Internal structure of chlorosomes from brown-colored chlorobium species and the role of carotenoids in their assembly
Language English Country United States Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
16731553
PubMed Central
PMC1518626
DOI
10.1529/biophysj.106.084228
PII: S0006-3495(06)71854-9
Knihovny.cz E-resources
- MeSH
- Bacteriochlorophylls chemistry metabolism MeSH
- Models, Biological MeSH
- Models, Chemical * MeSH
- Chlorobium chemistry metabolism ultrastructure MeSH
- Carotenoids chemistry metabolism MeSH
- Organelles chemistry ultrastructure MeSH
- Computer Simulation MeSH
- Light-Harvesting Protein Complexes chemistry metabolism ultrastructure MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Bacteriochlorophylls MeSH
- Carotenoids MeSH
- Light-Harvesting Protein Complexes MeSH
Chlorosomes are the main light harvesting complexes of green photosynthetic bacteria. Recently, a lamellar model was proposed for the arrangement of pigment aggregates in Chlorobium tepidum chlorosomes, which contain bacteriochlorophyll (BChl) c as the main pigment. Here we demonstrate that the lamellar organization is also found in chlorosomes from two brown-colored species (Chl. phaeovibrioides and Chl. phaeobacteroides) containing BChl e as the main pigment. This suggests that the lamellar model is universal among green sulfur bacteria. In contrast to green-colored Chl. tepidum, chlorosomes from the brown-colored species often contain domains of lamellar aggregates that may help them to survive in extremely low light conditions. We suggest that carotenoids are localized between the lamellar planes and drive lamellar assembly by augmenting hydrophobic interactions. A model for chlorosome assembly, which accounts for the role of carotenoids and secondary BChl homologs, is presented.
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Blankenship, R. E., and K. Matsuura. 2003. Antenna complexes from green photosynthetic bacteria. In Light Harvesting Antennas in Photosynthesis. B. R. Green, and W. W. Parson, editors. Kluwer Academic Publisher, Dordrecht. 195–217.
Frigaard, N. U., and D. A. Bryant. 2004. Seeing green bacteria in a new light: genomics-enabled studies of the photosynthetic apparatus in green sulfur bacteria and filamentous anoxygenic phototrophic bacteria. Arch. Microbiol. 182:265–276. PubMed
Staehelin, L. A., J. R. Golecki, R. C. Fuller, and G. Drews. 1978. Visualization of the supramolecular architecture of chlorosomes (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 chlorosomes (chlorobium vesicles) and of their membrane attachment sites in Chlorobium limicola. Biochim. Biophys. Acta. 589:30–45. PubMed
Psencik, J., T. P. Ikonen, P. Laurinmäki, M. C. Merckel, S. J. Butcher, R. E. Serimaa, and R. Tuma. 2004. Lamellar organization of pigments in chlorosomes, the light harvesting complexes of green photosynthetic bacteria. Biophys. J. 87:1165–1172. PubMed PMC
Hohmann-Marriott, M. F., R. E. Blankenship, and R. W. Roberson. 2005. The ultrastructure of Chlorobium tepidum chlorosomes revealed by electron microscopy. Photosynth. Res. 86:145–154. PubMed
Liaaen-Jensen, S. 1965. Bacterial carotenoids. XVIII. Aryl-carotenes from Phaeobium. Acta Chem. Scand. 19:1025–1030. PubMed
Francke, C., and J. Amesz. 1997. Isolation and pigment composition of the antenna system of four species of green sulfur bacteria. Photosynth. Res. 52:137–146.
Glaeser, J., L. Bañera, H. Rutters, and J. Overmann. 2002. Novel bacteriochlorophyll e structures and species-specific variability of pigment composition in green sulfur bacteria. Arch. Microbiol. 177:475–485. PubMed
Klinger, P., J. B. Arellano, F. E. Vacha, J. Hala, and J. Psencik. 2004. Effect of carotenoids and monogalactosyl diglyceride on bacteriochlorophyll c aggregates in aqueous buffer: implications for the self-assembly of chlorosomes. Photochem. Photobiol. 80:572–578. PubMed
Arellano, J. B., J. Psencik, C. M. Borrego, Y. Z. Ma, R. Guyoneaud, J. Garcia-Gil, and T. Gillbro. 2000. The effect of carotenoid biosynthesis inhibition on the organisation and function of chlorosomes from Chlorobium phaeobacteroides CL1401. Photochem. Photobiol. 71:715–723. PubMed
Arellano, J. B., C. M. Borrego, A. Martinez-Planells, and L. J. Garcia-Gil. 2001. Effect of carotenoid deficiency on cells and chlorosomes of Chlorobium phaeobacteroides. Arch. Microbiol. 175:226–233. PubMed
Brune, D. C., T. Nozawa, and R. E. Blankenship. 1987. Antenna organization in green photosynthetic bacteria. 1. Oligomeric bacteriochlorophyll c as a model for the 740 nm absorbing bacteriochlorophyll c in Chloroflexus aurantiacus chlorosomes. Biochemistry. 26:8644–8652. PubMed
Trüper, H. G., and N. Pfennig. 1992. The family Chlorobiaceae. In The Prokaryotes. A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications. A. Balows, H. G. Trüper, M. Dworkin, W. Harder, and K. H. Schleifer, editors. Springer-Verlag, Berlin. 3583–3592.
Frigaard, N. U., K. Matsuura, M. Hirota, M. Miller, and R. P. Cox. 1998. Studies of the location and function of isoprenoid quinones in chlorosomes from green sulfur bacteria. Photosynth. Res. 58:81–90.
Borrego, C. M., and L. J. Garcia-Gil. 1994. Separation of bacteriochlorophyll homologues from green photosynthetic sulfur bacteria by reversed-phase HPLC. Photosynth. Res. 41:157–163. PubMed
Oelze, J. 1985. Analysis of bacteriochlorophylls. Methods Microbiol. 18:257–284.
Sauer, K., J. R. Lindsay-Smith, and A. J. Schultz. 1986. The dimerization of chlorophyll a, chlorophyll b, and bacteriochlorophyll in solution. J. Am. Chem. Soc. 88:2681–2688.
Borrego, C. M., J. B. Arellano, C. A. Abellà, T. Gillbro, and L. J. Garcia-Gil. 1999. The molar extinction coefficient of bacteriochlorophyll e and the pigment stoichiometry in Chlorobium phaeobacteroides. Photosynth. Res. 60:257–264.
Britton, G. 1995. UV/visible spectroscopy. In Carotenoids, Vol. 1B: Spectroscopy. G. Britton, S. Liaaen-Jensen, and H. Pfander, editors. Birkhäuser, Basel. 13–62.
Martinez-Planells, A., J. B. Arellano, C. M. Borrego, C. Lopez-Iglesias, F. Gich, and J. Garcia-Gil. 2002. Determination of the topography and biometry of chlorosomes by atomic force microscopy. Photosynth. Res. 71:83–90. PubMed
Repeta, D. J., D. J. Simpson, B. B. Jørgensen, and H. W. Jannasch. 1989. Evidence for anoxygenic photosynthesis from the distribution of bacteriochlorophylls in the black-sea. Nature. 342:69–72. PubMed
Overmann, J., H. Cypionka, and N. Pfennig. 1992. An extremely low-light-adapted phototrophic sulfur bacterium from the Black Sea. Limnol. Oceanogr. 37:150–155.
Airs, R. L., C. M. Borrego, L. J. Garcia-Gil, and B. J. Keely. 2001. Identification of the bacteriochlorophyll homologues of Chlorobium phaeobacteroides strain UdG6053 grown at low light intensity. Photosynth. Res. 70:221–230. PubMed
Guyoneaud, R., C. M. Borrego, A. Martinez-Planells, E. T. Buitenhuis, and L. J. Garcia-Gil. 2001. Light responses in the green sulfur bacterium Prosthecochloris aestuarii: Changes in prosthecae length, ultrastructure, and antenna pigment composition. Arch. Microbiol. 176:278–284. PubMed
Structural and functional roles of carotenoids in chlorosomes
Structure of chlorosomes from the green filamentous bacterium Chloroflexus aurantiacus
Effect of quinones on formation and properties of bacteriochlorophyll c aggregates