On the role of basic residues in adapting the reaction centre-LH1 complex for growth at elevated temperatures in purple bacteria

Photosynthesis Research

Volumn 86, Issue 1-2, 2005, Pages 81-100

  Watson, Ashley J ^a   Hughes, Arwel V ^a   Fyfe, Paul K ^a,c   Wakeham, Marion C ^a   Holden Dye, Kate ^a   Heathcote, Peter ^b   Jones, Michael R ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Basic residues; Core complex; LH1 antenna; Mutagenesis; Reaction centre; Thermal stability

Indexed keywords

MEMBRANE PROTEIN;

CELL PROLIFERATION; CHEMICAL STRUCTURE; CHEMISTRY; CONFERENCE PAPER; ENZYME STABILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; NEAR INFRARED SPECTROSCOPY; PHOTOSYNTHESIS; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN TERTIARY STRUCTURE; PROTEOBACTERIA; TEMPERATURE;

CELL PROLIFERATION; ENZYME STABILITY; MEMBRANE PROTEINS; MODELS, MOLECULAR; MUTATION; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN STRUCTURE, TERTIARY; PROTEOBACTERIA; SPECTROSCOPY, NEAR-INFRARED; TEMPERATURE;

BACTERIA (MICROORGANISMS); BLASTOCHLORIS VIRIDIS; PHOTOBACTERIA; PROTEOBACTERIA; RHODOBACTER SPHAEROIDES; THERMOCHROMATIUM TEPIDUM;

EID: 25444501222     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-005-4047-x     Document Type: Conference Paper

References (101)

1. JP Allen G Feher TO Yeates H Komiya DC Rees 1987 Structure of the reaction center from Rhodobacter sphaeroides R-26 - the cofactors Proc Natl Acad Sci USA 84 5730 5734
2. S Bahatyrova RN Frese CA Siebert JD Olsen KO van der Werf R van Grondelle RA Niederman PA Bullough C Otto CN Hunter 2004a The native architecture of a photosynthetic membrane Nature 430 1058 1062
3. S Bahatyrova RN Frese KO van der Werf C Otto CN Hunter JD Olsen 2004b 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
4. A Bairoch R Apweiler 2000 The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000 Nucl Acids Res 28 45 48
5. DA Benson I Karsch-Mizrachi DJ Lipman J Ostell DL Wheeler 2003 GenBank Nucl Acids Res 31 23 27
6. MG Bertero RA Rothery M Palak C Hou D Lim F Blasco JH Weiner NC Strynadka 2003 Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A Nat Struct Biol 10 681 687
7. JU Bowie 2001 Stabilizing membrane proteins Curr Opin Struct Biol 11 397 402
8. A Camara-Artigas D Brune JP Allen 2002 Interactions between lipids and bacterial reaction centres determined by protein crystallography Proc Natl Acad Sci USA 99 11055 11060
9. CH Chang O El Kabbani D Tiede J Norris M Schiffer 1991 Structure of the membrane-bound protein photosynthetic reaction center from Rhodobacter sphaeroides Biochemistry 30 5352 5360
10. Collaborative Computational Project, Number 4 (1994) Acta Crystallogr D 50, pp 760-763.
11. MJ Conroy WHJ Westerhuis PS Parkes-Loach PA Loach CN Hunter MP Williamson 2000 The solution structure of Rhodobacter sphaeroides LH1 beta reveals two helical domains separated by a more flexible region: structural consequences for the LH1 complex J Mol Biol 298 83 94
12. J Deisenhofer O Epp K Miki R Huber H Michel 1985 Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3 Angstrom resolution Nature 318 618 624
13. J Deisenhofer O Epp I Sinning H Michel 1995 Crystallographic refinement at 2,3-angstrom resolution and refined model of the photosynthetic reaction-center from Rhodopseudomonas viridis J Mol Biol 246 429 457
14. DC Demirjian F Morís-Varas CS Cassidy 2001 Enzymes from extremophiles Curr Opin Chem Biol 5 144 151
15. H Engelhardt A Engel W Baumeister 1986 Stoichiometric model of the photosynthetic unit of Ectothiorhodospira halochloris Proc Natl Acad Sci USA 83 8972 8976
16. U Ermler G Fritzsch SK Buchanan H Michel 1994a Structure of the photosynthetic reaction-center from Rhodobacter sphaeroides at 2.65-angstrom resolution - cofactors and protein-cofactor interactions Structure 2 925 936
17. U Ermler H Michel M Schiffer 1994b Structure and function of the photosynthetic reaction center from Rhodobacter sphaeroides J Bioenerg Biomemb 26 5 15
18. I Fathir M Ashikaga K Tanaka T Katano T Nirasawa M Kobayashi ZY Wang T Nozawa 1998 Biochemical and spectral characterization of the core light harvesting complex 1 (LH1) from the thermophilic purple sulfur bacterium Chromatium tepidum Photosynth Res 58 193 202
19. I Fathir T Mori T Nogi M Kobayashi K Miki T Nozawa 2001 Structure of the H subunit of the photosynthetic reaction center from the thermophilic purple sulfur bacterium, Thermochromatium tepidum - implications for the specific binding of the lipid molecule to the membrane protein complex Eur J Biochem 268 2652 2657
20. R Feick JA Shiozawa A Erltmaier 1995 Biochemical and spectroscopic properties of the reaction center from the green filamentous bacterium Chloroflexus aurantiacus RE Blankenship MT Madigan C Bauer Anoxygenic Photosynthetic Bacteria Kluwer Academic Publishers Dordrecht, The Netherlands 699 708
21. D Fotiadis P Qian A Philippsen PA Bullough A Engel CN Hunter 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
22. PK Fyfe KE McAuley AW Roszak NW Isaacs RJ Cogdell MR Jones 2001 Probing the interface between membrane proteins and membrane lipids by X-ray crystallography Trends Biochem Sci 26 106 112
23. D Garcia P Parot A Vermeglio MT Madigan 1986 The light-harvesting complexes of a thermophilic purple sulfur photosynthetic bacterium Chromatium-tepidum Biochim Biophys Acta 850 390 395
24. A Harrenga H Michel 1999 The cytochrome c oxidase from Paracoccus denitrificans does not change the metal center ligation upon reduction J Biol Chem 274 33296 33299
25. GD Heda MT Madigan 1988 Thermal-properties and oxygenase activity of ribulose-1,5-bisphosphate carboxylase from the thermophilic purple bacterium, Chromatium-tepidum FEMS Micro Letts 51 45 50
26. GD Heda MT Madigan 1989 Purification and characterization of the thermostable ribulose-1,5-bisphosphate carboxylase oxygenase from the thermophilic purple bacterium Chromatium-tepidum Eur J Biochem 184 313 319
27. BA Heller D Holten C Kirmaier 1995 Control of electron-transfer between the L-side and M-side of photosynthetic reaction centers Science 269 940 945
28. X Hu K Schulten 1998 Model for the light-harvesting complex I (B875) of Rhodobacter sphaeroides Biophysical J 75 683 694
29. X Hu A Damjanović T Ritz K Schulten 1998 Architecture and mechanism of the light-harvesting apparatus of purple bacteria Proc Natl Acad Sci USA 95 5935 5941
30. I Ikeda-Yamasaki T Odahara K Mitsuoka Y Fujiyoshi K Murata 1998 Projection map of the reaction center-light harvesting 1 complex from Rhodopseudomonas viridis at 10 angstrom resolution FEBS Letts 425 505 508
31. JF Imhoff U Bias-Imhoff 1995 Lipids, quinones and fatty acids of anoxygenic phototrophic bacteria RE Blankenship MT Madigan C Bauer Anoxygenic Photosynthetic Bacteria Kluwer Academic Publishers Dordrecht, The Netherlands 179 205
32. JF Imhoff DJ Kushner SC Kushwaha M Kates 1982 Polar lipids in phototropic bacteria of the Rhodospirillaceae and Chromatiaceae families J Bact 150 1192 1201
33. JF Imhoff J Suling R Petri 1998 Phylogenetic relationships among the Chromatiaceae, their taxonomic reclassification and description of the new genera Allochromatium, Halochromatium, Isochromatium, Marichromatium, Thiococcus, Thiohalocapsa and Thermochromatium Int J Sys Bact 48 1129 1143
34. R Jaenicke G Bohm 1998 The stability of proteins in extreme environments Curr Opin Struct Biol 8 738 748
35. SJ Jamieson PY Wang P Qian JY Kirkland MJ Conroy CN Hunter PA Bullough 2002 Projection structure of the photosynthetic reaction centre-antenna complex of Rhodospirillum rubrum at 8.5 angstrom resolution EMBO J 21 3927 3935
36. MR Jones GJS Fowler LCD Gibson GG Grief JD Olsen W Crielaard CN Hunter 1992a Construction of 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
37. MR Jones RW Visschers R van Grondelle CN Hunter 1992b Construction and characterisation of a mutant of Rhodobacter sphaeroides with the reaction centre as the sole pigment-protein complex Biochemistry 31 4458 4465
38. MR Jones M Heer-Dawson TA Mattioli CN Hunter B Robert 1994 Site-specific mutagenesis of the reaction centre from Rhodobacter sphaeroides studied by Fourier transform Raman spectroscopy: mutations at tyrosine M210 do not affect the electronic structure of the primary donor FEBS Letts 339 18 24
39. P Jordan P Fromme HT Witt O Klukas W Saenger N Krauss 2001 Three-dimensional structure of cyanobacterial photosystem I at 2.5Å resolution Nature 411 909 917
40. M Jormakka S Tornroth B Byrne S Iwata 2002 Molecular basis of proton motive force generation: structure of formate dehydrogenase-N Science 295 1863 1868
41. C Jungas JL Ranck JL Rigaud P Joliot A Verméglio 1999 Supramolecular organization of the photosynthetic apparatus of Rhodobacter sphaeroides EMBO J 18 534 542
42. S Karrasch PA Bullough R Ghosh 1995 The 8.5 Å projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits EMBO J 14 631 638
43. G Katona U Andreasson EM Landau LE Andreasson R Neutze 2003 Lipidic cubic phase crystal structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2.35Å resolution J Mol Biol 331 681 692
44. C Kirmaier D Gaul R Debey D Holten CC Schenck 1991 Charge separation in a reaction center incorporating bacteriochlorophyll for photoactive bacteriopheophytin Science 251 922 927
45. 6f complex of oxygenic photosynthesis: tuning the cavity Science 302 1009 1014
46. 1 complex structure EMBO J 20 6591 6600
47. AG Lee 2003 Lipid-protein interactions in biological membranes: a structural perspective Biochim Biophys Acta 1612 1 40
48. B Lee G Vasmatzis 1997 Stabilization of protein structures Curr Opin Biotechnol 8 423 428
49. Z Liu H Yan K Wang T Kuang J Zhang L Gui X An W Chang 2004 Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution Nature 428 287 292
50. H Luecke B Schobert H-T Richter J-P Cartailler JK Lanyi 1999 Structure of bacteriorhodopsin at 1.55 angstrom resolution J Mol Biol 291 899 911
51. MT Madigan 1984 A novel photosynthetic purple bacterium isolated from a Yellowstone hot spring Science 225 314 316
52. MT Madigan 1986 Chromatium-tepidum sp-nov, a thermophilic photosynthetic bacterium of the family Chromatiaceae Int J Syst Bact 36 222 227
53. KE McAuley-Hecht PK Fyfe JP Ridge SM Prince CN Hunter NW Isaacs RJ Cogdell MR Jones 1998 Structural studies of wild type and mutant reaction centres from an antenna-deficient strain of Rhodobacter sphaeroides: monitoring the optical properties of the complex from cell to crystal Biochemistry 37 4740 4750
54. KE McAuley PK Fyfe JP Ridge NW Isaacs RJ Cogdell MR Jones 1999 Structural details of an interaction between cardiolipin and an integral membrane protein Proc Natl Acad Sci USA 96 14706 14711
55. KE McAuley PK Fyfe JP Ridge RJ Cogdell NW Isaacs MR Jones 2000 Ubiquinone binding, ubiquinone exclusion, and detailed cofactor conformation in a mutant bacterial reaction center Biochemistry 39 15032 15043
56. RN McElhaney 1989 The influence of membrane lipid-composition and physical-properties of membrane-structure and function in Acholeplasma-laidlawii Crit Rev Microbiol 17 1 32
57. P McGlynn CN Hunter MR Jones 1994 The Rhodobacter sphaeroides PufX protein is not required for photosynthetic competence in the absence of a light harvesting system FEBS Letts 349 349 353
58. KVP Nagashima K Matsuura N Wakao A Hiraishi K Shimada 1997 Nucleotide sequences of genes coding for photosynthetic reaction centers and light-harvesting proteins of Acidiphilium rubrum and related aerobic acidophilic bacteria Plant Cell Physiol 38 1249 1258
59. T Nogi I Fathir M Kobayashi T Nozawa K Miki 2000 Crystal structures of photosynthetic reaction centre and high-potential iron-sulfur protein from Thermochromatium tepidum: Thermostability and electron transfer Proc Natl Acad Sci USA 97 13561 13566
60. T Nozawa MT Madigan 1991 Temperature and solvent effects on reaction centers from Chloroflexus aurantiacus and Chromatium tepidum J Biochem 110 588 594
61. T Nozawa T Fukada M Hatano MT Madigan 1986 Organization of intracytoplasmic membranes in a novel thermophilic purple photosynthetic bacterium as revealed by absorption, circular-dichroism and emission-spectra Biochim Biophys Acta 852 191 197
62. T Nozawa JT Trost T Fukada M Hatano JD McManus RE Blankenship 1987 Properties of the reaction center of the thermophilic purple photosynthetic bacterium Chromatium tepidum Biochim Biophys Acta 894 468 476
63. JD Olsen GD Sockalingum B Robert CN Hunter 1994 Modification of a hydrogen-bond to a bacteriochlorophyll-a molecule in the light-harvesting 1-antenna of Rhodobacter-sphaeroides Proc Natl Acad Sci USA 91 7124 7128
64. o site inhibitor bound J Biol Chem 278 31303 31311
65. MZ Papiz SM Prince AM Hawthornthwaite-Lawless G McDermott AA Freer NW Isaacs RJ Cogdell 1996 A model for the photosynthetic apparatus of purple bacteria Trends Plant Sci 1 198 206
66. MZ Papiz SM Prince T Howard RJ Cogdell NW Isaacs 2003 The structure and thermal motion of the B800-850 LH2 complex from Rps. acidophila at 2.0 Å resolution and 100 K: new structural features and functionally relevant motions J Mol Biol 326 1523 1538
67. E Pebay-Peyroula C Dahout-Gonzalez R Kahn V Trezeguet GJ Lauquin G Brandolin 2003 Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside Nature 426 39 44
68. BK Pierson JP Thornber REB Seftor 1983 Partial purification, subunit structure and thermal stability of the photochemical reaction center of the thermophilic green bacterium Chloroflexus aurantiacus Biochim Biophys Acta 723 322 326
69. P Qian HA Addlesee AV Ruban PY Wang PA Bullough CN Hunter 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
70. Ridge JP (1998) PhD thesis, University of Sheffield
71. A ubiquinone and carotenoid in the reaction center from Rhodobacter sphaeroides Photosynth Res 59 9 26
72. AW Roszak TD Howard J Southall AT Gardiner CJ Law NW Isaacs RJ Cogdell 2003 Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris Science 302 1969 1972
73. NJ Russell 1984 Mechanisms of thermal adaptation in bacteria - blueprints for survival Trends Biochem Sci 9 108 112
74. NJ Russell N Fukunaga 1990 A comparison of thermal adaptation of membrane-lipids in psychrophilic and thermophilic bacteria FEMS Microbiol Rev 75 171 182
75. JM Sanchez-Ruiz GI Makhatadze 2001 To charge or not to charge? Trends Biotechnol 19 132 135
76. S Scheuring J Seguin S Marco D Levy B Robert JL Rigaud 2003 Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM Proc Natl Acad Sci USA 100 1690 1693
77. S Scheuring JN Sturgis V Prima A Bernadac D Levy JL Rigaud 2004a Watching the photosynthetic apparatus in native membranes Proc Natl Acad Sci USA 101 11293 11297
78. S Scheuring F Francia J Busselez BA Melandri J-L Rigaud D Lévy 2004b Structural role of PufX in the dimerization of the photosynthetic core complex of Rhodobacter sphaeroides J Biol Chem 279 3620 3626
79. S Scheuring J-L Rigaud JN Sturgis 2004c Variable LH2 stoichiometry and core clustering in native membranes of Rhodospirillum photometricum EMBO J 23 4127 4133
80. CA Siebert P Qian D Fotiadis A Engel CN Hunter PA Bullough 2004 Molecular architecture of photosynthetic membranes in Rhodobacter sphaeroides: the role of PufX EMBO J 23 690 700
81. M Sinensky 1974 Homeoviscous adaptation - a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli Proc Natl Acad Sci USA 71 522 525
82. H Stahlberg J Dubochet H Vogel R Ghosh 1998 Are the light-harvesting I complexes from Rhodospirillum rubrum arranged around the reaction centre in a square geometry? J Mol Biol 282 819 831
83. S Steiner SF Conti RL Lester 1969 Separation and identification of the polar lipids of Chromatium Strain D J Bacteriol 98 10 15
84. D Stroebel Y Choquet JL Popot D Picot 2003 An atypical haem in the cytochrome b(6)f complex Nature 426 413 418
85. JN Sturgis JD Olsen B Robert CN Hunter 1997 Functions of conserved tryptophan residues of the core light-harvesting complex of Rhodobacter sphaeroides Biochemistry 36 2772 2778
86. Suutari M and Laakso S (1994) Microbial fatty-acids and thermal adaptation. Crit Rev Microbiol: 285-328
87. A Szilágyi P Závodszky 2000 Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey Structure 8 493 504
88. JD Thompson DG Higgins TJ Gibson 1994 Clustal-W - improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucl Acids Res 22 4673 4680
89. B Tolner B Poolman WN Konings 1997 Adaptation of microorganisms and their transport systems to high temperatures Comp Biochem Physiol A 118 423 428
90. C Vieille GJ Zeikus 2001 Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability Microbiol Mol Biol Rev 65 1 43
91. G von Heijne 1992 Membrane protein structure prediction: hydrophobicity analysis and the positive-inside rule J Mol Biol 225 487 494
92. MC Wakeham MR Jones RB Sessions PK Fyfe 2001 Is there a conserved interaction between cardiolipin and the Type II bacterial reaction center? Biophys J 80 1395 1405
93. T Walz SJ Jamieson CM Bowers PA Bullough CN Hunter 1998 Projection structures of three photosynthetic complexes from Rhodobacter sphaeroides: LH2 at 6 angstrom LH1 and RC-LH1 at 25 angstrom J Mol Biol 282 833 845
94. ZY Wang M Shimonaga M Kobayashi T Nozawa 2002 N-terminal methylation of the core light-harvesting complex in purple photosynthetic bacteria FEBS Lett 519 164 168
95. Z-Y Wang M Shimonga M Kobayashi T Nozawa 2003 Purification and characterization of the polypeptides of core light-harvesting complexes from purple sulfur bacteria Photosynth Res 78 133 141
96. V Yankovskaya R Horsefield S Tornroth C Luna-Chavez H Miyoshi C Leger B Byrne G Cecchini S Iwata 2003 Architecture of succinate dehydrogenase and reactive oxygen species generation Science 299 700 704
97. JK Yano TL Poulos 2003 New understandings of thermostable and peizostable enzymes Curr Opin Biotech 14 360 365
98. TO Yeates H Komiya DC Rees JP Allen G Feher 1987 Structure of the reaction center from Rhodobacter-sphaeroides R-26 - membrane-protein interactions Proc Natl Acad Sci USA 84 6438 6442
99. 1 Nature 392 677 684
100. Y Zhou JU Bowie 2000 Building a thermostable membrane protein J Biol Chem 275 6975 6979
101. H Zuber RJ Cogdell 1995 Structure and organiszation of purple bacterial antenna complexes RE Blankenship MT Madigan C Bauer Anoxygenic Photosynthetic Bacteria Kluwer Academic Publishers Dordrecht, The Netherlands 315 348