Interactions stabilizing the structure of the core light-harvesting complex (LH1) of photosynthetic bacteria and its subunit (B820)

Biochemistry

Volumn 43, Issue 22, 2004, Pages 7003-7016

  Parkes Loach, Pamela S ^a   Majeed, Alia P ^a   Law, Christopher J ^a,b   Loach, Paul A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BACTERIA; CHLOROPHYLL; PHOTOSYNTHESIS; POLYPEPTIDES; SULFUR;

BACTERIOCHLOROPHYLL; HISTIDINE; LIGANDS;

BIOCHEMISTRY;

3 METHYLHISTIDINE; 9 FLUORENYLMETHYL CHLOROFORMATE; AMINO ACID; ARGININE; BACTERIOCHLOROPHYLL; LIGAND; METHIONINE; POLYPEPTIDE; TRYPTOPHAN;

ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; LIGHT HARVESTING SYSTEM; NONHUMAN; PEPTIDE SYNTHESIS; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; RHODOSPIRILLUM RUBRUM;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BACTERIOCHLOROPHYLLS; LIGANDS; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; METHIONINE; METHYLHISTIDINES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; RHODOBACTER SPHAEROIDES; RHODOSPIRILLUM RUBRUM; SAFROLE; SEQUENCE HOMOLOGY, AMINO ACID;

BACTERIA (MICROORGANISMS); PHAEOSPIRILLUM; PHAEOSPIRILLUM MOLISCHIANUM; PHOTOBACTERIA; RHODOSPIRILLUM; RHODOSPIRILLUM RUBRUM;

EID: 2642588087     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049798f     Document Type: Article

References (59)

1. Karrasch, S., Bullough, P. A., and Ghosh, R. (1995) The 8.5 A projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits, EMBO J. 14, 631-638.
2. Lilburn, T. G., Prince, R. C., and Beatty, J. T. (1995) Mutation of the Ser2 codon of the light-harvesting B870 alpha polypeptide of Rhodobacter capsulatus partially suppresses the pufX phenotype, J. Bacteriol. 177, 4593-4600.
3. Papiz, M. Z., Prince, S. M., Hawthornthwaite-Lawless, A. M., McDermontt, G., Freer, A. A., Isaacs, N. W., and Cogdell, R. J. (1996) A model for the photosynthetic apparatus of purple bacteria, Trends Plant Sci. 1, 198-206.
4. Walz, T., and Ghosh, R. (1997) Two-dimensional crystallization of the light-harvesting I-reaction centre photounit from Rhodospirillum rubrum, J. Mol. Biol. 265, 107-111.
5. Jamieson, S. J., Wang, P., Qian, P., Kirkland, J. Y., Conroy, M. J., Hunter, C. N., and Bullogh, 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.
6. Scheuring, S., Sequin, J., Marco, S., Levy, D., Robert, B., and Rigaud, J.-L. (2003) Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM, Proc. Natl. Acad. Sci. U.S.A. 100, 1690-1693.
7. Westerhuis, W. H. J., Vos, M., van Grondelle. R., Amesz, J., and Niederman, R. A. (1998) Altered organization of light-harvesting complexes in phospholipids-enriched Rhodobacter sphaeroides chromatophores as determined by fluorescence yield and singlet-singlet annihilation measurements, Biochim. Biophys. Acta 1366, 317-329.
8. Jungas, C., Ranck, J.-L., Joliot, P., and Vermeglio, A. (1999) Supramolecular organization of the photosynthetic apparatus of Rhodobacter sphaeroides, EMBO J. 18, 534-542.
9. Francia, F., Wang, J., Venturoli, G., Melandri, B. A., Barz, W. P., and Oesterhelt, D. (1999) The reaction center-LH1 antenna complex of Rhodobacter sphaeroides contains one PufX molecule which is involved in dimerization of this complex, Biochemistry 38, 6834-6845.
10. Francia, F., Wang, J., Zischka, H., Venturoli, G., and Oesterhelt, D. (2002) Role of the NB and C-terminal regions of the PufX protein in the structural organization of the photosynthetic core complex of Rhodobacter sphaeroides, Eur. J. Biochem. 269, 1877-1885.
11. 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.
12. Deisenhofer, J., Epp, O., Miki, F., Huber, R., and Michel, H. (1984) X-ray structure analysis of a membrane protein complex: electron density map at 3 A resolution and a model of the chromophores of the photosynthetic reaction center from Rhodopseudomonas viridis, J. Mol. Biol. 180, 385-398.
13. Allen, J. P., Feher, G., Yeates, T. O., Rees, D. C., Deisenhofer, J., Michel, H., and Huber, R. (1986) Structural homology of reaction centers from Rhodopseudomonas sphaeroides and Rhodopseudomonas viridis as determined by X-ray diffraction, Proc. Natl. Acad. Sci. U.S.A. 83, 8589-8593.
14. Chang, C. H., Tiede, D., Tang, J., Smith, U., Norris, J., and Schiffer, M. (1986) Structure of Rhodopseudomonas sphaeroides R-26 reaction center, FEBS Lett. 205, 82-86.
15. 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.
16. 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, 591-597.
17. van Grondelle, R., Dekker, J. P., Gillbro, T., and Sundstrom, V. (1994) Energy transfer and trapping in photosynthesis, Biochim. Biophys. Acta 1187, 1-65.
18. Frese, R. N., Olsen, J. D., Branvall, R., Westerhuis, W. H. J., Hunter, C. N., and van Grondelle, R. (2000) The long-range supraorganization of the bacterial photosynthetic unit: a key role for PufX, Proc. Natl. Acad. Sci. U.S.A. 97, 5197-5202.
19. Hu, X., Ritz, T., Damjanovic, A., Autenrieth, F., and Schulten, K. (2002) Photosynthetic apparatus of purple bacteria, Q. Rev. Biophys. 35, 1-62.
20. Loach, P. A., Parkes, P. S., Miller, J. F., Hinchigeri, S., and Callahan, P. M. (1985) Structure-function relationships of the bacteriochlorophyll-protein light-harvesting complex of Rhodospirillum rubrum, in Molecular Biology of the Photosynthetic Apparatus (Arntzen, C., Bogorad, L., Bonitz, S., and Steinback, K., Eds.) Cold Spring Harbor Symposium, pp 197-209, Cold Spring Harbor, NY.
21. 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.
22. Heller, B. A., and Loach, P. A. (1990) Isolation and characterization of a subunit form of the B875 light-harvesting complex from Rhodobacter capsulatus, Photochem. Photobiol. 51, 621-627.
23. Chang, M. C., Meyer, L., and Loach, P. A. (1990) Isolation and characterization of a structural subunit from the core light-harvesting complex of Rhodobactor sphaeroides 2.4.1 and puc705-BA, Photochem. Photobiol. 52, 873-881.
24. Jirsakova, V., and Reiss-Husson, F. (1993) Isolation and characterization of the core light-harvesting complex B875 and its subunit form, B820, from Rhodocyclus gelatinosus, Biochim. Biophys. Acta 1138, 301-308.
25. Meckenstock, R. U., Brunisholz, R. A., and Zuber, H. (1992) The light-harvesting core-complex and the B820-subunit from Rhodopseudomonas marina. Part 1. Purification and characterization, FEBS Lett. 311, 128-134.
26. Kerfeld, C. A., Yeates, T. O., and Thornber, J. P. (1994) Biochemical and spectroscopic characterization of the reaction center-LH1 complex and the carotenoid-containing B820 subunit of Chromatium purpuratum, Biochim. Biophys. Acta 1185, 193-202.
27. Parkes-Loach, P. S., Sprinkle, J. R., and Loach, P. A. (1988) Reconstitution of the B873 light-harvesting complex of Rhodospirillum rubrum from the separately isolated α- and β-polypeptides and bacteriochlorophyll a, Biochemistry 27, 2718-2727.
28. Loach, P. A., and Parkes-Loach, P. S. (1995) Structure-function relationships in core light-harvesting complexes (LH1) as determined by characterization of the structural subunit and by reconstitution experiments, in Advances in Photosynthesis: Anoxygenic Photosynthetic Bacteria (Blankenship, R. E., Madigan, M. T., and Bauer, C. D., Eds.) pp 437-471, Kluwer Academic Publishers, Dordrecht, The Netherlands.
29. Loach, P. A., Parkes-Loach, P. S., Davis, C. M., and Heller, B. A. (1994) Probing protein structural requirements for formation of the core light-harvesting complex of photosynthetic bacteria using hybrid reconstitution methodology, Photosynth. Res. 40, 231-245.
30. Parkes-Loach, P. S., Jones, S. M., and Loach, P. A. (1994) Probing the structure of the core light-harvesting complex (LH1) of Rhodopseudomonas viridis by dissociation and reconstitution methodology, Photosynth. Res. 40, 247-261.
31. Todd, J. B., Parkes-Loach, P. S., Leykam, J. F., and Loach, P. A. (1998) In vitro reconstitution of the core and peripheral light-harvesting complexes of Rhodospirillum molischianum from separately isolated components, Biochemistry 37, 17458-17468.
32. Davis, C. M., Bustamante, P. L., Todd, J. B., Parkes-Loach, P. S., McGlynn, P., Olsen, J. D., McMaster, L., Hunter, C. N., and Loach, P. A. (1997) Evaluation of structure-function relationships in the core light-harvesting complex (LH1) of photosynthetic bacteria by reconstitution with mutant polypeptides, Biochemistry 36, 3671-3679.
33. Meadows, K. A., Parkes-Loach, P. S., Kehoe, J. W., and Loach, P. A. (1998) Reconstitution of light-harvesting complexes of photosynthetic bacteria using chemically synthesized polypeptides: I. Minimal requirements for subunit formation, Biochemistry 37, 3411-3417.
34. Kehoe, J. W., Meadows, K. A., Parkes-Loach, P. S., and Loach, P. A. (1998) Reconstitution of light-harvesting complexes of photosynthetic bacteria using chemically synthesized polypeptides: II. Determination of structural features that stabilize complex formation and implications on the structure of the subunit complex, Biochemistry 37, 3418-3428.
35. Todd, J. B., Recchia, P. A., Parkes-Loach, P. S., Olsen, J. D., Fowler, G. J. S., McGlynn, P., Hunter, C. N., and Loach, P. A. (1999) Minimal requirements for in vitro reconstitution of the structural subunit of light-harvesting complexes of photosynthetic bacteria, Photosynth. Res. 62, 85-98.
36. Meadows, K. A., Iida, K., Kazuichi, T., Recchia, P. A., Heller, B. A., Antonio, B., Nango, M., and Loach, P. (1995) Enzymatic and chemical cleavage of the core light-harvesting polypeptides of photosynthetic bacteria: Determination of the minimal polypeptide size and structure required for subunit and light-harvesting complex formation, Biochemistry 34, 1559-1574.
37. McGlynn, P., Westerhuis, W. H. J., Jones, M. R., and Hunter, C. N. (1996) Consequences for the organization of reaction center-light harvesting antenna 1 (LH1) core complexes of Rhodobacter sphaeroides arising from deletion of amino acid residues from the C terminus of the LH1 apolypeptide, J. Biol. Chem. 271, 3285-3292.
38. Berger, G., Wollenweber, A. M., Kleo, J., Andrianambinintsoa, S., and Mantele, W. G. (1987) A rapid preparative method for purification of bacteriochlorophyll-a and bacteriochlorophyll-b, J. Liq. Chromatogr. 10, 1519-1531.
39. Michalski, T. J., Hunt, J. E., Bradshaw, C., Wagner, A. M., Norris, J. R., and Katz, J. J. (1988) Enzyme-catalyzed organic syntheses: transesterification reactions of chlorophyll a, bacteriochlorophyll a, and derivatives with chlorophyllase, J. Am. Chem. Soc. 110, 5888-5891.
40. Tonn, S. J., Gogel, G. E., and Loach, P. A. (1977) Isolation and characterization of an organic solvent soluble polypeptide component from photoreceptor complexes of Rhodospirillum rubrum, Biochemistry 16, 877-885.
41. +, FEBS Lett. 129, 150-154.
42. Brunisholz, R. A., Suter, F., and Zuber, H. (1984) The light-harvesting polypeptides of Rhodospirillum rubrum. 1. the amino acid-sequence of the 2nd light-harvesting polypeptide b-880-beta (b-870-beta) of Rhodospirillum rubrum s-1 and the carotenoidless mutant g-9+ - aspects of the molecular-structure of the 2 light-harvesting polypeptides b-880-alpha (b-870-alpha) and b-880-beta (b-870-beta) and of the antenna complex b-880 (b-870) from Rhodospirillum rubrum-s, Hoppe-Seyler's Z. Physiol. Chem. 365, 675-688.
43. Lee, J. K., Kiley, P. J., and Kaplan, S. (1989) Posttranscriptional control of puc operon expression of b800-850 light-harvesting complex-formation in Rhodobacter sphaeroides, J. Bacteriol. 171, 3391-3405.
44. Theiler, R., Suter, F., Wiemken, V., and Zuber, H. (1984) The light-harvesting polypeptides of Rhodopseudomonas sphaeroides r-26.1. 1. isolation, purification and sequence analyses, Hoppe-Seyler's Z. Physiol. Chem. 365, 703-719.
45. Parkes-Loach, P. S., Law, C. J., Recchia, P. A., Kehoe, J., Nehrlich, S., Chen, J., and Loach, P. A. (2001) Role of the core region of the pufx protein in inhibition of reconstitution of the core light-harvesting complexes of Rhodobacter sphaeroides and Rhodobacter capsulatus, Biochemistry 40, 5593-5601.
46. Loach, P. A., Parkes-Loach, P. S., Chang, M. C., Heller, B. A., Bustamante, P. L., and Michalski, T. (1990) Comparison of structural subunits of the core light-harvesting complexes of photosynthetic bacteria, in Molecular Biology of Membrane-Bound Complexes in Phototrophic Bacteria (Drews, E. G., and Dawes, E. A., Eds.) pp 235-244, Plenum Press, New York.
47. van Mourik, F., van der Ord, J. R., Visscher, K. J., Parkes-Loach, P. A., Loach, P. A., Visschers, R. W., and van Grondelle, R. (1991) Exciton interactions in the light-harvesting antenna of photosynthetic bacteria studied with triplet-singlet spectroscopy and singlet-triplet annihilation on the B820 subunit form of Rhodospirillum rubrum, Biochim. Biophys. Acta 1059, 111-119.
48. Visschers, R. W., Chang, M. C., van Mourik, F., Parkes-Loach, P. S., Heller, B. A., Loach, P. A., and van Grondelle, R. (1991) Fluorescence polarization and low-temperature absorption spectroscopy of a subunit form of light-harvesting complex I from purple photosynthetic bacteria, Biochemistry 30, 5734-5742.
49. Chang, M. C., Callahan, P. C., 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.
50. Law, C. J., Chen, J., Parkes-Loach, P. S., and Loach, P. A. (2003) Interaction of bacteriochlorophyll with the LH1 and PufX polypeptides of photosynthetic bacteria: use of chemically synthesized analogues and covalently attached fluorescent probes, Photosynth. Res. 75, 193-210.
51. Barrick, D. (1994) Replacement of the proximal ligand of sperm whale myoglobin with free imidazole in the mutant His-93→Gly, Biochemistry 33, 6546-6554.
52. Pond, A. E., Roach, M. P., Thomas, M. R., Boxer, S. G., Dawson, J. H. (2000) The H93G myoglobin cavity mutant as a versatile template for modeling heme proteins: Ferrous, Ferric, and Ferryl mixed-ligand complexes with imidazole in the cavity, Inorg. Chem. 39, 6061-6066.
53. 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.
54. Wang, Z.-Y., Shimonaga, M., Muraoka, Y., Kobayashi, M., and Nozawa, T. (2001) Methionine oxidation and its effect on the stability of a reconstituted subunit of the light-harvesting complex from Rhodospirillum rubrum, Eur. J. Biochem. 268, 3375-3382.
55. Visschers, R. W., van Grondelle, R., and Robert, B. (1993) Resonance Raman spectroscopy of the B820 subunit of the core antenna from Rhodospirillum rubrum G9, Biochim. Biophys. Acta 1183, 369-373.
56. Wang, Z.-Y., Muraoka, Y., Shimonaga, M., Kobayashi, M., and Nozawa, T. (2002) Selective detection and assignment of the solution NMR signals of bacteriochlorophyll a in a reconstituted subunit of a light-harvesting complex, J. Am. Chem. Soc. 124, 1072-1078.
57. Arluison, V., Seguin, J., Le Caer, J.-P., Sturgis, J. N., and Robert, B. (2004) Hydrophobic pockets at the membrane interface: An original mechanism for membrane protein interactions, Biochemistry 43, 1276-1282.
58. Zuber, H., and Cogdell, R. J. (1995) in Anoxygenic Photosynthetic Bacteria (Blankenship, R. E., Madigan, M. T., and Bauer, C. E., Eds.) pp 315-348, Kluwer Academic Publishers, Dordrecht.
59. 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.