Abstract
The organization of bacteriochlorophyll c (BChl c) molecules was studied in normal and carotenoid-deficient chlorosomes isolated from the green phototrophic bacterium Chloroflexus aurantiacus. Carotenoid-deficient chlorosomes were obtained from cells grown in the presence of 60 µg of 2-hydroxybiphenyl per ml. At this concentration, BChl c synthesis was not affected while the formation of the 5.7 kDa chlorosome polypeptide was inhibited by about 50% (M. Foidl et al., submitted). Absorption, linear dichroism and circular dichroism spectroscopy showed that the organization of BChl c molecules with respect to each other as well as to the long axis of the chlorosomes was similar for both types of chlorosomes. Therefore, it is concluded that the organization of BChl c molecules is largely independent on the presence of the bulk of carotenoids as well as of at least half of the normal amount of the 5.7 kDa polypeptide. The Stark spectra of the chlorosomes, as characterized by a large difference polarizability for the ground- and excited states of the interacting BChl c molecules, were much more intense than those of individual pigments. It is proposed that this is caused by the strong overlap of BChl c molecules in the chlorosomes. In contrast to individual chlorophylls, BChl c in chlorosomes did not give rise to a significant difference permanent dipole moment for the ground- and excited states. This observation favors models for the BChl c organization which invoke the anti-parallel stacking of linear BChl c aggregates above those models in which linear BChl c aggregates are stacked in a parallel fashion. The difference between the Stark spectrum of carotenoid-deficient and WT chlorosomes indicates that the carotenoids are in the vicinity of the BChls.
Similar content being viewed by others
References
Blankenship RE, Olson JM and Miller M (1995) Antenna complexes from green photosynthetic bacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 399-435. Kluwer Academic Publishers, Dordrecht, the Netherlands
Beekman LMP, Steffen M, Van Stokkum IHM, Olsen JD, Hunter CN, Boxer SG and Van Grondelle R (1997a) Characterisation of the light harvesting antennas of photosynthetic purple bacteria by Stark spectroscopy: 1. LH1 antenna complex and the B820 sub-unit from Rhodospirillum rubrum. J Phys Chem B 101: 7284-7292
Beekman LMP, Frese RN, Fowler GJS, Cogdell RJ, Van Stokkum IHM, Hunter CN and Van Grondelle R (1997b) Characterisation of the light harvesting antennas of photosynthetic purple bacteria by Stark spectroscopy 2: LH2 complexes: Influence of the protein environment. J Phys Chem B 101: 7293-7301
Boxer SG (1996) Stark spectroscopy of photosynthetic systems. In: Amesz J and Hoff AJ (eds) Biophysical Techniques, pp 177-189. Kluwer Academic Publishers, Dordrecht, the Netherlands
Foidl M, Golecki JR and Oelze J (1994) Bacteriochlorophyll cformation and chlorosome development in Chloroflexus aurantiacus. Photosynth Res 41: 145-150
Ganago AO, Fok MV, Abdourakhmanov IA, Solov'ev AA and Erokhin YuE (1980) Analysis of the linear dichroism of reaction centers oriented in polyacrylamide gels. Mol Biol (Mosc) 14: 381-389
Gottfried DS, Stocker JW and Boxer SG (1991a) Stark effect spectroscopy of bacteriochlorophyll in light-harvesting complexes from photosynthetic bacteria. Biochim Biophys Acta 1059: 63-75
Gottfried DS, Steffen MA and Boxer SG (1991b) Stark effect spectroscopy of carotenoids in photosynthetic antenna and reaction center complexes. Biochim Biophys Acta 1059: 76-90
Griebenow K, Holzwarth AR, Van Mourik F and Van Grondelle R (1991) Pigment organization and energy transfer in green bacteria. 2. Circular and linear dichroism spectrum of protein-containing and protein-free chlorosomes isolated from Chloroflexus aurantiacusstrain Ok-70-fl. Biochim Biophys Acta 1058: 194-202
Holzwarth AR and Schaffner K (1994) On the structure of bacteriochlorophyll molecular aggregates in the chlorosomes of green bacterium Chloroflexus aurantiacus. Photosynth Res 41: 225-233
Hush NS and Reiners JR (1995) Vibrational Stark spectroscopy. 1. Basic Theory and Application to the CO Stretch. J Phys Chem 99: 15798-15805
Krawczyk S (1991) Electrochromism of chlorophyll amonomer and special pair dimer. Biochim Biophys Acta 1056: 64-70
Krawczyk S and Daniluk (1995) Solvent effects and vibrational dependence in electrochromic spectra of carotenoids. Chem Phys Lett 236: 431-437
Lehman RP, Brunisholz RA and Zuber H (1994) Giant circular dichroism of chlorosomes from Chloroflexus aurantiacustreated with 1-hexanol and proteolytic enzymes. Photosynth Res 41: 165-173
Liptay W (1974) Dipole moments and polarizabilities of molecules in excited electronic states. In: Lim CE (ed) Excited States, Vol 1, pp 129-229. Academic Press, New York
Lockhart DJ and Boxer SG (1987) Magnitude and direction of the change in dipole moment associated with excitation of the primary electron donor in Rhodopseudomonas spaeroidesreaction centers. Biochemistry 26: 664-668
Nozawa T, Ohtomo K, Suzuki M, Morishita Y and Madigan MT (1993) Structures and organization of bacteriochlorophyll c's in chlorosomes from a new thermophilic bacterium Chlorobium tepidum. Bull Chem Soc Jpn 66: 231-237
Mathies R and Stryer L (1976) Retinal has a highly dipolar vertically excited singlet state: Implications for vision. Proc Natl Acad Sci USA 73: 2169-2173
Matsuura K, Hirota M, Shimada K and Mimuro M (1993) Spectral forms and orientation of bacteriochlrophyll cand ain of chlorosomes of the green photosynthetic bacterium Chloroflexus aurantiacus. Photochem Photobiol 57: 92-97
Middendorf TR, Mazzola LT, Lao K, Steffen MA and Boxer SG (1993) Stark effect (electroabsorption) spectroscopy of photosynthetic reaction centers at 1.5 K: Evidence that the special pair has a large excited-state polarizability. Biochim Biophys Acta 1143: 223-234
Mimuro M, Matsuura K, Shimada K, Nishimura Y, Yamazaki I, Kobayashi M, Wang ZY and Nozawa T (1995) Molecular networks and funneling process of energy transfer in green photosynthetic bacteria. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, Vol 1, pp 41-52. Kluwer Academic Publishers, Dordrecht, the Netherlands
Oelze J and Golecki JR (1995) Membranes and chlorosomes of green bacteria: structure, composition and development. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 259-278. Kluwer Academic Publishers, Dordrecht, the Netherlands
Wu H-M, Reddy RS, and Small GJ (1997) Direct observation and hole burning of the lowest exciton level (B870) of the LH2 antenna complex of rhodopseudomonas acidophila(Strain 10050). J Phys Chem B 101: 651-656.
Somsen OJG, Van Grondelle R and Van Amerongen H (1996) Spectral broadening of interacting pigments: Polarized absorption by photosynthetic proteins. Biophys J 71: 1934-1951
Van Amerongen H, Vasmel H and Van Grondelle R (1988) Linear dichroism of chlorosomes from Chloroflexus aurantiacusin compressed gels and electric fields. Biophys J 54: 65-76
Van Amerongen H, Van Haeringen B, Van Gurp M and Van Grondelle R (1991) Polarized fluorescence measurements on ordered photosynthetic antenna complexes: Chlorosomes of Chloroflexus aurantiacusand B800–850 antenna complexes of Rhodobacter sphaeroides. Biophys J 59: 992-1001
Van Dorssen RJ, Vasmel H and Amesz J (1986) Pigment organization and energy transfer in the green photosynthetic bacterium Chloroflexus aurantiacus. II The chlorosome. Photosynth Res 9: 33-45
Van Grondelle R, Dekker JP, Gillbro T and Sundstrom V (1994) Energy transfer and trapping in photosynthesis. Biochim Biophys Acta 1187: 1-65
Wechsler T, Suter F, Fuller RC and Zuber H (1985) The complete amino acid sequence of the bacteriochlorophyll cbinding polypeptide from chlorosomes of the green photoynthetic bacterium Chloroflexus aurantiacus. FEBS Lett 181: 173-178
Wullink W, Knudsen J, Olson JM, Redlinger TE and Van Bruggen EFJ (1991) Localization of polypeptides in isolated chlorosomes from green phototrophic bacteria by immunogold labeling electron microscopy. Biochim Biophys Acta 1060: 97-105
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Frese, R., Oberheide, U., van Stokkum, I. et al. The organization of bacteriochlorophyll c in chlorosomes from Chloroflexus aurantiacus and the structural role of carotenoids and protein. Photosynthesis Research 54, 115–126 (1997). https://doi.org/10.1023/A:1005903613179
Issue Date:
DOI: https://doi.org/10.1023/A:1005903613179