Photosystem I at 4 Å resolution represents the first structural model of a joint photosynthetic reaction centre and core antenna system

Norbert Krau¹, Wolf-Dieter Schubert¹, Olaf Klukas¹, Petra Fromme², Horst Tobias Witt^2, 4 & Wolfram Saenger^1, 3

  ¹Institut für Kristallographie, Freie Universität Berlin, Takustr. 6,0-14195 Berlin, Germany

  ²Max-Volmer-lnstitut für biophysikalische Chemie und Biochemie, Technische Universität Berlin, Strae-des-17.Juni 135, D-10623 Berlin, Germany

  ³saenger@chemie.fu-berlin.de

  ⁴witt@phosis1.chem.tu-berlin.de

The 4 Å X-ray structure model of trimeric photosystem I of the cyanobacterium Synechococcus elongatus reveals 31 transmembrane, nine surface and three stromal -helices per monomer, assigned to the 11 protein subunits: PsaA and PsaB are related by a pseudo two-fold axis normal to the membrane plane, along which the electron transfer pigments are arranged. 65 antenna chlorophyll a (Chl a) molecules separated by 16 Å form an oval, clustered net, continuous with the electron transfer chain through the second and third Chl a pairs of the electron transfer system. This suggests a dual role for these Chl a both in excitation energy and electron transfer. The architecture of the protein core indicates quinone and iron-sulphur type reaction centres to have a common ancestor.

1. Hill, R. & Bendall, F. Function of the two cytochrome components in chloroplasts: A working hypothesis. Nature 186, 136−137 (1960). | ISI | ChemPort |
2. Kok, B. & Hoch, G. in Light and Life (eds W.D. McElroy & B. Glass) 397−405 (John Hopkins Press, 1961). | ChemPort |
3. Duysens, L.N.M., Amesz, J. & Kamp, B.M. Two photochemical systems in photosynthesis. Nature 190, 510−511 (1961). | PubMed | ISI | ChemPort |
4. Witt, H.T., Müller, A. & Rumberg, B. Experimental evidence for the mechanism of photosynthesis. Nature 191, 194−195 (1961). | ISI | ChemPort |
5. Yu, L., Zhao, J., Mühlenhoff, U., Bryant, D.A. & Golbeck, J.H. PsaE is required for in vivo cyclic electron flow around Photosystem I in the cyanobacerium Synechococcus sp. PCC7002. Plant Physiol. 103, 171−180 (1993). | PubMed | ISI | ChemPort |
6. Yu, L. et al in Res. Photosynth. Proclnt. Congr. Photosynth. 9th Ed. (Ed. N. Murata) 565−568 (Kluwer, Dordrecht, Netherlands, 1992). | ChemPort |
7. Fork, D.C. & Herbert, S.K. Electron transport and photophosphorylation by Photosystem I in vivo in plants and cyanobacteria. Photosynth. Res. 36 149−168 (1993). | ISI | ChemPort |
8. 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, 618−624 (1985). | ISI |
9. Ermler, U., Fritsch, G., Buchannan, 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, 925−936 (1994) | PubMed | ISI | ChemPort |
10. Ducruix, A. & Reiss-Husson, F. Preliminary characterisation by X-ray diffraction of crystals of photochemical reaction centres from wild-type Rhodopseudomonas sphaeroides. J. Mot. Biol. 193, 419−421 (1987). | ChemPort |
11. Alien, J.P., Feher, G., Yeates, T.O., Komiya, H. & Rees, D.C. Structure of the reaction center from Rhodobacter sphaeroides R-26: The protein subunits. Proc. Natl Acad. Sci. USA 84, 6162−6166 (1987). | PubMed | ChemPort |
12. Chang, C.H., el-Kabbani, O., Tiede, D., Morris, J. & Schiffer, M. Structure of the membrane-bound protein photosynthetic reaction center from Rhodobacter sphaeroides. Biochemistry 30, 5352−5360 (1991). | PubMed | ISI | ChemPort |
13. Golbeck, J.H. Photosystem I in cyanobacteria. in Molecular Biology of Cyanobacteria, (ed. D.A. Bryant) 179−220 (Kluwer, Dordrecht, 1994).
14. Chitnis, P.R., Xu, Q., Chitnis, V.P. & Nechushtai, R. Function and organisation of Photosystem I polypeptides. Photosynth. Res. 44, 23−40 (1995). | ISI | ChemPort |
15. Mühlenhoff, U., Haehnel, W., Witt, H. & Herrmann, R.G. Genes encoding eleven subunits of Photosystem I from the thermophilic cyanobacterium Synechococcus sp. Gene 127, 71−78 (1993). | Article | PubMed | ISI |
16. Hladík, J. & Sofrová, D. Does the trimeric form of the Photosystem 1 reaction center of cyanobacteria in vivo exist? Photosynthesis Research 29, 171−175 (1991). | ISI |
17. Shubin, V.V., Tsuprun, V.L., Bezsmertnaya, I.N. & Karapetyan, N.B. Trimeric forms of the Photosystem I reaction center complex pre-exits in the membranes of cyanobacterium Spirulina platensis. FEBS Lett. 334, 79−82 (1993). | Article | PubMed | ISI | ChemPort |
18. Tsiotis, G., Haase, W., Engel, A. & Michel, H. Isolation and structural characterisation of trimeric cyanobacterial Photosystem I complex with the help of recombinant antibody fragments. Eur. J. Biochem. 231, 823−830 (1995). | PubMed | ISI | ChemPort |
19. Rögner, M., Mühlenhoff, U., Boekema, E.J. & Witt, H.T. Mono-, di-, and trimeric PS I reaction center complexes isolated from the thermophilic cyanobacterium Synechococcus sp. Size, shape and activity. Biochim. Biophys. Acta 1015, 415−424 (1990). | ISI |
20. Witt, I. et al. X-ray characterisation of single crystals of the reaction center I of water splitting photosynthesis. Ber. Bunsenges. Phys. Chem. 92, 1503−1506 (1988). | ChemPort |
21. Witt, H.T., Krau, N., Hinrichs, W., Witt, I., Fromme, P. & Saenger, W. Three-dimensional crystals of photosystem I from Synechococcus sp. and X-Ray structure analysis at 6 Å resolution., in Research in Photosynthesis., Vol 1 (ed. N. Murata) 521−528 (Kluwer, Dordrecht, 1992). | ChemPort |
22. Krau, N. et al. Three-dimensional structure of system I of photosynthesis at 6 Å resolution. Nature 361, 326−331 (1993). | Article | ISI | ChemPort |
23. Schubert, W.-D. et al. Present state of the crystal structure analysis of Photosystem I at 4.5 Å resolution. in Photosynthesis: from Light to Biosphere, 2 (ed. P. Mathis) 3−11 (Kluwer, Dordrecht, 1995). | ChemPort |
24. Richardson, J.S. & Richardson, D.C. Interpretation of electron density maps. Meths Enzymol. 115, 189−206 (1985). | Article | ChemPort |
25. Adman, E.T., Sieker, L.C. & Jensen, L.H. The structure of Peptococcus aerogenes ferredoxin. Refinement at 2 Å resolution. J. Biol. Chem. 251, 3801−3806 (1976). | PubMed | ISI | ChemPort |
26. Falzone, C.J., Kao, Y.-H., Zhao, J., Bryant, D.A. & Lecomte, J.T.J. Three-dimensional solution structure of PsaE from the cyanobacterium Synechococcus sp. Strain PCC 7002, a Photosystem I protein that shows structural homology with SH3 Domains. Biochemistry 33, 6052−6062 (1994). | PubMed | ISI | ChemPort |
27. Xu, Q., Chitnis, V.P. & Chitnis, P.R. Structural organization of photosystem I polypeptides in Photosynthesis: from Light to Biosphere. 2 (ed. P. Mathis) 87−90 (Kluwer, Dordrecht, 1995). | ChemPort |
28. Jansson, S. Cross-linking studies of PS I. Plant Physiol. in the press, (1996).
29. Jekow, P., Fromme, P., Witt, H.T. & Saenger, W. Photosystem I from Synechococcus elongatus: preparation and crystallization of monomers with varying subunit compositions. Biochim. Biophys. Acta 1229, 115−1120 (1995). | Article | ISI | ChemPort |
30. Boekema, E.J., Boonstra, A.F., Dekker, J.P. & Rögner, M. Electron microscopic structural analysis of Photosystem I, Photosystem II, and the cytochrome b₆/f complex from green plants and cyanobacteria. J. Bioenerg. Biomem. 26, 17−29 (1994). | ISI | ChemPort |
31. Böttcher, B., Gräber, P. & Boekema, E.J. The structure of Photosystem I from the thermophilic cyanobacterium Synechococcus sp. determined by electron microscopy of two-dimensional crystals. Biochim. Biophys. Acta 1100, 125−136 (1992). | PubMed | ISI |
32. Kruip, J., Boekema, E.J., Bald, D., Boonstra, A.F. & Rögner, M. Isolation and Structural Characterisation of Monomeric and Trimeric Photosystem I Complexes (P700.F_A/F_B and P700.F_X) from the Cyanobacterium Synechocystis PCC 6803. J. Biol. Chem. 268, 23353−23360 (1993). | PubMed | ISI | ChemPort |
33. Rodday, S.M., Jun, S.-S. & Biggins, J. Interaction of the F_AF_B-containing subunit with the Photosystem 1 core heterodimer. Photosynth. Res. 36, 1−9 (1993). | ISI | ChemPort |
34. Chitnis, V.P. et al. Targeted inactivation of the gene psaL encoding a subunit of Photosystem I of the cyanobacterium Synechocystis sp PCC 6803. J. Biol. Chem. 268, 11678−11684 (1993). | PubMed | ISI | ChemPort |
35. Okkels, J.S., Scheller, H.V., Svendsen, I. & Møller, B.L. Isolation and characterization of a cDNA clone encoding an 18-kDa hydrophobic Photosystem I subunit (PSI-L) from barley (Hordeum vulgare L.) J. Biol. Chem. 266, 6767−6773 (1991). | PubMed | ISI | ChemPort |
36. Xu, Q. et al. Mutational analysis of Photosystem I polypeptides in the cyanobacterium Synechocystis sp. PCC 6803. Targeted inactivation of psal reveals the function of Psal in the structural organization of PsaL. J. Biol. Chem. 270, 16243−16250 (1995). | Article | PubMed | ISI | ChemPort |
37. Franzén, L.-G., Frank, G., Zuber, H. & Rochaix, J.-D. Isolation and characterization of cDNA clones encoding Photosystem I subunits with molecular masses 11.0, 10.0, and 8.4 kDa from Chlamydomonas reinhardtii. Mol. Gen. Genet. 219, 137−144 (1989). | PubMed | ISI | ChemPort |
38. Farah, J., Rappaport, F., Choquet, Y., Joliot, P. & Rochaix, J-D. Isolation of a psaF-deficient mutant of Chlamydomonas reinhardtii: efficient interaction of plastocyanin with the Photosystem I reaction center is mediated by the PsaF subunit. EMBO J. 14, 4976−4984 (1995). | PubMed | ISI | ChemPort |
39. Hippler, M., Ratajczak, R. & Haehnel, W. Identification of the plastocyanin-binding subunit of Photosystem I. FEBS Lett. 250, 280−284 (1989). | Article | ISI | ChemPort |
40. Kruip, J. et al. Localization of subunits in PS1, PS2 and in a PS2/Light-Harvesting-Supercomplex. in Photosynthesis: from Light to Biosphere., 3 (ed. P. Mathis) 405−408 (Kluwer, Dordrecht., 1995). | ChemPort |
41. Golbeck, J.H., Parrett, K.G., Mehari, T., Jones, K.L. & Brand, J.J. Isolation of the intact Photosystem I reaction center core containing P700 and iron-sulfur center F_X. FEBS Lett. 288, 268−272 (1988). | Article |
42. Rousseau, F. & Lagoutte, B. Evidence for the involvement of PSI-E subunit in the reduction of ferredoxin by Photosystem I. EMBO J. 12, 1755−1765 (1993). | PubMed | ISI | ChemPort |
43. Høj, P.B., Svendsen, I., Scheller, H.V., Møller, B.L. Identification of a chloroplast-encoded 9-kDa polypeptide as a 2[4Fe-4S] protein carrying centers A and B of Photosystem I. J. Biol. Chem. 262, 12676−12684 (1987). | PubMed | ISI |
44. Hayashida, N. et al. The gene for the 9 kDa polypeptide, a possible apoprotein for the iron-sulfur centers A and B of the Photosystem I complex, in tobacco chloroplast DNA. Curr. Genet. 12, 247−250 (1987). | PubMed | ISI | ChemPort |
45. Oh-oka, H. et al. The 8 kDa polypeptide in Photosystem I is a probable candidate of an iron-sulfur center protein coded by the chloroplast gene frxA. FEBS Lett. 218, 52−54 (1987). | Article | ChemPort |
46. Kamlowski, A., van der Est, A., Fromme, P. & Stehlik, D. Structural organization of the acceptors A₁, F_X, F_A and F_B in Photosystem I from EPR in solution and single crystals in Photosynthesis: from Light to Biosphere. 2 (ed. P. Mathis) 29−34 (Kluwer, Dordrecht, 1995). | ChemPort |
47. Zhao Li, N., Warren, P.V., Golbeck, J.H. & Bryant, D.A. Site-Directed conversion of a cystein to aspartate leads to the assembly of a [3Fe-4S] cluster in PsaC of Photosystem I. The photoreduction of F_A is independent of F_B. Biochemistry 31, 5093−5099 (1992). | PubMed | ISI | ChemPort |
48. Kä, H., Bittersmann-Weidlich, E., Andreasson, L.-E., Boenigk, B. & Lubitz, W.ENDOR and ESEEM of the ¹⁵N labelled radical cations of chlorophyll a and the primary donor P700 in Photosystem I. Chem. Phys. 194, 419−432 (1995). | Article | ISI |
49. Evans, M.C.W., Bratt, P.J., Heathcote, P., Moënne-Loccoz, P., Fourier transform electron spin echo envelope modulation spectroscopy of the 14N primary donors, P700⁺ and P870⁺. in Photosynthesis: from Light to Biosphere. Vol. 2 (ed. P. Mathis), 183−186 (Kluwer, Dordrecht, 1995).
50. Arlt, T. et al. The accessory bacteriochlorophyll: a real electron carrier in primary photosynthesis. Proc. Natl. Acad Sci. USA 90, 11757−11761 (1993). | PubMed | ChemPort |
51. Brettel, K. New assignment for the 250 s kinetics in Photosystem I: P-700^* recombines with A₁^- (not F_X^-). Biochim. Biophys. Acta. 576, 246−249 (1989).
52. Flemming, C. Charakterisierung des Antennensystems von monomeren und trimeren Photosystem I Komplexen. Diploma Thesis, Technische Universität Berlin, 1996.
53. van Grondelle, R., Energy transfer and trapping in photosynthesis, Biochim. Biophys. Acta. 1187, 1−65, (1994). | Article |
54. Vermaas, W.F.J. Evolution of heliobacteria: implications for photosynthetic reaction center complexes. Photosynth. Res. 41, 285−294 (1994). | PubMed | ISI | ChemPort |
55. Fromme, P., Witt, H.T., Schubert, W.-D., Klukas, O., Saenger, W. & Krau, N. Structure of Photosystem I at 4.5 Å resolution: A short review including evolutionary aspects. Biochim. Biophys. Acta 1275, 76−83 (1996). | Article | ISI | ChemPort |
56. Leslie, A.G.W. in Joint CCP4 and ESF-EACMB Newsletter on Protein Crystallography, No. 26, Daresbury Laboratory, Warrington, United Kingdom (1992).
57. Otwinowski, Z., Oscillation Data Reduction Protgramm, in Proceedings of the CCP4 Study Weekend: Data Collection and Processing (eds L. Sawyer, N. Isaacs, S. Bailey) 56−62 (SERC, Daresbury Laboratory, England, 1993).
58. CCP4, The Collaborative Computational Project, Number 4. The CCP4 Suite; Programms for Protein Crystallography. Acta Cryst. D50, 760−763 (1994).
59. Cowtan, K. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography 31, 34−48 (1994).
60. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Cryst. A47, 110−119 (1991). | ChemPort |
61. Krabben, L. et al. Site-directed mutations of PsaB for the study of cofactor-protein and protein-protein interaction of Photosystem I. in Photosynthesis: from Light to Biosphere. Vol. 2 (ed. P. Mathis) 123−126 (Kluwer, Dordrecht, 1995). | ChemPort |
62. 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, 133−47 (1991). | ISI | ChemPort |
63. Gavel, Y., Steppuhn, J., Herrmann, R.G. & von Heijne, G. The 'positive-inside rule' applies to thylakoid membrane proteins. FEBS Lett. 282, 41−16 (1991). | Article | PubMed | ISI | ChemPort |
64. Vallon, O. & Bogograd, L. Topological study of PSI-A and PSI-B, the large subunits of the Photosystem-l reaction center. Eur. J. Biochem. 214, 907−915 (1993). | PubMed | ISI | ChemPort |
65. Kraulis, P.K. Molscript: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946−950 (1991). | Article | ISI |

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