Hexacoordination of bacteriochlorophyll in photosynthetic antenna LH1

Biochemistry

Volumn 45, Issue 6, 2006, Pages 1910-1918

  Fiedor, Leszek ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CHEMICAL COMPOUNDS; CHLOROPHYLL; PIGMENTS; PROTEINS; SPECTRUM ANALYSIS;

BACTERIOCHLOROPHYLL; HEXACOORDINATION; PHOTOSYNTHETIC ANTENNA LH1; QX TRANSITION ENERGY;

PHOTOSYNTHETIC MEMBRANES;

APOPROTEIN; BACTERIOCHLOROPHYLL; CAROTENOID;

ARTICLE; CHROMATOPHORE; COMPLEX FORMATION; ENERGY TRANSFER; LIGHT HARVESTING SYSTEM; NONHUMAN; PHOTOSYNTHESIS; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; SPECTROSCOPY;

BACTERIAL PROTEINS; BACTERIOCHLOROPHYLLS; CAROTENOIDS; ENERGY TRANSFER; INTRACELLULAR MEMBRANES; LIGANDS; LIGHT-HARVESTING PROTEIN COMPLEXES; MOLECULAR STRUCTURE; SPECTRUM ANALYSIS;

BACTERIA (MICROORGANISMS); PHOTOBACTERIA; PROTEOBACTERIA;

EID: 32344438831     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0514055     Document Type: Article

References (83)

1. Scheer, H. (1991) Chlorophylls, CRC Press, Boca Raton, FL.
2. Hanson, L. K. (1991) Molecular orbital theory of monomer pigments, in Chlorophylls (Scheer, H., Ed.) pp 993-1012, CRC Press, Boca Raton, FL.
3. Robert, B., and Lutz, M. (1985) Structures of antenna complexes of several Rhodospirillales from their resonance Raman spectra, Biochim. Biophys. Acta 807, 10-23.
4. Parkes-Loach, P. S., Michalski, T. J., Bass, W. J., Smith, U., and Loach, P. A. (1990) Probing the bacteriochlorophyll binding site by reconstitution of the light-harvesting complex of Rhodospirillum rubrum with bacteriochlorophyll a analogues, Biochemistry 29, 2951-2960.
5. Chang, M. C., Callahan, P. M., Parkes-Loach, P. S., Cotton, T. M., and Loach, P. A. (1990) Spectroscopic characterization of the light-harvesting complex of Rhodospirillum rubrum and its structural subunit, Biochemistry 29, 421-429.
6. Scheer, H., and Struck, A. (1993) Bacterial reaction centers with modified tetrapyrrole chromophores, in The Photosynthetic Reaction Center (Deisenhofer, J., and Norris, J. R., Eds.) pp 157-192, Academic Press, San Diego.
7. Sturgis, J. N., Jirsakova, V., Reiss-Husson, F., Cogdell, R. J., and Robert, B. (1995) Structure and properties of the bacteriochlorophyll binding site in peripheral light-harvesting complexes of purple bacteria, Biochemistry 34, 517-523.
8. Davis, C. M., Parkes-Loach, P. S., Cook, C. K., Meadows, K. A., Bandilla, M., Scheer, H., and Loach, P. A. (1996) Comparison of the structural requirements for bacteriochlorophyll binding in the core light-harvesting complexes of Rhodospirillum rubrum and Rhodobacter sphaeroides using reconstitution methodology with bacteriochlorophyll analogs, Biochemistry 35, 3072-3084.
9. Yang, C., Kosemund, K., Cornet, C., and Paulsen, H. (1999) Exchange of pigment-binding amino acids in light-harvesting chlorophyll a/b protein, Biochemistry 38, 16205-16213.
10. Deisenhofer, J., and Norris, J. R. (1993) The Photosynthetic Reaction Center, Academic Press, San Diego.
11. McDermott, G., Prince, S. M., Freer, A. A., Hawthornthwaite-Lawless, A. M., Papiz, M. Z., Cogdell, R. J., and Isaacs, N. W. (1995) Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria, Nature 374, 517-521.
12. Koepke, J., Hu, X., Muenke, C., Schulten, K., and Michel, H. (1996) The crystal structure of the light-harvesting complex II (B800-850) from Rhodospirillum molischianum, Structure 4, 581-597.
13. Jordan, P., Fromme, P., Witt, H. T., Klukas, O., Saenger, W., and Krauss, N. (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution, Nature 411, 909-917.
14. Byrdin, M., Jordan, P., Krauss, N., Fromme, P., Stehlik, D., and Schlodder, E. (2002) Light harvesting in photosystem I: Modeling based on the 2.5-Å structure of photosystem I from Synechococcus elongatus, Biophys. J. 83, 433-457.
15. Kamiya, N., and Shen, J.-R. (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution, Proc. Natl. Acad. Sci. U.S.A. 100, 98-103.
16. Ben-Shem, A., Frolow, F., and Nelson, N. (2003) Crystal structure of plant photosystem I, Nature 426, 630-635.
17. Liu, Z., Yan, H., Wang, K., Kuang, T., Jiping, Z., Gui, L., An, X., and Chang, W. (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution, Nature 428, 287-292.
18. Sturgis, J. N., and Robert, B. (1994) Thermodynamics of membrane polypeptide oligomerization in light-harvesting complexes and associated structural changes, J. Mol. Biol. 238, 445-454.
19. Loach, P. A., and Parkes-Loach, P. S. (1995) Structure-function relationships in core light-harvesting complexes (LHI) as determined by characterization of the structural subunit and by reconstitution experiments, in Anoxygenic Photosynthetic Bacteria (Blankenship, R. E., Madigan, M. T., and Bauer, C. E., Eds.) pp 437-471, Kluwer Academic Publishers, Dordrecht, The Netherlands.
20. Zuber, H., and Cogdell, R. J. (1995) Structure and organization of purple bacterial antenna complexes, in Anoxygenic Photosynthetic Bacteria (Blankenship, R. E., Madigan, M. T., and Bauer, C. E., Eds.) pp 315-348, Kluwer Academic Publishers, Dordrecht, The Netherlands2E
21. Goldsmith, J. O., King, B., and Boxer, S. G. (1996) Mg coordination by amino acid side chains is not required for assembly and function of the special pair in bacterial photosynthetic reaction centers, Biochemistry 35, 2421-2428.
22. Schunck, E., and Marchlewski, L. (1894) Zur Chemie des Chlorophylls, Liebigs Ann. Chem. 278, 329-345.
23. Willstätter, R., and Stoll, A. (1913) Untersuchungen über Chlorophyll, Verlag von Julius Springer, Berlin.
24. Vernon, L. P., and Seely, G. R. (1966) The Chlorophylls, Academic Press, London.
25. Strell, M., and Urumow, T. (1977) Neue Methoden zur Einführung von Metallen in Chlorophyll-derivative, Liebigs Ann. Chem., 970-974.
26. Hynninen, P. H. (1991) Chemistry of chlorophylls: Modifications, in Chlorophylls (Scheer, H., Ed.) pp 145-209, CRC Press, Boca Raton, FL.
27. Hartwich, G., Fiedor, L., Simonin, I., Cmiel, E., Schäfer, W., Noy, D., Scherz, A., and Scheer, H. (1998) Metal-Substituted Bacteriochlorophylls. 1. Preparation and influence of metal and coordination on spectra, J. Am. Chem. Soc. 120, 3675-3683.
28. Noy, D., Fiedor, L., Hartwich, G., Scheer, H., and Scherz, A. (1998) Metal-substituted bacteriochlorophylls. 2. Changes in redox potentials and electronic transition energies are dominated by intramolecular electrostatic interactions, J. Am. Chem. Soc. 120, 3684-3693.
29. Cotton, A. A., and Wilkinson, G. (1988) Advanced Inorganic Chemistry, 5th ed., John Wiley & Sons, NewYork.
30. Evans, T. A., and Katz, J. J. (1975) Evidence for 5- and 6-coordinated magnesium in bacteriochlorophyll a from visible absorption spectroscopy, Biochim. Biophys. Acta 396, 414-426.
31. Callahan, P. M., and Cotton, T. M. (1987) Assignment of bacteriochlorophyll a ligation state from absorption and resonance Raman spectra, J. Am. Chem. Soc. 109, 7001-7007.
32. Sauer, K., Smith, J. R. L., and Schultz, A. J. (1966) The dimerization of chlorophyll a, chlorophyll b, and bacteriochlorophyll in solution, J. Am. Chem. Soc. 88, 2681-2688.
33. Ballschmiter, K., Truesdell, K., and Katz, J. J. (1969) Aggregation of chlorophyll in nonpolar solvents from molecular weight measurements, Biochim. Biophys. Acta 184, 604-613.
34. Katz, J. J., Shipman, L. L., Cotton, T. M., and Janson, T. J. (1978) Chlorophyll aggregation: Coordination interactions in chlorophyll monomers, dimers, and oligomers, in The Porphyrins (Dolphin, D., Ed.) pp 401-458, Academic Press, New York.
35. Balaban, T. S. (2003) Are syn-ligated (bacterio)chlorophyll dimers energetic traps in light-harvesting systems? FEBS Lett. 545, 97-102.
36. Oba, T., and Tamiaki, H. (2002) Which side of the π-macrocycle plane of (bacterio)chlorophylls is favored for binding of the fifth ligand? Photosynth. Res. 74, 1-10.
37. Katz, J. J., Strain, H. H., Leussing, D. L., and Dougherty, R. C. (1968) Chlorophyll-ligand interactions from nuclear magnetic resonance studies, J. Am. Chem. Soc. 90, 784-791.
38. Watanabe, T., and Kobayashi, M. (1991) Electrochemistry of chlorophylls, in Chlorophylls (Scheer, H., Ed.) pp 287-315, CRC Press, Boca Raton, FL.
39. Omata, T., and Murata, N. (1983) Preparation of chlorophyll a, chlorophyll b and bacteriochlorophyll a by column chromatography with DEAE-Sepharose CL-6B and Sepharose CL-6B, Plant Cell Physiol. 24, 1093-1100.
40. Watanabe, T., Hongu, A., Honda, K., Nakazato, M., Mazaki, H., Konno, M., and Saitoh, S. (1984) Preparation of chlorophylls and pheophytins by isocratic liquid chromatography, Anal. Chem. 56, 251-256.
41. Fiedor, L., Rosenbach-Belkin, V., and Scherz, A. (1992) The stereospecific interaction between chlorophylls and chlorophyllase. Possible implication for chlorophyll biosynthesis and degradation, J. Biol. Chem. 267, 22043-22047.
42. Fiedor, L., and Scheer, H. (2005) Trapping of an intermediate of LH1 complex assembly beyond the B820 subunit, J. Biol. Chem. 280, 20921-20926.
43. Picorel, R., Belanger, G., and Gingras, G. (1983) Antenna holochrome B880 of Rhodospirillum rubrum S1. Pigment, phospholipid, and polypeptide composition, Biochemistry 22, 2491-2497.
44. Fiedor, L., Akahane, J., and Koyama, Y. (2004) Carotenoid-induced cooperative formation of bacterial photosynthetic LH1 complex, Biochemistry 43, 16487-16496.
45. Kania, A., and Fiedor, L. (2005) Steric control of bacteriochlorophyll ligation, J. Am. Chem. Soc. 128, 454-458.
46. Scherz, A., and Rosenbach-Belkin, V. (1989) Comparative study of optical absorption and circular dichroism of bacteriochlorophyll oligomers in Triton X-100, the antenna pigment B850, and the primary donor P-860 of photosynthetic bacteria indicates that all are similar dimers of bacteriochlorophyll a, Proc. Natl. Acad. Sci. U.S.A. 86, 1505-1509.
47. Miller, J. F., Hinchigeri, S. B., Parkes-Loach, P. S., Callahan, P. M., Sprinkle, J. R., Riccobono, J. R., and Loach, P. A. (1987) Isolation and characterization of a subunit form of the light-harvesting complex of Rhodospirillum rubrum, Biochemistry 26, 5055-5062.
48. Permentier, H. P., Neerken, S., Overmann, J., and Amesz, J. (2001) A bacteriochlorophyll a antenna complex from purple bacteria absorbing at 963 nm, Biochemistry 40, 5573-5578.
49. Schwerzmann, R. U., and Bachofen, R. (1989) Carotenoid profiles in pigment-protein complexes of Rhodospirillum rubrum, Plant Cell Physiol. 30, 497-504.
50. Davis, C. M., Bustamante, P. L., and Loach, P. A. (1995) Reconstitution of the bacterial core light-harvesting complexes of Rhodobacter sphaeroides and Rhodospirillum rubrum with isolated α- and β-polypeptides, bacteriochlorophyll a, and carotenoid, J. Biol. Chem. 270, 5793-5804.
51. Akahane, J., Rondonuwu, F. S., Fiedor, L., Watanabe, Y., and Koyama, Y. (2004) Dependence of singlet-energy transfer on the conjugation length of carotenoids reconstituted into the LH1 complex from Rhodospirillum rubrum G9, Chem. Phys. Lett. 393, 184-191.
52. Umetsu, M., Wang, Z.-Y., Yoza, K., Kobayashi, M., and Nozawa, T. (2000) Interaction of photosynthetic pigments with various organic solvents 2. Application of magnetic circular dichroism to bacteriochlorophyll a and light-harvesting complex 1, Biochim. Biophys. Acta 1457, 106-117.
53. Küpper, H., Spiller, M., and Küpper, F. C. (2000) Photometric method for the quantification of chlorophylls and their derivatives in complex mixtures: Fitting with Gauss-peak spectra, Anal. Biochem. 286, 247-256.
54. Eichwurzel, I., Stiel, H., Teuchner, K., Leupold, D., Scheer, H., Salomon, Y., and Scherz, A. (2000) Photophysical consequences of coupling bacteriochlorophyll a with serine and its resulting solubility in water, Photochem. Photobiol. 72, 204-209.
55. Zucchelli, G., Jennings, R. C., Garlaschi, F. M., Cinque, G., Bassi, R., and Cremonesi, O. (2002) The calculated in vitro and in vivo chlorophyll a absorption bandshape, Biophys. J. 82, 378-390.
56. Kramer, H. J. M., Pennoyer, J. D., van Grondelle, R., Westerhuis, W. H. J., Niederman, R. A., and Amesz, J. (1984) Low-temperature optical properties and pigment organization of the B875 light-harvesting bacteriochlorophyll- protein complex of purple photosynthetic bacteria, Biochim. Biophys. Acta 767, 335-344.
57. Van Dorssen, R. J., Hunter, C. N., van Grondelle, R., Korenhof, A. H., and Amesz, J. (1988) Spectroscopic properties of antenna complexes of Rhodobacter sphaeroides in vitro, Biochim. Biophys. Acta 932, 179-188.
58. Law, C. J., and Cogdell, R. J. (1998) The effect of chemical oxidation on the fluorescence of the LH1 (B880) complex from the purple bacterium Rhodobium marinum, FEBS Lett. 432, 27-30.
59. Fiedor, L., Leupold, D., Teuchner, K., Voigt, B., Hunter, C. N., Scherz, A., and Scheer, H. (2001) Excitation trap approach to analyze size and pigment-pitment coupling: Reconstitution of LH1 antenna of Rhodobacter sphaeroides with Ni-substituted bacteriochlorophyll, Biochemistry 40, 3737-3747.
60. Qian, P., Yagura, T., Koyama, Y., and Cogdell, R. J. (2000) Isolation and purification of the reaction center (RC) and the core (RC-LH1) complex from Rhodobium marinum: The LH1 ring of the detergent-solubilized complex contains 32 bacteriochlorophylls, Plant Cell Physiol. 41, 1347-1353.
61. Jamieson, S. J., Wang, P., Qian, P., Kirkland, J. Y., Conroy, M. J., Hunter, C. N., and Bullough, P. A. (2002) Projection structure of the photosynthetic reaction centre-antenna complex of Rhodospirillum rubrum at 8.5 Å resolution, EMBO J. 21, 3927-3935.
62. Qian, P., Addlesee, H. A., Ruban, A. V., Wang, P., and Bullough, P. A. (2003) A reaction center-light-harvesting 1 complex (RC-LH1) from a Rhodospirillum rubrum mutant with altered esterifying pigments, J. Biol. Chem. 278, 23678-23685.
63. Gudowska-Nowak, E., Newton, M. D., and Fajer, J. (1990) Conformational and environmental effects on bacteriochlorophyll optical spectra: Correlations of calculated spectra with structural results, J. Phys. Chem. 94, 5795-5801.
64. Lapouge, K., Nveke, A., Gall, A., Ivancich, A., Seguin, J., Scheer, H., Sturgis, J. N., Matiolli, T. A., and Robert, B. (1999) Conformation of bacteriochlorophyll molecules in photosynthetic proteins from purple bacteria, Biochemistry 38, 11115-11121.
65. Cotton, T. M., and Van Duyne, R. P. (1981) Characterization of bacteriochlorophyll interactions in vitro by resonance Raman spectroscopy, J. Am. Chem. Soc. 103, 6020-6026.
66. Fujiwara, M., and Tasumi, M. (1986) Resonance Raman and infrared studies on axial coordinatioon of chlorophyll a and b in vitro, J. Phys. Chem. 90, 250-255.
67. Sturgis, J. N., and Robert, B. (1997) Pigment binding-site and electronic properties in light-harvesting proteins of purple bacteria, J. Phys. Chem. B 101, 7227-7231.
68. Näveke, A., Lapouge, K., Sturgis, J. N., Hartwich, G., Simonin, I., Scheer, H., and Robert, B. (1997) Resonance Raman spectroscopy of metal-substituted bacteriochlorophylls: Characterization of Raman bands sensitive to bacteriochlorin conformation, J. Raman Spectrosc. 28, 599-604.
69. Yerushalmi, R., Scherz, A., and Baldridge, K. K. (2004) Direct experimental evaluation of charge scheme performance by a molecular charge-meter, J. Am. Chem. Soc. 126, 5897-5905.
70. Krawczyk, S. (1989) The effects of hydrogen bonding and coordination interaction in visible absorption and vibrational spectra of chlorophyll a, Biochim. Biophys. Acta 976, 140-149.
71. Fenna, R. E., and Matthews, B. W. (1975) Chlorophyll arrangement in a bacteriochlorophyll protein from Chlorobium limicola, Nature 258, 573-577.
72. Fiedor, L., Rosenbach-Belkin, V., Sai, M., and Scherz, A. (1996) Preparation of tetrapyrrole-amino acid covalent complexes, Plant Physiol. Biochem. 34, 393-398.
73. Wang, Z.-Y., Gokan, K., Kobayashi, M., and Nozawa, T. (2005) Solution structures of the core light-harvesting α and β polypeptides from Rhodospirillum rubrum: Implications for the pigment-protein and protein-protein interactions, J. Mol. Biol. 347, 465-477.
74. Roszak, A. W., Howard, T. D., Southall, J., Gardiner, A. T., Law, C. J., Isaacs, N. W., and Cogdell, R. J. (2003) Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris, Science 302, 1969-1972.
75. Gerken, U., Jelezko, F., Götze, B., Branschädel, M., Tietz, C., Ghosh, R., and Wrachtrup, J. (2003) Membrane environment reduces the accessible conformational space available to an integral membrane protein, J. Phys. Chem. 107, 338-343.
76. Fotiadis, D., Qian, P., Philippsen, A., Bullough, P. A., Engel, A., and Hunter, C. N. (2004) Structural analysis of the reaction center light-harvesting complex I photosynthetic core complex of Rhodospirillum rubrum using atomic force microscopy, J. Biol. Chem. 279, 2063-2068.
77. Bahatyrova, S., Frese, R. N., van der Werf, K. O., Otto, C., Hunter, C. N., and Olsen, C. N. (2004) Flexibility and size heterogeneity of the LH1 light harvesting complex revealed by atomic force microscopy, J. Biol. Chem. 279, 21327-21333.
78. Lapouge, K., Näveke, A., Robert, B., Scheer, H., and Sturgis, J. N. (2000) Exchanging cofactors in the core antennae from purple bacteria: Structure and properties of Zn-bacteriopheophytin-containing LH1, Biochemistry 39, 1091-1099.
79. 2 or S1 state of bacteriochlorophyll, J. Chem. Phys. 98, 8012-8023.
80. Ritz, T., Damjanovic, A., Schulten, K., Zhang, J.-P., and Koyama, Y. (2000) Efficient light harvesting through carotenoids, Photosynth. Res. 66, 125-144.
81. 2 state in a photosynthetic light-harvesting complex, Biophys. J. 80, 923-930.
82. Freer, A., Prince, S., Sauer, K., Papiz, M., Hawthornthwaite-Lawless, A., McDermott, G., Cogdell, R., and Isaacs, N. W. (1996) Pigment-pitment interactions and energy transfer in the antenna complex of the photosynthetic bacterium Rhodopseudomonas acidophila, Structure 4, 449-462.
83. Desamero, R. Z. B., Chynwat, V., van der Hoef, I., Jansen, F. J., Lugtenburg, J., Gosztola, D., Wasielewski, M. R., Cua, A., Bocian, D. F., and Frank, H. A. (1998) Mechanism of energy transfer from carotenoids to bacteriochlorophyll: Light-harvesting by carotenoids having different extents of π-electron conjugation incorporated into the B850 antenna complex from the carotenoidless bacterium Rhodobacter sphaeroides R-26.1, J. Phys. Chem. B 102, 8151-8162.