:69–76. 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 c organisation in protein-free and protein-containing chlorosomes from Chloroflexus aurantiacus. Z. Naturforsch. 46c:228–232.

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 c as determined by electronic-absorption and NMR spectroscopies: Dependence on the stereoisomeric configuration and on the bulkiness of the 8-C side chain. Photochem. Photobiol. 71:596–609. PubMed

Montano, G. A., B. P. Bowen, J. T. LaBelle, N. W. Woodbury, V. B. Pizziconi, and R. Blankenship. 2003. Characterization of Chlorobium tepidum chloromes: A calculation of bacteriochlorophyll c per chlorosome and oligomer modeling. Biophys. J. 85:2560–2565. 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 c in Chlorobium tepidum from solid state high resolution CP/MAS 13C NMR. Photosynth. Res. 41:211–233. PubMed

Oelze, J., and J. R. Golecki. 1995. Membranes and chlorosomes of green bacteria: structure, composition, and development. In Anoxygenic Photosynthetic Bacteria. R. E. Blankenship, M. T. Madigan, and C. E. Bauer, editors. Kluwer Academic Publishers, Dordrecht, The Netherlands. 259–278.

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 Chloroflexus aurantiacus and Chlorobium tepidum. Biophys. J. 79:2105–2120. 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 Chlorobium phaeobacteroides. Biophys. J. 84:1161–1179. 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 d dimer. J. Am. Chem. Soc. 108:1111–1120.

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 Chloroflexus aurantiacus. Arch. Microbiol. 119:269–277.

Staehelin, L. A., J. R. Golecki, and G. Drews. 1980. Supramolecular organization of chlorosome (Chlorobium vesicles) and of their membrane attachment site in Chlorobium limicola. Biochim. Biophys. Acta. 589:30–45. 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 c aggregates: T-shaped and antiparallel dimers. J. Phys. Chem. B. 106:3987–3995.

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 Chlorobium tepidum from proton chemical shift constraints obtained with high-field 2-D and 3-D MAS NMR dipolar correlation spectroscopy. Biochemistry. 40:1587–1595. 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 H1 NMR spectra and structural analysis of intact bacteriochlorophyll c dimer in solution. J. Phys. Chem. B. 103:3742–3753.

Wang, Z. Y., M. Umetsu, M. Kobayashi, and T. Nozawa. 1999b. C-13- and N-15-NMR studies on the intact bacteriochlorophyll c dimers in solutions. J. Am. Chem. Soc. 121:9363–9369.

Wullink, W., and E. F. J. van Bruggen. 1988. Structural studies on chlorosomes from Prosthecochlorisaestuarii. In Green Photosynthetic Bacteria. J. M. Olson, J. G. Ormerod, J. Amesz, E. Stackebrandt, and H. G. Trüper, editors. Plenum Press, New York. 3–14.

Anoxygenic photosynthesis with emphasis on green sulfur bacteria and a perspective for hydrogen sulfide detoxification of anoxic environments

Photosynthetic Light-Harvesting (Antenna) Complexes-Structures and Functions

Superradiance of bacteriochlorophyll c aggregates in chlorosomes of green photosynthetic bacteria

In situ mapping of the energy flow through the entire photosynthetic apparatus

Structural and functional roles of carotenoids in chlorosomes

Self-assembly and energy transfer in artificial light-harvesting complexes of bacteriochlorophyll c with astaxanthin

The lamellar spacing in self-assembling bacteriochlorophyll aggregates is proportional to the length of the esterifying alcohol

Structure of chlorosomes from the green filamentous bacterium Chloroflexus aurantiacus

Effect of quinones on formation and properties of bacteriochlorophyll c aggregates

Internal structure of chlorosomes from brown-colored chlorobium species and the role of carotenoids in their assembly