A common ancestor for oxygenic and anoxygenic photosynthetic systems: A comparison based on the structural model of photosystem I

Journal of Molecular Biology

Volumn 280, Issue 2, 1998, Pages 297-314

  Schubert, Wolf Dieter ^a   Klukas, Olaf ^a   Saenger, Wolfram ^a   Witt, Horst Tobias ^b   Fromme, Petra ^b   Krauß, Norbert ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Green sulfur bacteria; Heliobacteria; Photosynthetic reaction centers; Photosystem I and photosystem II; Purple bacteria

Indexed keywords

ALPHA HELIX; ARTICLE; CHLOROBIUM; COMPARATIVE STUDY; ELECTRON TRANSPORT; GENETIC CONSERVATION; MODEL; NONHUMAN; PHOTOSYNTHESIS; PHOTOSYSTEM I; PHOTOSYSTEM II; PRIORITY JOURNAL;

EID: 0032504023     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.1824     Document Type: Article

References (82)

1. 533. Biochemistry. 36:1997;1927-1932
2. Alfonso M., Montoya G., Cases R., Roriguez R., Picorel R. Core antenna complexes, CP43 and CP47 of higher plant photosystem II. Spectral properties, pigment stoichiometry and amino acid composition. Biochemistry. 33:1994;10494-10500
3. Allen J.P., Feher G., Yeates T.O., Rees D.C., Deisenhofer J., Michel H., Huber R. Structural homology of reaction centers from Rhodopseudomonas sphaeroides and Rhodopseudomonas viridis as determined by X-ray diffraction. Proc. Natl Acad. Sci. USA. 83:1986;8589-8593
4. Arlt A., Schmidt S., Kaiser W., Lauterwasser C., Meyer M., Scheer H., Zinth W. The accessory bacteriochlorophyll a real electron carrier in primary photosynthesis. Proc. Natl Acad. Sci. USA. 90:1993;11757-11761
5. Arnoux B., Ducruix A., Reiss-Husson F., Lutz M., Norris J., Schiffer M., Chang C.H. Structure of spheroidene in the photosynthetic reaction center from Rhodobacter sphaeroides Y. FEBS Letters. 258:1989;47-50
6. Arnoux B., Gaucher J.-F., Ducruix A., Reiss-Husson F. Structure of the photochemical centre of a spheroidene-containing purple bacterium, Rhodobacter sphaeroides Y, at 3 Å resolution. Acta Crystallog. sect. D. 51:1995;368-379
7. Barber J. Similarities and differences between photosystem II and the purple bacterial reaction centers. Stevens S.E., Bryant D.A. Light-energy transduction in Photosynthesis: Higher Plant and Bacterial Models. 1988;178-196 The American Society of Plant Physiologists, Rockville, ML
8. Beanland T.J. Evolutionary relationships between 'Q-type' photosynthetic reaction centres Hypothesis testing using parsimony. J. Theoret. Biol. 145:1990;535-545
9. 1 in photosystem I of the cyanobacterium Synechocystis 6803. Biochemistry. 27:1988;1494-1500
10. Bittl R., Zech S.G., Fromme P., Witt H.T., Lubitz W. Pulsed EPR structure analysis of photosystem I single crystals localization of the phylloquinone acceptor. Biochemistry. 36:1997;12001-12004
11. Blankenship R.E. Origin and early evolution of photosynthesis. Photosynth. Res. 33:1992;91-111
12. Brettel K. Electron transfer and arrangement of the redox cofactors in Photosystem I. Biochim. Biophys. Acta. 1318:1997;322-373
13. Bricker T.M. The structure and function of CPa-1 and CPa-2 in photosystem II. Photosynth. Res. 24:1990;1-13
14. Bryant D.A. Gene nomenclature recommendations for green photosynthetic bacteria and heliobacteria. Photosynth. Res. 41:1994;27-28
15. Buttner M., Xie D.-L., Nelson H., Pinther W., Hauska G., Nelson N. Photosynthetic reaction center genes in green sulfur bacteria and in photosystem 1 are related. Proc. Natl Acad. Sci. USA. 89:1992;8135-8139
16. Chang C.H., el-Kabbani O., Tiede D., Norris J., Schiffer M. Structure of the membrane-bound protein photosynthetic reaction center from Rhodobacter sphaeroides. Biochemistry. 30:1991;5352-5360
17. Deisenhofer J., Michel H. Three-dimensional structure of the photosynthetic reaction centre from Rhodopseudomonas viridis. Deisenhofer J., Norris J.R. The Photosynthetic Reaction Center. vol. 2:1993;541-558 Academic Press, London
18. Deisenhofer J., Epp O., Miki K., Huber R., Michel H. Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3 Å resolution. Nature. 318:1985;618-624
19. Deisenhofer J., Epp O., Sinning I., Michel H. Crystallographic refinement at 2. 3 Å resolution and refined model of the photosynthetic reaction centre from Rhodopseudomonas viridis. J. Mol. Biol. 246:1995;429-457
20. Diner B.A., Babcock G.T. Structure, dynamics, and energy conversion efficiency in photosystem II. Ort D.R., Yocum C.F. Oxygenic Photosynthesis: The Light Reactions. 1996;213-247 Kluwer, Dordrecht
21. Ermler U., Fritsch G., Buchanan S.K., Michel H. Structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2.65 Å resolution cofactors and protein-cofactor interactions. Structure. 2:1994;925-936
22. Feiler U., Hauska G. The reaction center from green sulfur bacteria. Blankenship R.E., Madigan M.T., Bauer C.E. Anoxygenic Photosynthetic Bacteria, Advances in Photosynthesis. vol. 2:1995;665-685 Kluwer, Dordrecht
23. Feiler U., Albouy D., Robert B., Mattioli T.A. Symmetric structural features and binding site of the primary electron donor in the reaction center of Chlorobium. Biochemistry. 34:1995;11099-11105
24. Fish L., Kuck U., Bogorad L. Two partially homologous adjacent light-inducible maize chloroplast genes encoding polypeptides of the P700 chlorophyll a-protein complex of Photosystem I. J. Biol. Chem. 260:1985;1413-1421
25. Fromme P., Schubert W.-D., Krauß N. Structure of photosystem I suggestions on the docking sites for plastocyanin, ferredoxin and the co-ordination of P700. Biochim. Biophys. Acta. 1187:1994;99-105
26. Fromme P., Witt H.T., Schubert W.-D., Klukas O., Saenger W., Krauß N. Structure of photosystem I at 4.5 Å resolution a short review including evolutionary aspects. Biochim. Biophys. Acta. 1275:1996;76-83
27. 559reaction centre complex of photosystem two isolated by two different methods. FEBS Letters. 265:1990;88-92
28. Hager-Braun C., Xie D.-L., Jarosch U., Herold E., Buttner M., Zimmermann R., Deutzmann R., Hauska G., Nelson N. Stable photobleaching of P840 in Chlorobium reaction center preparations presence of the 42-kDa bacteriochlorophyll a protein and a 17-kDa polypeptide. Biochemistry. 34:1995;9617-9624
29. Hager-Braun C., Jarosch U., Hauska G., Nitschke W., Riedel A. EPR studies of the terminal electron acceptors of the green sulfur bacterial reaction centre. Revisited. Photosynth. Res. 51:1997;127-136
30. Hauska G., Hager-Braun C., Schneebauer N., Schutz M., Zimmermann R., Nelson N. Biochemical aspects of the reaction center in green sulfur bacteria comparison with other FeS-types. Mathis P. Photosynthesis: from Light to Biosphere., Proc. 10th Int. Conf. Photosynth. vol. 2:1995;11-16 Kluwer, Dordrecht
31. 1between digitonin particles and chlorophyll-proteins of chloroplast membranes from Nicotiana tabacum. Z. Naturforsch. 36c:1981;276-283
32. 2/cytochrome b-559 reaction center complex from spinach. FEBS Letters. 260:1990;138-140
33. Krauß N., Hinrichs W., Witt I., Fromme P., Pritzkow W., Dauter Z., Betzel C., Wilson K.S., Witt H.T., Saenger W. Three-dimensional structure of system I of photosynthesis at 6 Å resolution. Nature. 361:1993;326-331
34. Krauß N., Schubert W.-D., Klukas O., Fromme P., Witt H.T., Saenger W. Photosystem I at 4 Å resolution represents the first structural model of a joint photosynthetic reaction center and core antenna system. Nature Struct. Biol. 3:1996;965-973
35. Kühlbrandt W., Wang D.N., Fujiyoshi Y. Atomic model of plant light-harvesting complex by electron crystallography. Nature. 367:1994;614-621
36. Kuhn M., Fromme P., Krabben L. A 'membrane attached' alpha-helix a conserved structural motif in bacterial reaction centres, photosystem I and chloroplast NADH-plastoquinone oxidoreductase. Trends Biochem. Sci. 19:1994;401-402
37. Lancaster R.C., Ermler U., Michel H. The structures of photosynthetic reaction centers from purple bacteria as revealed by X-ray crystallography. Blankenship R.E., Madigan M.T., Bauer C.E. Anoxygenic Photosynthetic Bacteria, Advances in Photosynthesis. vol. 2:1995;503-526 Kluwer, Dordrecht
38. Liebl U., Möckensturm-Wilson M., Trost J.T., Brune D.C., Blankenship R.E., Vermaas W. Single core polypeptide in the reaction center of the photosynthetic bacterium Heliobacillus mobilis structural implications and relations to other photosystems. Proc. Natl Acad. Sci. USA. 90:1993;7124-7128
39. B. FEBS Letters. 338:1994;197-202
40. +. Biochemistry. 35:1996;13288-13293
41. 1molecules in the PSI electron acceptor complex. FEBS Letters. 208:1986;343-346
42. Malkin R. Photosystem I electron transfer reactions components and kinetics. Ort D.R., Yocum C.F. Oxygenic Photosynthesis: The Light Reactions. 1996;313-332 Kluwer, Dordrecht
43. -mechanism in reaction centers of photosynthetic bacteria. Chem. Phys. Letters. 133:1987;471-477
44. Margulies M.M. Sequence similarity between photosystems I and II. Identification of a photosystem I reaction center transmembrane helix that is similar to transmembrane helix IV of the D2 subunit of photosystem II and the M subunit of the non-sulfur purple and flexible green bacteria. Photosynth. Res. 29:1991;133-147
45. Margulis L. Symbiosis in Cell Evolution. 1981;WH Freeman and Company, San Francisco
46. Margulis L. Archaeal-eubacterial mergers in the origin of Eukarya phylogenetic classification of life. Proc. Natl Acad. Sci. USA. 93:1996;1071-1076
47. Mathis P. Compared structure of plant and bacterial photosynthetic reaction centers. Evolutionary implications. Biochim. Biophys. Acta. 1018:1990;163-167
48. Michel H., Deisenhofer J. Relevance of the photosynthetic reaction center from purple bacteria to the structure of photosystem II. Biochemistry. 27:1988;1-7
49. Michel H., Weyer K.A., Gruenberg H., Dunger I., Oesterhelt D., Lottspeich F. The 'light' and 'medium' subunits of the photosynthetic reaction centre fromRhodopseudomonas viridis isolation of the genes, nucleotide and amino acid sequence. EMBO J. 5:1986;1149-1158
50. X. Biochemistry. 33:1994;10037-10042
51. Mulkidjanian A.Y., Cherepanov D.A., Haumann M., Junge W. Photosystem II of green plants topology of core pigments and redox cofactors as inferred from electrochromic difference spectra. Biochemistry. 35:1996;3093-3107
52. Nitschke W., Rutherford A.W. Photosynthetic reaction centres variations on a common structural theme? Trends Biochem. Sci. 16:1991;241-245
53. Nitschke W., Feiler U., Lockau W., Hauska G. The photosystem of the green sulfur bacterium Chlorobium limicola contains two early electron acceptors similar to photosystem I. FEBS Letters. 218:1987;283-286
54. Otsuka J., Miyachi H., Horimoto K. Structure model of core proteins in photosystem I inferred from the comparison with those in photosystem II and bacteria; an application of principal component analysis to detect the similar regions between distantly related families of proteins. Biochim. Biophys. Acta. 1118:1992;194-210
55. Pace N.R. A molecular view of microbial diversity and the biosphere. Science. 276:1997;734-740
56. Prince R.C., Gest T., Blankenship R.E. Thermodynamic properties of the photochemical reaction center of Heliobacterium chlorum. Biochim. Biophys. Acta. 810:1985;377-384
57. Rhee K.-H., Morris E.P., Zheleva D., Hankamer B., Kuhlbrandt W., Barber J. Two-dimensional structure of plant photosystem II at 8-Å resolution. Nature. 389:1997;522-526
58. Robert B., Moënne-Loccoz P. Is there a proteic substructure common to all photosynthetic reaction centers? Baltscheffsky M. Current Research on Photosynthesis, Proc. 8th Int. Conf. Photosynth. vol. 2:1990;65-68 Kluwer, Dordrecht
59. Rochaix J.D., Dron M., Rahire M., Maloe P. Sequence homology between the 32k dalton and the D2 chloroplast membrane polypeptides of Chlamydomonas reinhardtii. Plant Mol. Biol. 3:1984;363-370
60. Ruffle S.V., Donnelly D., Blundell T.L., Nugent J.H.A. A three-dimensional model of the photosystem II reaction center of Pisum sativum. Photosynth. Res. 34:1992;298-301
61. Rutherford A.W. Photosystem II, the oxygen evolving photosystem. Stevens S.E., Bryant D.A. Light-energy Transduction in Photosynthesis: Higher Plant and Bacterial Models. 1988;163-177 American Society of Plant Physiologists, Rockville, MD
62. Sakurai H., Kusumoto N., Inoue K. Function of the reaction center of green sulfur bacteria. Photochem. Photobiol. 64:1996;5-13
63. Schubert W.-D., Klukas O., Krauß N., Saenger W., Fromme P., Witt H.T. Present state of the crystal structure analysis of photosystem I at 4.5 Å resolution. Mathis P. Photosynthesis: From Light to Biosphere, Proc. 10th Int. Conf. Photosynth. vol. 2:1995;3-11 Kluwer, Dordrecht
64. Schubert W.-D., Klukas O., Krauß N., Saenger W., Fromme P., Witt H.T. Photosystem I of Synechococcus elongatus at 4 Å resolution comprehensive structure analysis. J. Mol. Biol. 272:1997;741-769
65. Schwartz T., Brettel K. Search for the presence and role of a second phylloquinone in the core of photosystem I. Mathis P. Photosynthesis: From Light to Biosphere., Proc. 10th Int. Conf. Photosynth. vol. 2:1995;43-46 Kluwer, Dordrecht
66. Setif P. Energy transfer and trapping in photosystem I. Barber J. The Photosystems: Structure, Function and Molecular Biology, Topics in Photosynthesis 11. 1992;471-499 Elsevier, Amsterdam
67. Shiozawa J.A., Lottspeich F., Oesterhelt D., Feick R. The primary structure of the Chloroflexus aurantiacus reaction-center polypeptides. Eur. J. Biochem. 180:1989;75-84
68. Small G.J. On the validity of the standard model for primary charge separation in the bacterial reaction center. Chem. Phys. 197:1995;239-257
69. Stiller J.W., Hall B.D. The origin of red algae implications for plastid evolution. Proc. Natl Acad. Sci. USA. 94:1997;4520-4525
70. Svensson B., Vass I., Styring S. Sequence analysis of the D1 and D2 reaction center proteins of photosystem II. Z. Naturforsch. 46C:1991;765-776
71. Svensson B., Etchebest C., Tuffery P., van Kan P., Smith J., Styring S. A model for the photosystem II reaction center core including the structure of the primary donor P680. Biochemistry. 35:1996;14486-14502
72. Trebst A. The topology of the plastoquinone and herbicide binding peptides of photosystem II in the thylakoid membrane. Z. Naturforsch. 41C:1986;240-245
73. Trost J.T., Blankenship R.E. Isolation of a photoactive photosynthetic reaction center-core antenna complex from Heliobacillus mobilis. Biochemistry. 28:1989;9898-9904
74. Trost J.T., Brune D.C., Blankenship R.E. Protein sequences and redox titrations indicate that the electron acceptors in reaction centers from heliobacteria are similar to photosystem I. Photosynth. Res. 32:1992;11-22
75. Vacha F., Joseph D.M., Durrant J.R., Telfer A., Klug D.R., Porter G., Barber J. Photochemistry and spectroscopy of a five-chlorophyll reaction center of photosystem II isolated by using a Cu affinity column. Proc. Natl Acad. Sci. USA. 92:1995;2929-2933
76. 1to the iron-sulphur centers in photosystem I as studied by transient EPR spectroscopy. Biochemistry. 33:1994;11789-11797
77. Vermaas W.F.J. Evolution of heliobacteria implications for photosynthetic reaction center complexes. Photosynth. Res. 41:1994;285-294
78. Webber A.N., Su H., Bingham S.E., Käß H., Krabben L., Kuhn M., Jordan R., Schlodder E., Lubitz W. Site-directed mutations affecting the spectroscopic characteristics and midpoint potential of the primary donor in photosystem I. Biochemistry. 35:1996;12857-12863
79. Woese C.R. Bacterial evolution. Microbiol. Rev. 51:1987;221-271
80. Woese C.R., Kandler O., Wheelis M.L. Towards a natural system of organisms proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA. 87:1990;4576-4579
81. Xiong J., Subramaniam S., Govindjee. Modeling of the D1/D2 proteins and cofactors of the photosystem II reaction center implications for herbicide and bicarbonate binding. Protein Sci. 5:1996;2054-2073
82. Zinth W., Arlt T., Wachveitl J. The primary process of bacterial photosynthesis ultrafast reaction of the optimum use of light energy. Ber. Bunsenges. Phys. Chem. 100:1996;1962-1966