Crystal structure of a RuBisCO-like protein from the green sulfur bacterium Chlorobium tepidum

Structure

Volumn 13, Issue 5, 2005, Pages 779-789

  Li, Huiying ^a   Sawaya, Michael R ^a   Tabita, F Robert ^b   Eisenberg, David ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; RIBULOSEBISPHOSPHATE CARBOXYLASE; RIBULOSEBISPHOSPHATE CARBOXYLASE LIKE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; BIOSYNTHESIS; CARBOXYLATION; CATALYSIS; CHLOROBI; CHLOROBIUM TEPIDUM; CONTROLLED STUDY; CRYSTAL STRUCTURE; NONHUMAN; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; CHLOROBIUM; CRYSTALLOGRAPHY, X-RAY; ELECTROSTATICS; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; RIBULOSE-BISPHOSPHATE CARBOXYLASE;

BACTERIA (MICROORGANISMS); CHLOROBACULUM TEPIDUM; CHLOROBIUM;

EID: 18944389308     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2005.02.017     Document Type: Article

References (68)

1. I. Andersson Large structures at high resolution: the 1.6 A crystal structure of spinach ribulose-1,5-bisphosphate carboxylase/oxygenase complexed with 2-carboxyarabinitol bisphosphate J. Mol. Biol. 259 1996 160 174
2. I. Andersson, and T.C. Taylor Structural framework for catalysis and regulation in ribulose-1,5-bisphosphate carboxylase/oxygenase Arch. Biochem. Biophys. 414 2003 130 140
3. H. Ashida, Y. Saito, C. Kojima, K. Kobayashi, N. Ogasawara, and A. Yokota A functional link between RuBisCO-like protein of Bacillus and photosynthetic RuBisCO Science 302 2003 286 290
4. T.S. Baker, D. Eisenberg, and F. Eiserling Ribulose bisphosphate carboxylase: a two-layered, square-shaped molecule of symmetry 422 Science 196 1977 293 295
5. P.M. Bowers, M. Pellegrini, M.J. Thompson, J. Fierro, T.O. Yeates, and D. Eisenberg Prolinks: a database of protein functional linkages derived from coevolution Genome Biol. 5 2004 R35
6. A.T. Brunger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszewski, M. Nilges, and N.S. Pannu Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54 1998 905 921
7. M.S. Chapman, S.W. Suh, D. Cascio, W.W. Smith, and D. Eisenberg Sliding-layer conformational change limited by the quaternary structure of plant RuBisCO Nature 329 1987 354 356
8. W.W. Cleland, T.J. Andrews, S. Gutteridge, F.C. Hartman, and G.H. Lorimer Mechanism of RuBisCO: the carbamate as general base Chem. Rev. 98 1998 549 562
9. CCP4 (Collaborative Computational Project, Number 4) The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
10. C. Colovos, and T.O. Yeates Verification of protein structures: patterns of nonbonded atomic interactions Protein Sci. 2 1993 1511 1519
11. P.M. Curmi, D. Cascio, R.M. Sweet, D. Eisenberg, and H. Schreuder Crystal structure of the unactivated form of ribulose-1,5-bisphosphate carboxylase/oxygenase from tobacco refined at 2.0-Å resolution J. Biol. Chem. 267 1992 16980 16989
12. T. Dandekar, B. Snel, M. Huynen, and P. Bork Conservation of gene order: A fingerprint of proteins that physically interact Trends Biochem. Sci. 23 1998 324 328
13. DeLano, W.L. (2002). The PyMOL Molecular Graphics System (http://www.pymol.org).
14. A.P. Duff, T.J. Andrews, and P.M. Curmi The transition between the open and closed states of RuBisCO is triggered by the inter-phosphate distance of the bound bisphosphate J. Mol. Biol. 298 2000 903 916
15. J.A. Eisen, K.E. Nelson, I.T. Paulsen, J.F. Heidelberg, M. Wu, R.J. Dodson, R. Deboy, M.L. Gwinn, W.C. Nelson, and D.H. Haft The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium Proc. Natl. Acad. Sci. USA 99 2002 9509 9514
16. D. Eisenberg, and A.D. McLachlan Solvation energy in protein folding and binding Nature 319 1986 199 203
17. R.J. Ellis The most abundant protein in the world Trends Biochem. Sci. 4 1979 241 244
18. A.J. Enright, I. Iliopoulos, N.C. Kyrpides, and C.A. Ouzounis Protein interaction maps for complete genomes based on gene fusion events Nature 402 1999 86 90
19. M.W. Finn, and F.R. Tabita Synthesis of catalytically active form III ribulose 1,5-bisphosphate carboxylase/oxygenase in archaea J. Bacteriol. 185 2003 3049 3059
20. N.U. Frigaard, and D.A. Bryant Seeing green bacteria in a new light: genomics-enabled studies of the photosynthetic apparatus in green sulfur bacteria and filamentous anoxygenic phototrophic bacteria Arch. Microbiol. 182 2004 265 276
21. S. Hansen, V.B. Vollan, E. Hough, and K. Andersen The crystal structure of RuBisCO from Alcaligenes eutrophus reveals a novel central eight-stranded beta-barrel formed by beta-strands from four subunits J. Mol. Biol. 288 1999 609 621
22. T.E. Hanson, and F.R. Tabita A ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO)-like protein from Chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress Proc. Natl. Acad. Sci. USA 98 2001 4397 4402
23. T.E. Hanson, and F.R. Tabita Insights into the stress response and sulfur metabolism revealed by proteome analysis of a Chlorobium tepidum mutant lacking the RuBisCO-like protein Photosynth. Res. 78 2003 231 248
24. R.W. Hooft, G. Vriend, C. Sander, and E.E. Abola Errors in protein structures Nature 381 1996 272
25. T.A. Jones, J.Y. Zou, S.W. Cowan, and M. Kjeldgaard Improved methods for building protein models in electron density maps and the location of errors in these models Acta Crystallogr. A 47 1991 110 119
26. C.R. Kissinger, D.K. Gehlhaar, and D.B. Fogel Rapid automated molecular replacement by evolutionary search Acta Crystallogr. D Biol. Crystallogr. 55 1999 484 491
27. K. Kitano, N. Maeda, T. Fukui, H. Atomi, T. Imanaka, and K. Miki Crystal structure of a novel-type archaeal rubisco with pentagonal symmetry Structure (Camb) 9 2001 473 481
28. H.P. Klenk, R.A. Clayton, J.F. Tomb, O. White, K.E. Nelson, K.A. Ketchum, R.J. Dodson, M. Gwinn, E.K. Hickey, and J.D. Peterson The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus Nature 390 1997 364 370
29. S. Knight, I. Andersson, and C.I. Branden Crystallographic analysis of ribulose 1,5-bisphosphate carboxylase from spinach at 2.4 Å resolution: subunit interactions and active site J. Mol. Biol. 215 1990 113 160
30. F. Kunst, N. Ogasawara, I. Moszer, A.M. Albertini, G. Alloni, V. Azevedo, M.G. Bertero, P. Bessieres, A. Bolotin, and S. Borchert The complete genome sequence of the gram-positive bacterium Bacillus subtilis Nature 390 1997 249 256
31. F.W. Larimer, P. Chain, L. Hauser, J. Lamerdin, S. Malfatti, L. Do, M.L. Land, D.A. Pelletier, J.T. Beatty, and A.S. Lang Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris Nat. Biotechnol. 22 2004 55 61
32. G. Lu TOP: a new method for protein structure comparisons and similarity searches J. Appl. Crystallogr. 33 2000 176 183
33. T. Lundqvist, and G. Schneider Crystal structure of the binary complex of ribulose-1,5-bisphosphate carboxylase and its product, 3-phospho-D-glycerate J. Biol. Chem. 264 1989 3643 3646
34. T. Lundqvist, and G. Schneider Crystal structure of the complex of ribulose-1,5-bisphosphate carboxylase and a transition state analogue, 2-carboxy-D-arabinitol 1,5-bisphosphate J. Biol. Chem. 264 1989 7078 7083
35. T. Lundqvist, and G. Schneider Crystal structure of activated ribulose-1,5-bisphosphate carboxylase complexed with its substrate, ribulose-1,5-bisphosphate J. Biol. Chem. 266 1991 12604 12611
36. T. Lundqvist, and G. Schneider Crystal structure of the ternary complex of ribulose-1,5-bisphosphate carboxylase, Mg(II), and activator CO2 at 2.3-Å resolution Biochemistry 30 1991 904 908
37. N. Maeda, K. Kitano, T. Fukui, S. Ezaki, H. Atomi, K. Miki, and T. Imanaka Ribulose bisphosphate carboxylase/oxygenase from the hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1 is composed solely of large subunits and forms a pentagonal structure J. Mol. Biol. 293 1999 57 66
38. E.M. Marcotte, M. Pellegrini, H.L. Ng, D.W. Rice, T.O. Yeates, and D. Eisenberg Detecting protein function and protein-protein interactions from genome sequences Science 285 1999 751 753
39. A.L. Morris, M.W. MacArthur, E.G. Hutchinson, and J.M. Thornton Stereochemical quality of protein structure coordinates Proteins 12 1992 345 364
40. B.A. Murphy, F.J. Grundy, and T.M. Henkin Prediction of gene function in methylthioadenosine recycling from regulatory signals J. Bacteriol. 184 2002 2314 2318
41. C.M. Ott, B.D. Smith, A.R. Portis Jr., and R.J. Spreitzer Activase region on chloroplast ribulose-1,5-bisphosphate carboxylase/oxygenase: nonconservative substitution in the large subunit alters species specificity of protein interaction J. Biol. Chem. 275 2000 26241 26244
42. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
43. R. Overbeek, M. Fonstein, M. D'Souza, G.D. Pusch, and N. Maltsev The use of gene clusters to infer functional coupling Proc. Natl. Acad. Sci. USA 96 1999 2896 2901
44. M. Pellegrini, E.M. Marcotte, M.J. Thompson, D. Eisenberg, and T.O. Yeates Assigning protein functions by comparative genome analysis: protein phylogenetic profiles Proc. Natl. Acad. Sci. USA 96 1999 4285 4288
45. M. Pellegrini, M. Thompson, J. Fierro, and P. Bowers Computational method to assign microbial genes to pathways J. Cell. Biochem. Suppl. 2001 106 109
46. J. Pontius, J. Richelle, and S.J. Wodak Deviations from standard atomic volumes as a quality measure for protein crystal structures J. Mol. Biol. 264 1996 121 136
47. G.N. Ramachandran, and V. Sasisekharan Conformation of polypeptides and proteins Adv. Protein Chem. 23 1968 283 438
48. G. Schneider, Y. Lindqvist, and C.I. Branden RuBisCO: structure and mechanism Annu. Rev. Biophys. Biomol. Struct. 21 1992 119 143
49. G. Schneider, Y. Lindqvist, and T. Lundqvist Crystallographic refinement and structure of ribulose-1,5-bisphosphate carboxylase from Rhodospirillum rubrum at 1.7 Å resolution J. Mol. Biol. 211 1990 989 1008
50. H.A. Schreuder, S. Knight, P.M. Curmi, I. Andersson, D. Cascio, C.I. Branden, and D. Eisenberg Formation of the active site of ribulose-1,5- bisphosphate carboxylase/oxygenase by a disorder-order transition from the unactivated to the activated form Proc. Natl. Acad. Sci. USA 90 1993 9968 9972
51. H.A. Schreuder, S. Knight, P.M. Curmi, I. Andersson, D. Cascio, R.M. Sweet, C.I. Branden, and D. Eisenberg Crystal structure of activated tobacco RuBisCO complexed with the reaction-intermediate analogue 2-carboxy-arabinitol 1,5-bisphosphate Protein Sci. 2 1993 1136 1146
52. A. Sekowska, and A. Danchin The methionine salvage pathway in Bacillus subtilis BMC Microbiol. 2 2002 8
53. N. Shibata, T. Inoue, K. Fukuhara, Y. Nagara, R. Kitagawa, S. Harada, N. Kasai, K. Uemura, K. Kato, A. Yokota, and Y. Kai Orderly disposition of heterogeneous small subunits in D-ribulose-1,5-bisphosphate carboxylase/ oxygenase from spinach J. Biol. Chem. 271 1996 26449 26452
54. D. Sitkoff, D.J. Lockhart, K.A. Sharp, and B. Honig Calculation of electrostatic effects at the amino terminus of an alpha helix Biophys. J. 67 1994 2251 2260
55. E. Soderlind, G. Schneider, and S. Gutteridge Substitution of ASP193 to ASN at the active site of ribulose-1,5-bisphosphate carboxylase results in conformational changes Eur. J. Biochem. 206 1992 729 735
56. T.S. Soper, R.J. Mural, F.W. Larimer, E.H. Lee, R. Machanoff, and F.C. Hartman Essentiality of Lys-329 of ribulose-1,5-bisphosphate carboxylase/oxygenase from Rhodospirillum rubrum as demonstrated by site-directed mutagenesis Protein Eng. 2 1988 39 44
57. R.J. Spreitzer, and M.E. Salvucci RuBisCO: structure, regulatory interactions, and possibilities for a better enzyme Annu. Rev. Plant Biol. 53 2002 449 475
58. H. Sugawara, H. Yamamoto, N. Shibata, T. Inoue, S. Okada, C. Miyake, A. Yokota, and Y. Kai Crystal structure of carboxylase reaction-oriented ribulose 1,5-bisphosphate carboxylase/oxygenase from a thermophilic red alga, Galdieria partita J. Biol. Chem. 274 1999 15655 15661
59. F.R. Tabita Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: A different perspective Photosynth. Res. 60 1999 1 28
60. T.C. Taylor, and I. Andersson Structural transitions during activation and ligand binding in hexadecameric RuBisCO inferred from the crystal structure of the activated unliganded spinach enzyme Nat. Struct. Biol. 3 1996 95 101
61. T.C. Taylor, and I. Andersson Structure of a product complex of spinach ribulose-1,5-bisphosphate carboxylase/oxygenase Biochemistry 36 1997 4041 4046
62. T.C. Taylor, and I. Andersson The structure of the complex between RuBisCO and its natural substrate ribulose 1,5-bisphosphate J. Mol. Biol. 265 1997 432 444
63. T.C. Taylor, A. Backlund, K. Bjorhall, R.J. Spreitzer, and I. Andersson First crystal structure of RuBisCO from a green alga, Chlamydomonas reinhardtii J. Biol. Chem. 276 2001 48159 48164
64. T.C. Taylor, M.D. Fothergill, and I. Andersson A common structural basis for the inhibition of ribulose 1,5-bisphosphate carboxylase by 4-carboxyarabinitol 1,5-bisphosphate and xylulose 1,5-bisphosphate J. Biol. Chem. 271 1996 32894 32899
65. A.C. Wallace, R.A. Laskowski, and J.M. Thornton LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions Protein Eng. 8 1995 127 134
66. G.M. Watson, J.P. Yu, and F.R. Tabita Unusual ribulose 1,5-bisphosphate carboxylase/oxygenase of anoxic Archaea J. Bacteriol. 181 1999 1569 1575
67. K.Y. Zhang, D. Cascio, and D. Eisenberg Crystal structure of the unactivated ribulose 1,5-bisphosphate carboxylase/oxygenase complexed with a transition state analog, 2-carboxy-D-arabinitol 1,5-bisphosphate Protein Sci. 3 1994 64 69
68. Z. Zhang, M. Lindstam, J. Unge, C. Peterson, and G. Lu Potential for dramatic improvement in sequence alignment against structures of remote homologous proteins by extracting structural information from multiple structure alignment J. Mol. Biol. 332 2003 127 142