Chlorosomes are large light-harvesting complexes found in three phyla of anoxygenic photosynthetic bacteria. Chlorosomes are primarily composed of self-assembling pigment aggregates. In addition to the main pigment, bacteriochlorophyll c, d, or e, chlorosomes also contain variable amounts of carotenoids. Here, we use X-ray scattering and electron cryomicroscopy, complemented with absorption spectroscopy and pigment analysis, to compare the morphologies, structures, and pigment compositions of chlorosomes from Chloroflexus aurantiacus grown under two different light conditions and Chlorobaculum tepidum. High-purity chlorosomes from C. aurantiacus contain about 20% more carotenoid per bacteriochlorophyll c molecule when grown under low light than when grown under high light. This accentuates the light-harvesting function of carotenoids, in addition to their photoprotective role. The low-light chlorosomes are thicker due to the overall greater content of pigments and contain domains of lamellar aggregates. Experiments where carotenoids were selectively extracted from intact chlorosomes using hexane proved that they are located in the interlamellar space, as observed previously for species belonging to the phylum Chlorobi. A fraction of the carotenoids are localized in the baseplate, where they are bound differently and cannot be removed by hexane. In C. tepidum, carotenoids cannot be extracted by hexane even from the chlorosome interior. The chemical structure of the pigments in C. tepidum may lead to π-π interactions between carotenoids and bacteriochlorophylls, preventing carotenoid extraction. The results provide information about the nature of interactions between bacteriochlorophylls and carotenoids in the protein-free environment of the chlorosome interior.

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

Zobrazit více v PubMed

Blankenship RE, Matsuura K. 2003. Antenna complexes from green photosynthetic bacteria, p 195–217 In Green BR, Parson WW. (ed), Light-harvesting antennas in photosynthesis. Kluwer Academic Publishers, Dordrecht, The Netherlands

Frigaard NU, Bryant DA. 2006. Chlorosomes: antenna organelles in photosynthetic green bacteria, p 79–114 In Shively JM. (ed), Complex intracellular structures in prokaryotes. Microbiology monographs, vol 2. Springer, Berlin, Germany

Oostergetel GT, van Amerongen H, Boekema EJ. 2010. The chlorosome: a prototype for efficient light harvesting in photosynthesis. Photosynth. Res. 104:245–255 PubMed PMC

Pedersen MO, Linnanto J, Frigaard NU, Nielsen NC, Miller M. 2010. A model of the protein-pigment baseplate complex in chlorosomes of photosynthetic green bacteria. Photosynth. Res. 104:233–243 PubMed

Montano GA, Bowen BP, LaBelle JT, Woodbury NW, Pizziconi VB, Blankenship RE. 2003. Characterization of Chlorobium tepidum chloromes: a calculation of bacteriochlorophyll c per chlorosome and oligomer modeling. Biophys. J. 85:2560–2565 PubMed PMC

Saga Y, Shibata Y, Ltoh S, Tamiaki H. 2007. Direct counting of submicrometer-sized photosynthetic apparatus dispersed in medium at cryogenic temperature by confocal laser fluorescence microscopy: estimation of the number of bacteriochlorophyll c in single light-harvesting antenna complexes chlorosomes of green photosynthetic bacteria. J. Phys. Chem. B 111:12605–12609 PubMed

Garcia Costas AM, Tsukatani Y, Romberger SP, Oostergetel GT, Boekema EJ, Golbeck JH, Bryant DA. 2011. Ultrastructural analysis and identification of envelope proteins of “Candidatus Chloracidobacterium thermophilum” chlorosomes. J. Bacteriol. 193:6701–6711 PubMed PMC

Psencik J, Ikonen TP, Laurinmäki P, Merckel MC, Butcher SJ, Serimaa RE, Tuma R. 2004. Lamellar organization of pigments in chlorosomes, the light harvesting complexes of green photosynthetic bacteria. Biophys. J. 87:1165–1172 PubMed PMC

Psencik J, Arellano JB, Ikonen TP, Borrego CM, Laurinmaki PA, Butcher SJ, Serimaa RE, Tuma R. 2006. Internal structure of chlorosomes from brown-colored Chlorobium species and the role of carotenoids in their assembly. Biophys. J. 91:1433–1440 PubMed PMC

Psencik J, Collins AM, Liljeroos L, Torkkeli M, Laurinmaki P, Ansink HM, Ikonen TP, Serimaa RE, Blankenship RE, Tuma R, Butcher SJ. 2009. Structure of chlorosomes from the green filamentous bacterium Chloroflexus aurantiacus. J. Bacteriol. 191:6701–6708 PubMed PMC

Psencik J, Torkkeli M, Zupcanova A, Vacha F, Serimaa RE, Tuma R. 2010. The lamellar spacing in self-assembling bacteriochlorophyll aggregates is proportional to the length of the esterifying alcohol. Photosynth. Res. 104:211–219 PubMed

Ganapathy S, Oostergetel GT, Wawrzyniak PK, Reus M, Chew AGM, Buda F, Boekema EJ, Bryant DA, Holzwarth AR, de Groot HJM. 2009. Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes. Proc. Natl. Acad. Sci. U. S. A. 106:8525–8530 PubMed PMC

Oostergetel GT, Reus M, Gomez Maqueo Chew A, Bryant DA, Boekema EJ, Holzwarth AR. 2007. Long-range organization of bacteriochlorophyll in chlorosomes of Chlorobium tepidum investigated by cryo-electron microscopy. FEBS Lett. 581:5435–5439 PubMed

Kim H, Li H, Maresca JA, Bryant DA, Savikhin S. 2007. Triplet exciton formation as a novel photoprotection mechanism in chlorosomes of Chlorobium tepidum. Biophys. J. 93:192–201 PubMed PMC

van Dorssen RJ, Vasmel H, Amesz J. 1986. Pigment organization and energy transfer in the green photosynthetic bacterium Chloroflexus aurantiacus. II. The chlorosome. Photosynth. Res. 9:33–45 PubMed

Melo TB, Frigaard NU, Matsuura K, Naqvi KR. 2000. Electronic energy transfer involving carotenoid pigments in chlorosomes of two green bacteria: Chlorobium tepidum and Chloroflexus aurantiacus. Spectrochim. Acta A Mol. Biol. Spectrosc. 56:2001–2010 PubMed

Psencik J, Ma YZ, Arellano JB, Garcia-Gil J, Holzwarth AR, Gillbro T. 2002. Excitation energy transfer in chlorosomes of Chlorobium phaeobacteroides strain CL1401: the role of carotenoids. Photosynth. Res. 71:5–18 PubMed

Alster J, Polivka T, Arellano JB, Chabera P, Vacha F, Psencik J. 2010. β-Carotene to bacteriochlorophyll c energy transfer in self-assembled aggregates mimicking chlorosomes. Chem. Phys. 373:90–97

Klinger P, Arellano JB, Vacha FE, Hala J, Psencik J. 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

Brune DC, Nozawa T, Blankenship RE. 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

Borrego CM, Garcia-Gil LJ. 1995. Rearangement of light harvesting bacteriochlorophyll homologues as a response of green sulfur bacteria to low light intensities. Photosynth. Res. 45:21–30 PubMed

Schmidt K, Maarzahl M, Mayer F. 1980. Development and pigmentation of chlorosomes in Chloroflexus aurantiacus strain Ok-70-fl. Arch. Microbiol. 127:87–97

Borrego CM, Gerola PD, Miller M, Cox RP. 1999. Light intensity effects on pigment composition and organisation in the green sulfur bacterium Chlorobium tepidum. Photosynth. Res. 59:159–166

Hanada S, Pierson B. 2006. The family Chloroflexaceae, p 815–842 In Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E. (ed), The prokaryotes. Springer, Berlin, Germany

Feick RG, Fuller RC. 1984. Topography of the photosynthetic apparatus of Chloroflexus aurantiacus. Biochemistry 23:3693–3700

Ikonen TP, Li H, Psencik J, Laurinmaki PA, Butcher SJ, Frigaard NU, Serimaa RE, Bryant DA, Tuma R. 2007. X-ray scattering and electron cryomicroscopy study on the effect of carotenoid biosynthesis to the structure of Chlorobium tepidum chlorosomes. Biophys. J. 93:620–628 PubMed PMC

Larsen KL, Cox RP, Miller M. 1994. Effects of illumination intensity on bacteriochlorophyll c homolog distribution in Chloroflexus aurantiacus grown under controlled conditions. Photosynth. Res. 41:151–156 PubMed

Blankenship RE, Olson JM, Miller M. 1995. Antenna complexes from green photosynthetic bacteria, p 399–435 In Blankenship RE, Madigan MT, Bauer CE. (ed), Anoxygenic photosynthetic bacteria. Kluwer Academic Publisher, Dordrecht, The Netherlands

Sprague SG, Staehelin LA, Dibartolomeis MJ, Fuller RC. 1981. Isolation and development of chlorosomes in the green bacterium Chloroflexus aurantiacus. J. Bacteriol. 147:1021–1031 PubMed PMC

Guyoneaud R, Borrego CM, Martinez-Planells A, Buitenhuis ET, Garcia-Gil LJ. 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

Mallorqui-Fernandez N. 2003. Estudi dels carotenoides en especies marrons de bacteris verds del sofre: diversitat, eco-fisiologia i regulacio. Ph.D. thesis University of Girona, Girona, Spain

Frigaard NU, Matsuura K, Hirota M, Miller M, Cox RP. 1998. Studies of the location and function of isoprenoid quinones in chlorosomes from green sulfur bacteria. Photosynth. Res. 58:81–90

Montano GA, Wu HM, Lin S, Brune DC, Blankenship RE. 2003. Isolation and characterization of the B798 light-harvesting baseplate from the chlorosomes of Chloroflexus aurantiacus. Biochemistry 42:10246–10251 PubMed

Fuciman M, Chabera P, Zupcanova A, Hribek P, Arellano JB, Vacha F, Psencik J, Polivka T. 2010. Excited state properties of aryl carotenoids. Phys. Chem. Chem. Phys. 12:3112–3120 PubMed

Alster J, Kabelac M, Tuma R, Psencik J, Burda JV. 2012. Computational study of short-range interactions in bacteriochlorophyll aggregates. Comput. Theor. Chem. 998:87–97

Wang YL, Mao LS, Hu XC. 2004. Insight into the structural role of carotenoids in the Photosystem I: a quantum chemical analysis. Biophys. J. 86:3097–3111 PubMed PMC

Low-temperature spectroscopy of bacteriochlorophyll c aggregates