Structural basis of light harvesting by carotenoids: Peridinin- chlorophyll-protein from Amphidinium carterae

Science

Volumn 272, Issue 5269, 1996, Pages 1788-1791

  Hofmann, Eckhard ^a   Wrench, Pamela M ^b   Sharples, Frank P ^b   Hiller, Roger G ^b   Welte, Wolfram ^a   Diederichs, Kay ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b MACQUARIE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CAROTENOID; CHLOROPHYLL;

ARTICLE; DINOFLAGELLATE; MOLECULAR INTERACTION; NONHUMAN; PHOTOSTIMULATION; PHOTOSYNTHESIS; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION;

AMPHIDINIUM CARTERAE; DINOPHYCEAE;

EID: 0030055628     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.272.5269.1788     Document Type: Article

References (42)

1. For recent reviews about the photoprotective and light-harvesting functions of carotenoids, see H. A. Frank and R. J. Cogdell, in Carotenoids in Photosynthesis, A Young and G. Britton, Eds. (Chapman & Hall, London, 1993); Y. Koyama, M. Kuki, P. O. Andersson, T. Gillbro, Photochem Photobiol. 63, 243 (1996).
2. For recent reviews about the photoprotective and light-harvesting functions of carotenoids, see H. A. Frank and R. J. Cogdell, in Carotenoids in Photosynthesis, A Young and G. Britton, Eds. (Chapman & Hall, London, 1993); Y. Koyama, M. Kuki, P. O. Andersson, T. Gillbro, Photochem Photobiol. 63, 243 (1996).
3. R G. Hiller, P. M. Wrench, A A. Gooley, G Shoebridge, J. Breton, Photochem. Photobiol. 57, 125 (1993), R. Iglesias-Prieto. N S. Govind, R K Trench, Philos Trans. R. Soc. London Ser. B 403, 381 (1993); R. G. Hiller, P. M. Wrench, F. P. Sharples, FEBS Lett 363, 175 (1995).
4. R G. Hiller, P. M. Wrench, A A. Gooley, G Shoebridge, J. Breton, Photochem. Photobiol. 57, 125 (1993), R. Iglesias-Prieto. N S. Govind, R K Trench, Philos Trans. R. Soc. London Ser. B 403, 381 (1993); R. G. Hiller, P. M. Wrench, F. P. Sharples, FEBS Lett 363, 175 (1995).
5. R G. Hiller, P. M. Wrench, A A. Gooley, G Shoebridge, J. Breton, Photochem. Photobiol. 57, 125 (1993), R. Iglesias-Prieto. N S. Govind, R K Trench, Philos Trans. R. Soc. London Ser. B 403, 381 (1993); R. G. Hiller, P. M. Wrench, F. P. Sharples, FEBS Lett 363, 175 (1995).
6. W Kühlbrandt and D. N. Wang, Nature 350, 130 (1991); - and Y. Fujioshi, ibid. 367, 614 (1994).
7. W Kühlbrandt and D. N. Wang, Nature 350, 130 (1991); - and Y. Fujioshi, ibid. 367, 614 (1994).
8. B. J. Norns and D. J. Miller, Plant Mol. Biol. 24, 673 (1994).
9. F T. Haxo, J. H. Kycia, G. F. Somers, A. Bennett, H. W Siegelman, Plant Physiol. 57, 297 (1976); B. B. Prezelin, in The Biology of Dinoflagellates, F J. R Taylor, Ed. (Blackwell Scientific, Oxford, 1987), p. 174; R Iglesias-Prieto, N. S. Govind, R. K. Trench, Proc R. Soc. London Ser. B 246, 275 (1991); E L Triplett et al., Mol. Mar Biol. Biotechnol 2, 246 (1993).
10. F T. Haxo, J. H. Kycia, G. F. Somers, A. Bennett, H. W Siegelman, Plant Physiol. 57, 297 (1976); B. B. Prezelin, in The Biology of Dinoflagellates, F J. R Taylor, Ed. (Blackwell Scientific, Oxford, 1987), p. 174; R Iglesias-Prieto, N. S. Govind, R. K. Trench, Proc R. Soc. London Ser. B 246, 275 (1991); E L Triplett et al., Mol. Mar Biol. Biotechnol 2, 246 (1993).
11. F T. Haxo, J. H. Kycia, G. F. Somers, A. Bennett, H. W Siegelman, Plant Physiol. 57, 297 (1976); B. B. Prezelin, in The Biology of Dinoflagellates, F J. R Taylor, Ed. (Blackwell Scientific, Oxford, 1987), p. 174; R Iglesias-Prieto, N. S. Govind, R. K. Trench, Proc R. Soc. London Ser. B 246, 275 (1991); E L Triplett et al., Mol. Mar Biol. Biotechnol 2, 246 (1993).
12. F T. Haxo, J. H. Kycia, G. F. Somers, A. Bennett, H. W Siegelman, Plant Physiol. 57, 297 (1976); B. B. Prezelin, in The Biology of Dinoflagellates, F J. R Taylor, Ed. (Blackwell Scientific, Oxford, 1987), p. 174; R Iglesias-Prieto, N. S. Govind, R. K. Trench, Proc R. Soc. London Ser. B 246, 275 (1991); E L Triplett et al., Mol. Mar Biol. Biotechnol 2, 246 (1993).
13. R. G Hiller, P. M. Wrench, F P Sharples, in Photosynthesis From Light to Biosphere, P. Mathis, Ed. (Kluwer, Dordrecht, Netherlands, 1995), vol. 1, p. 24.
14. P. S. Song, P. Koka, B. B. Prezelin, F. T Haxo, Biochemistry 15, 4422 (1976), P. Koka and P. S Song, Biochim. Biophys Acta 495, 220 (1977).
15. P. S. Song, P. Koka, B. B. Prezelin, F. T Haxo, Biochemistry 15, 4422 (1976), P. Koka and P. S Song, Biochim. Biophys Acta 495, 220 (1977).
16. D Carbonera, G. Giacometti, G. Agostini, Spectrochim. Acta A 51, 115 (1995).
17. G. McDermott et al., Nature 374, 517 (1995).
18. 2, 50 mM KCl, and 25 mM MES-KOH (pH 5.8)] with a reservoir of 8 to 12% PEG8000 For heavy-atom screening, crystals were transferred to droplets of equivalent PEG concentration in MES crystallization buffer containing the heavy-atom compound
19. A Rawlyer, M Meylan-Bettex, P A. Siegenthaler, Biochim. Biophys. Acta 1233, 122 (1995).
20. 2- and COOH-terminal halves; consequently, they do not obey twofold local symmetry.
21. J. Richardson, Adv. Protein Chem. 34, 167 (1981).
22. Structural comparisons against databases of unique structures were performed with two different programs DAU [L Holm and C. Sander, J. Mol Biol 233, 123 (1993)] and SUPERIMPOSE [ K. Diederichs, Proteins Struct. Funct. Genet. 23, 187 (1995)].
23. Structural comparisons against databases of unique structures were performed with two different programs DAU [L Holm and C. Sander, J. Mol Biol 233, 123 (1993)] and SUPERIMPOSE [ K. Diederichs, Proteins Struct. Funct. Genet. 23, 187 (1995)].
24. These two other crystal forms of POP were obtained by a different purification scheme involving ammonium sulfate precipitation [K. Steck, T. Wacker, W. Weite, F. P. Sharples, R G Hiller, FEBS Lett. 268, 48 (1990)]. Data for space group P1 were collected to 2.7 Å resolution from one crystal on a RAXIS IIc image plate detector at Molecular Structure Corporation (Houston, TX). Data for space group C2 with cell axes different from (10) were measured from one crystal on a FAST area detector at CNRS (Grenoble, France) to a maximum resolution of 3.2 Å. The crystal structures were solved by the molecular replacement procedures as implemented in the program X-PLOR (24). In both cases, we used a trimer of PCP as the search model and obtained unambiguous solutions of the rotation and translation functions. After rigid body refinement, the R factor was less than 30% for both crystal forms. The correctness of the molecular replacement solutions was confirmed by omit maps showing the chlorophyll molecules, which had been left out of the model used for structure factor calculation
25. B. W. Matthews, R. E. Fenna, M. C Bolognesi, M F. Schmid, J. M. Olson, J. Mol. Biol. 131, 259 (1979).
26. T Schirmer. W Bode, R. Huber, W. Sidier, H. J. Zuber, ibid. 184, 257 (1985)
27. For a review, see T. Förster, in Modern Quantum Chemistry, Istanbul Lectures, Part III: Action of Light and Organic Crystals, O. Sinanoglu, Ed (Academic Press, New York, 1965), pp. 93.
28. Estimates of distances permitting efficient energy transfer from peridinins to chlorophyll were given as at most 5.8 to 8.6 Å (7), approximately 5.0 Å (22), arid 4.5 Å [T. Gillbro et al , Photochem. Photobiol. 57, 44 (1993)].
29. Pairwise comparisons give root-mean-squares deviations between 0.6 and 1.3 Å.
30. y transition moment was taken as the vector between the C1B and C2D atoms of the porphyrin ring [nomenclature as in D. E. Tronrud, M. F. Schmid, B. W. Matthews, J. Mol. Biol. 188, 443 (1986)].
31. M. Mimuro, N Tamai, T Ishimaru, I. Yamazaki, Biochim. Biophys. Acta 1016, 280 (1990).
32. T A Jones, J. Y. Zou, S. W. Cowan, M. Kjetdgaard, Acta Crystallogr. A 47, 110 (1991)
33. A T. Brùnger, X-PLOR Version 3.1 (Yale Univ. Press, New Haven, CT, 1987); Nature 355, 472 (1992).
34. A T. Brùnger, X-PLOR Version 3.1 (Yale Univ. Press, New Haven, CT, 1987); Nature 355, 472 (1992).
35. P. Kraulis, J. Appl. Crystallogr. 24, 946 (1991).
36. W. Kabsch, ibid. 21, 916 (1988).
37. G M. Sheldrick, Acta Crystallogr. A 46, 467 (1990).
38. R. E Dickerson, J. E. Weinzierl, R. A Palmer, Acta Crystallogr B 24, 997 (1968); K. Diederichs, Jt. CCP4 ESF-EACBM Newsl. Protein Crystallogr 31, 23 (1994).
39. R. E Dickerson, J. E. Weinzierl, R. A Palmer, Acta Crystallogr B 24, 997 (1968); K. Diederichs, Jt. CCP4 ESF-EACBM Newsl. Protein Crystallogr 31, 23 (1994).
40. W. Furey and S. Swaminathan, in Methods Enzymol., in press
41. V. S. Lamzin and K. S. Wilson, Acta Crystallogr. D 49, 127 (1993).
42. We thank the staff of the European Molecular Biology Laboratory at the Deutsches Elektronen-Synchrotron (DESY) (Hamburg, Germany) for help during synchrotron data collection and the staff of Molecular Structure Corporation (Houston, TX) for the opportunity to collect x-ray data of a P1 crystal during a demonstration. We also thank K. Steck and P. Timmins for help in the early stages of the project, P. A. Karplus for comments on the manuscript, and W. Kreutz for support. This work was supported by grants from the Deutsche Forschungsgemeinschaft and the Australian Research Council. The atomic coordinates have been submitted to the Brookhaven protein database (ID code 1PPR).