Three-dimensional structure of the Rhodobacter sphaeroides rc-lh1-pufx complex: Dimerization and quinone channels promoted by PufX

Biochemistry

Volumn 52, Issue 43, 2013, Pages 7575-7585

  Qian, Pu ^a   Papiz, Miroslav Z ^b   Jackson, Philip J ^a   Brindley, Amanda A ^a   Ng, Irene W ^a   Olsen, John D ^a   Dickman, Mark J ^a   Bullough, Per A ^a   Hunter, C Neil ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PHOTOSYNTHESIS; BACTERIOCHLOROPHYLLS; CYTOPLASMIC DOMAINS; NUCLEAR MAGNETIC RESONANCE(NMR); RHODOBACTER SPHAEROIDES; SITE DIRECTED MUTAGENESIS; THREE-DIMENSIONAL STRUCTURE; TRANSMEMBRANE HELICES;

MASS SPECTROMETRY; POLYPEPTIDES; SOLAR ENERGY; SYNTHESIS (CHEMICAL); THREE DIMENSIONAL; X RAY CRYSTALLOGRAPHY;

DIMERIZATION;

BACTERIAL PROTEIN; BACTERIOCHLOROPHYLL A; POLYPEPTIDE; QUINONE DERIVATIVE; REACTION CENTER LIGHT HARVESTING 1 PUFX PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; DIMERIZATION; ELECTRON MICROSCOPY; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; RHODOBACTER SPHAEROIDES; SITE DIRECTED MUTAGENESIS; X RAY CRYSTALLOGRAPHY;

BACTERIAL PROTEINS; BACTERIOCHLOROPHYLL A; BENZOQUINONES; CAROTENOIDS; LIGHT-HARVESTING PROTEIN COMPLEXES; MASS SPECTROMETRY; MODELS, MOLECULAR; OXIDATION-REDUCTION; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; RHODOBACTER SPHAEROIDES; X-RAY DIFFRACTION;

EID: 84887072558     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4011946     Document Type: Article

References (52)

1. Bullough, P. A., Qian, P., and Hunter, C. N. (2008) Reaction center-light harvesting core complexes of purple bacteria, in The Purple Phototrophic Bacteria (Hunter, C. N., Daldal, F., Thurnauer, M. C., and Beatty, J. T., Eds.), pp 155-179, Springer, Dordrecht.
2. 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
3. Qian, P., Hunter, C. N., and Bullough, P. A. (2005) The 8.5 Å projection structure of the core RC-LH1-PufX dimer of Rhodobacter sphaeroides J. Mol. Biol. 349, 948-960
4. Farchaus, J. W., Gruenberg, H., and Oesterhelt, D. (1990) Complementation of a reaction center-deficient Rhodobacter sphaeroides pufLMX deletion strain in trans with pufBALM does not restore the photosynthesis-positive phenotype J. Bacteriol. 172, 977-985
5. Lilburn, T. G., Haith, C. E., Prince, R. C., and Beatty, J. T. (1992) Pleiotropic effects of pufX gene deletion on the structure and function of the photosynthetic apparatus of Rhodobacter capsulatus Biochim. Biophys. Acta 1100, 160-170
6. Francia, F., Wang, J., Zischka, H., Venturoli, G., and Oesterhelt, D. (2002) Role of the N- 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
7. Ratcliffe, E. C., Tunnicliffe, R. B., Ng, I. W., Adams, P. G., Qian, P., Holden-Dye, K., Jones, M. R., Williamson, M. P., and Hunter, C. N. (2011) Experimental evidence that the membrane-spanning helix of PufX adopts a bent conformation that facilitates dimerisation of the Rhodobacter sphaeroides RC-LH1 complex through N-terminal interactions Biochim. Biophys. Acta 1807, 95-107
8. Qian, P., Bullough, P., and Hunter, C. N. (2008) Three-dimensional reconstruction of a membrane-bending complex J. Biol. Chem. 283, 14002-14011
9. Frese, R. N., Pàmies, J. C., Olsen, J. D., Bahatyrova, S., van der Weij-de Wit, C. D., Aartsma, T. J., Otto, C., Hunter, C. N., Frenkel, D., and van Grondelle, R. (2008) Protein shape and crowding drive domain formation and curvature in biological membranes Biophys. J. 94, 640-647
10. Adams, P. G., Mothersole, D. J., Ng, I. W., Olsen, J. D., and Hunter, C. N. (2011) Monomeric RC-LH1 core complexes retard LH2 assembly and intracytoplasmic membrane formation in PufX-minus mutants of Rhodobacter sphaeroides Biochim. Biophys. Acta 1807, 1044-1055
11. Tucker, J. D., Siebert, C. A., Escalante, M., Adams, P. G., Olsen, J. D., Otto, C., Stokes, D. L., and Hunter, C. N. (2010) Membrane invagination in Rhodobacter sphaeroides is initiated at curved regions of the cytoplasmic membrane, then forms both budded and fully detached spherical vesicles Mol. Microbiol. 76, 833-847
12. Sener, M. K., Olsen, J. D., Hunter, C. N., and Schulten, K. (2007) Atomic-level structural and functional model of a bacterial photosynthetic membrane vesicle Proc. Natl. Acad. Sci. U.S.A. 104, 15723-15728
13. Jones, M. R., Fowler, G. J. S., Gibson, L. C. D., Grief, G. G., Olsen, J. D., Crielaard, W., and Hunter, C. N. (1992) Mutants of Rhodobacter sphaeroides lacking one or more pigment-protein complexes and complementation with reaction-centre, LH1, and LH2 genes Mol. Microbiol. 6, 1173-1184
14. Leslie, A. G. W. (1999) Integration of macromolecular diffraction data Acta Crystallogr., Sect. D 55, 1696-1702
15. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Krissinel, E. B., Leslie, A. G. W., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments Acta Crystallogr., Sect. D 67, 235-242
16. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674
17. Cowtan, K. and Main, P. (1998) Miscellaneous algorithms for density modification Acta Crystallogr., Sect. D 54, 487-493
18. 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
19. McLuskey, K., Prince, S. M., Cogdell, R. J., and Isaacs, N. W. (2001) The crystallographic structure of the B800-820 LH3 light-harvesting complex from the purple bacteria Rhodopseudomonas acidophila strain 7050 Biochemistry 40, 8783-8789
20. Ermler, U., Fritzsch, G., Buchanan, S. K., and Michel, H. (1994) Structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2.65 Å resolution: Cofactors and protein-cofactor interactions Structure 2, 925-936
21. Koepke, J., Hu, X. C., Muenke, C., Schulten, K., and Michel, H. (1996) The crystal structure of the light-harvesting complex II (B800-B850) from Rhodospirillum molischanum Structure 4, 581-597
22. Sali, A. and Blundell, T. L. (1993) Comparative protein modeling by satisfaction of spatial restraints J. Mol. Biol. 234, 779-815
23. Conroy, M. J., Westerhuis, W. H., Parkes-Loach, P. S., Loach, P. A., Hunter, C. N., and Williamson, M. P. (2000) The solution structure of Rhodobacter sphaeroides LH1β reveals two helical domains separated by a more flexible region: Structural consequences for the LH1 complex J. Mol. Biol. 298, 83-94
24. Tunnicliffe, R. B., Ratcliffe, E. C., Hunter, C. N., and Williamson, M. P. (2006) The solution structure of the PufX polypeptide from Rhodobacter sphaeroides FEBS Lett. 580, 6967-6971
25. 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
26. Ho, B. K. and Gruswitz, F. (2008) HOLLOW: Generating accurate representations of channel and interior surfaces in molecular structures BMC Struct. Biol 8, 49-54
27. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific Inc., San Carlos, CA.
28. - state energy on the conjugation length J. Phys. Chem. B 104, 5011-5019
29. Clayton, R. K. (1966) Spectroscopic analysis of bacteriochlorophylls in vitro and in vivo Photochem. Photobiol. 5, 669-677
30. Sistrom, W. R. (1978) Control of Antenna Pigment Components, in The Photosynthetic Bacteria (Clayton, R. K. and Sistrom, W. R., Eds.) pp 841-848, Plenum, New York.
31. Broglie, R. M., Hunter, C. N., Delepelaire, P., Niederman, R. A., Chua, N.-H., and Clayton, R. K. (1980) Isolation and characterization of the pigment-protein complexes of Rhodopseudomonas sphaeroides by lithium dodecyl sulfate polyacrylamide gel electrophoresis Proc. Natl. Acad. Sci. U.S.A. 77, 87-91
32. Grimes, M., Burroughs, J. N., Gouet, P., Diprose, J. M., Malby, R., Zientara, S., Mertens, P. P., and Stuart, D. I. (1998) The atomic structure of the bluetongue virus core Nature 395, 470-478
33. Olsen, J. D., Sturgis, J. N., Westerhuis, W. H., Fowler, G. J. S., Hunter, C. N., and Robert, B. (1997) Site-directed modification of the ligands to the bacteriochlorophylls of the light-harvesting LH1 and LH2 complexes of Rhodobacter sphaeroides Biochemistry 36, 12625-12632
34. Sturgis, J. N., Olsen, J. D., Robert, B., and Hunter, C. N. (1997) Functions of conserved tryptophan residues of the core light-harvesting complex of Rhodobacter sphaeroides Biochemistry 36, 2772-2778
35. Olsen, J. D., Sockalingum, G. D., Robert, B., and Hunter, C. N. (1994) Modification of a hydrogen bond to a bacteriochlorophyll a molecule in the light harvesting 1 antenna of Rhodobacter sphaeroides Proc. Natl. Acad. Sci. U.S.A. 91, 7124-7128
36. Pornillos, O., Ganser-Pornillos, B. K., Kelly, B. N., Hua, Y. Z., Whitby, F. G., Stout, C. D., Sundquist, W. I., Hill, C. P., and Yeager, M. (2009) X-ray structures of the hexameric building block of the HIV capsid Cell 137, 1282-1292
37. Garcia, B. L., Ramyar, K. X., Tzekou, A., Ricklin, D., McWhorter, W. J., Lambris, J. D., and Geisbrecht, B. V. (2010) Molecular basis for complement recognition and inhibition determined by crystallographic studies of the staphylococcal complement inhibitor (SCIN) bound to C3c and C3b J. Mol. Biol. 402, 17-29
38. Dezi, M., Francia, F., Mallardi, A., Colafemmina, G., Palazzo, G., and Venturoli, G. (2007) Stabilization of charge separation and cardiolipin confinement in antenna-reaction center complexes purified from Rhodobacter sphaeroides Biochim. Biophys. Acta 1767, 1041-1056
39. Koepke, J., Krammer, E. M., Klingen, A. R., Sebban, P., Ullmann, G. M., and Fritzsch, G. (2007) pH modulates the quinone position in the photosynthetic reaction center from Rhodobacter sphaeroides in the neutral and charge separated states J. Mol. Biol. 371, 396-409
40. Pugh, R. J., McGlynn, P., Jones, M. R., and Hunter, C. N. (1998) The LH1-RC core complex of Rhodobacter sphaeroides: Interaction between components, time-dependent assembly, and topology of the PufX protein Biochim. Biophys. Acta 1366, 301-316
41. Ng, I. W. (2008) A structural and functional study of the RC-LH1-PufX core complex from Rhodobacter sphaeroides, Ph.D. Thesis, University of Sheffield, Sheffield, United Kingdom.
42. Bahatyrova, S., Frese, R. N., Siebert, C. A., Olsen, J. D., van der Werf, K. O., van Grondelle, R., Niederman, R. A., Bullough, P. A., Otto, C., and Hunter, C. N. (2004) The native architecture of a photosynthetic membrane Nature 430, 1058-1062
43. Magis, G. J., Olsen, J. D., Reynolds, N. P., Leggett, G. J., Hunter, C. N., Aartsma, T. J., and Frese, R. N. (2011) Use of engineered unique cysteine residues to facilitate oriented coupling of proteins directly to a gold substrate Photochem. Photobiol. 87, 1050-1057
44. Šlouf, V., Chabera, P., Olsen, J. D., Martin, E. C., Qian, P., Hunter, C. N., and Polivka, T. (2012) Photoprotection in a purple phototrophic bacterium mediated by oxygen-dependent alteration of carotenoid excited-state properties Proc. Natl. Acad. Sci. U.S.A. 109, 8570-8575
45. 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
46. 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
47. Visscher, K. J., Bergström, H., Sundström, V., Hunter, C. N., and van Grondelle, R. (1989) Temperature dependence of energy-transfer from the long wavelength antenna BChl-896 to the reaction center in Rhodospirillum rubrum, Rhodobacter sphaeroides (w.t. and M21 mutant) from 77 to 177K, studied by picosecond absorption spectroscopy Photosynth. Res. 22, 211-217
48. Hess, S., Chachisvilis, M., Timpmann, K., Jones, M. R., Fowler, G. J. S., Hunter, C. N., and Sundström, V. (1995) Temporally and spectrally resolved subpicosecond energy transfer within the peripheral antenna complex (LH2) and from LH2 to the core antenna complex in photosynthetic purple bacteria Proc. Natl. Acad. Sci. U.S.A. 92, 12333-12337
49. Noy, D., Moser, C. C., and Dutton, P. L. (2006) Design and engineering of photosynthetic light-harvesting and electron transfer using length, time, and energy scales Biochim. Biophys. Acta 1757, 90-105
50. Comayras, R., Jungas, C., and Lavergne, J. (2005) Functional consequences of the organization of the photosynthetic apparatus in Rhodobacter sphaeroides. I. Quinone domains and excitation transfer in chromatophores and reaction center center antenna complexes J. Biol. Chem. 280, 11203-11213
51. Sener, M., Hsin, J., Trabuco, L. G., Villa, E., Qian, P., Hunter, C. N., and Schulten, K. (2009) Structural model and excitonic properties of the dimeric RC-LH1-PufX complex from Rhodobacter sphaeroides Chem. Phys. 357, 188-197
52. Bahatyrova, S., Frese, R. N., van der Werf, K. O., Otto, C., Hunter, C. N., and Olsen, J. D. (2004) Flexibility and size heterogeneity of the LH1 light harvesting complex revealed by atomic force microscopy: functional significance for bacterial photosynthesis J. Biol. Chem. 279, 21327-21333