Triplet state dynamics in peridinin-chlorophyll-a-protein: A new pathway of photoprotection in LHCs?

Biophysical Journal

Volumn 93, Issue 6, 2007, Pages 2118-2128

  Alexandre, Maxime T A ^a   Lührs, Daniel C ^a   Van Stokkum, Ivo H M ^a   Hiller, Roger ^b   Groot, Marie Louise ^a   Kennis, John T M ^a   Van Grondelle, Rienk ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b MACQUARIE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONYL DERIVATIVE; CAROTENOID; CHLOROPHYLL A; LACTONE; PERIDININ CHLOROPHYLL A PROTEIN COMPLEX; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

AMPHIDINIUM CARTERAE; ARTICLE; COMPLEX FORMATION; DINOFLAGELLATE; ENERGY; ENERGY TRANSFER; EXCITATION; INFRARED SPECTROSCOPY; LIGHT HARVESTING SYSTEM; MOLECULAR INTERACTION; NONHUMAN; PHOTOSYNTHESIS; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN LOCALIZATION; SPECTRAL SENSITIVITY;

AMPHIDINIUM CARTERAE;

EID: 34548749295     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.107.106674     Document Type: Article

References (62)

1. van Grondelle, R., J. P. Dekker, T. Gillbro, and V. Sundström. 1994. Energy-transfer and trapping in photosynthesis. Biochim. Biophys. Acta. 1187:1-65.
2. Hofmann, E., P. M. Wrench, F. P. Sharples, R. G. Hiller, W. Welte, and K. Diederichs. 1996. Structural basis of light harvesting by carotenoids: peridinin-chlorophyll-protein from Amphidinium carterae. Science. 272:1788-1791.
3. Christensen, R. L. 1999. The electronic states of carotenoids. In The Photochemistry of Carotenoids. H. A. Frank, A. J. Young, M. Braun, and R. J. Cogdell, editors. Kluwer, Dordrecht, The Netherlands. 137-159.
4. Krinsky, N. I. 1971. Function. In Carotenoids. O. Isler, G. Guttman, and U. Solms, editors. Birkhäuser, Basel, Switzerland. 669-716.
5. Song, P.-S., P. Koka, B. B. Prezelin, and F. T. Haxo. 1976. Molecular topology of photosynthetic light-harvesting pigment complex, peridinin-chlorophyll-a-protein, from marine dinoflagellates. Biochemistry. 15:4422-4427.
6. Koka, P., and P.-S. Song. 1977. The chromophore topography and binding environment of peridinin-chlorophyll a-protein complexes from marine dinoflagellate algae. Biochim. Biophys. Acta. 495:220-231.
7. Mimuro, M., U. Nagashima, S. Nagaoka, Y. Nishimura, S. Takaichi, T. Katoh, and I. Yamazaki. 1992. Quantitative-analysis of the solvent effect on the relaxation processes of carotenoids showing dual emissive characteristics. Chem. Phys. Lett. 191:219-224.
8. Mimuro, M., Y. Nishimura, S. Takaichi, Y. Yamano, M. Ito, S. Nagaoka, I. Yamazaki, T. Katoh, and U. Nagashima. 1993. The effect of molecular-structure on the relaxation processes of carotenoids containing a carbonyl group. Chem. Phys. Lett. 213:576-580.
9. Bautista, J. A., R. G. Hiller, F. P. Sharples, D. Gosztola, M. Wasielewski, and H. A. Frank. 1999. Singlet and triplet energy transfer in the peridinin-chlorophyll a protein from Amphidinium carterae. J. Phys. Chem. A. 103:2267-2273.
10. Krueger, B. P., S. S. Lampoura, I. H. M. van Stokkum, E. Papagiannakis, J. M. Salverda, C. C. Gradinaru, D. Rutkauskas, R. G. Hiller, and R. van Grondelle. 2001. Energy transfer in the peridinin chlorophyll-a protein of Amphidinium carterae studied by polarized transient absorption and target analysis. Biophys. J. 80:2843-2855.
11. Kleima, F. J., M. Wendling, E. Hofmann, E. J. G. Peterman, R. van Grondelle, and H. van Amerongen. 2000. Peridinin chlorophyll a protein: relating structure and steady-state spectroscopy. Biochemistry. 39:5184-5195.
12. Damjanovic, A., T. Ritz, and K. Schulten. 1999. Energy transfer between carotenoids and bacteriochlorophylls in a light harvesting protein. Physical Review E. 59:3293-3311.
13. Damjanovic, A., T. Ritz, and K. Schulten. 2000. Excitation transfer in the peridinin-chlorophyll-protein of Amphidinium carterae. Biophys. J. 79:1695-1705.
14. Nagae, H., T. Kakitani, T. Katoh, and M. Mimuro. 1993. Calculation of the excitation transfer-matrix elements between the S(2) or S(1) state of carotenoid and the S(2) or S(1). State of bacteriochlorophyll. J. Chem. Phys. 98:8012-8023.
15. Krueger, B. P., G. D. Scholes, R. Jimenez, and G. R. Fleming. 1998. Electronic excitation transfer from carotenoid to bacteriochlorophyll in the purple bacterium Rhodopseudomonas acidophila. J. Phys. Chem. B. 102:2284-2292.
16. Krueger, B. P., G. D. Scholes, and G. R. Fleming. 1998. Calculation of couplings and energy-transfer pathways between the pigments of LH2 by the ab initio transition density cube method. J. Phys. Chem. B. 102:5378-5386.
17. Frank, H. A., and R. J. Cogdell. 1996. Carotenoids in photosynthesis. Photochem. Photobiol. 63:257-264.
18. Cogdell, R. J., T. D. Howard, R. Bittl, E. Schlodder, I. Geisenheimer, and W. Lubitz. 2000. How carotenoids protect bacterial photosynthesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355:1345-1349.
19. Bensasson, R., E. J. Land, and B. Maudinas. 1976. Triplet-states of carotenoids from photosynthetic bacteria studied by nanosecond ultraviolet and electron pulse irradiation. Photochem. Photobiol. 18:189-193.
20. Mathis, P., and J. Kleo. 1973. Triplet-state of beta-carotene and of analog polyenes of different length. Photochem. Photobiol. 18:343-346.
21. Siefermann-Harms, D. 1987. The light-harvesting and protective functions of carotenoids in photosynthetic membranes. Physiol. Plant. 69:561-568.
22. Cogdell, R. J., and H. A. Frank. 1987. How carotenoids function in photosynthetic bacteria. Biochim. Biophys. Acta. 895:63-79.
23. Tandori, J., E. Hideg, L. Nagy, P. Maroti, and I. Vass. 2001. Photoinhibition of carotenoidless reaction centers from Rhodobacter sphaeroides by visible light. Effects on protein structure and electron transport. Photosynth. Res. 70:175-184.
24. Zigmantas, D., R. G. Hiller, V. Sundström, and T. Polivka. 2002. Carotenoid to chlorophyll energy transfer in the peridinin-chlorophyll-a-protein complex involves an intramolecular charge transfer state. Proc. Natl. Acad. Sci. USA. 99:16760-16765.
25. Dexter, D. L. 1953. A theory of sensitized luminescence in solids. J. Chem. Phys. 21:834-850.
26. Carbonera, D., G. Giacometti, U. Segre, A. Angerhofer, and U. Gross. 1999. Model for triplet-triplet energy transfer in natural clusters of peridinin molecules contained in dinoflagellate's outer antenna proteins. J. Phys. Chem. B. 103:6357-6362.
27. Carbonera, D., G. Giacometti, and U. Segre. 1996. Carotenoid interactions in peridinin chlorophyll a proteins from dinoflagellates: evidence for optical excitons and triplet migration. J. Chem. Soc. Faraday Transactions. 92:989-993.
28. Peterman, E. J. G., F. M. Dukker, R. van Grondelle, and H. van Amerongen. 1995. Chlorophyll a and carotenoid triplet states in light-harvesting complex II of higher plants. Biophys. J. 69:2670-2678.
29. Van der Vos, R., D. Carbonera, and A. J. Hoff. 1991. Microwave and optical spectroscopy of carotenoid triplets in light-harvesting complex LHC II of spinach by absorbance-detected magnetic resonance. Appl. Magn. Res. 2:179-202.
30. Angerhofer, A., F. Bornhauser, A. Gall, and R. J. Cogdell. 1995. Optical and optically detected magnetic-resonance investigation on purple photosynthetic bacterial antenna complexes. Chem. Phys. 194:259-274.
31. Holzwarth, A. R. 1996. Data analysis of time-resolved measurements. In Biophysical Techniques in Photosynthesis. J. Amesz and A. J. Hoff, editors. Kluwer, Dordrecht, The Netherlands. 75-92.
32. van Stokkum, I. H. M., D. S. Larsen, and R. van Grondelle. 2004. Global and target analysis of time-resolved spectra. Biochim. Biophys. Acta. 1657:82-104.
33. Gurzadyan, G. G., and S. Steenken. 2002. Photoionization of beta-carotene via electron transfer from excited states to chlorinated hydrocarbon solvents. A picosecond transient absorption study. Phys. Chem. Chem. Phys. 4:2983-2988.
34. Hashimoto, H., Y. Koyama, Y. Hirata, and N. Mataga. 1991. S1 and T1 species of β-carotene generated by direct photo-excitation from the all-trans, 9-cis, 13-cis and 15-cis isomers as revealed by picosecond transient absorption and transient Raman spectroscopies. J. Phys. Chem. 95:3072-3076.
35. - excited state of carotenoids. Chem. Phys. Lett. 175:163-169.
36. Nagae, H., M. Kuki, J.-P. Zhang, T. Sashima, Y. Mukai, and Y. Koyama. 2000. Vibronic coupling through the in-phase, C=C stretching mode plays a major role in the 2Ag- to 1Ag-internal conversion of all-trans carotene. J. Phys. Chem. A. 104:4155-4166.
37. Bernhard, K., and M. Grosjean. 1995. Infrared spectroscopy. In Carotenoids. G. Britton, S. Liaaen-Jensen, and H. Pfander, editors. Birkhäuser. Basel, Switzerland.
38. Breton, J., E. Nabedryk, and W. Leibl. 1999. FTIR study of the primary electron donor of photosystem I (P700) revealing delocalization of the charge in P700(+) and localization of the triplet character in (3)P700. Biochemistry. 38:11585-11592.
39. Breton, J. 2001. Fourier transform infrared spectroscopy of primary electron donors in type I photosynthetic reaction centers. Biochim. Biophys. Acta. 1507:180-193.
40. Noguchi, T. 2002. Dual role of triplet localization on the accessory chlorophyll in the photosystem II reaction center: photoprotection and photodamage of the D1 protein. Plant Cell Physiol. 43:1112-1116.
41. Mantele, W. G., A. M. Wollenweber, E. Nabedryk, and J. Breton. 1988. Infrared spectroelectrochemistry of bacteriochlorophylls and bacteriopheophytins: implications for the binding of the pigments in the reaction center from photosynthetic bacteria. Proc. Natl. Acad. Sci. USA. 85:8468-8472.
42. Okubo, T., and T. Noguchi. 2007. Selective detection of the structural changes upon photoreactions of several redox cofactors in photosystem II by means of light-induced ATR-FTIR difference spectroscopy. Spectrochim. Acta A Mol. Biomol. Spectrosc. 66:863-868.
43. Hartwich, G., C. Geskes, H. Scheer, J. Heinze, and W. Mantele. 1995. Fourier-transform infrared-spectroscopy of electrogenerated anions and cations of metal-substituted bacteriochlorophyll-alpha. J. Am. Chem. Soc. 117:7784-7790.
44. Kristallovich, E. L., I. D. Shamyanov, M. R. Yagudaev, and V. M. Malikov. 1987. Frequencies and integral intensities of lactone and ester carbonyls of natural guaianolides. Him. Prir. Soedin. 6:805-811.
45. Peterman, E. J. G., C. Gradinaru, F. Calkoen, J. C. Borst, R. van Grondelle, and H. van Amerongen. 1997. Xanthophylls in light-harvesting complex II of higher plants: light harvesting and triplet quenching. Biochemistry. 36:12208-12215.
46. Akimoto, S., S. Takaichi, T. Ogata, Y. Nishimura, I. Yamazaki, and M. Mimuro. 1996. Excitation energy transfer in carotenoid-chlorophyll protein complexes probed by femtosecond fluorescence decays. Chem. Phys. Lett. 260:147-152.
47. Rondonuwu, F. S., T. Taguchi, R. Fujii, K. Yokoyama, Y. Koyama, and Y. Watanabe. 2004. The energies and kinetics of triplet carotenoids in the LH2 antenna complexes as determined by phosphorescence spectroscopy. Chem. Phys. Lett. 384:364-371.
48. Takiff, L., and S. G. Boxer. 1988. Phosphorescence spectra of bacteriochlorophylls. J. Am. Chem. Soc. 110:4425-4426.
49. You, Z. Q., C. P. Hsu, and G. R. Fleming. 2006. Triplet-triplet energy-transfer coupling: theory and calculation. J. Chem. Phys. 124:044506.
50. Kodis, G., C. Herrero, R. Palacios, E. Marino-Ochoa, S. Gould, L. de la Garza, R. van Grondelle, D. Gust, T. A. Moore, A. L. Moore, and J. T. M. Kennis. 2004. Light harvesting and photoprotective functions of carotenoids in compact artificial photosynthetic antenna designs. J. Phys. Chem. B. 108:414-425.
51. Berera, R., C. Herrero, L. H. M. van Stokkum, M. Vengris, G. Kodis, R. E. Palacios, H. van Amerongen, R. van Grondelle, D. Gust, T. A. Moore, A. L. Moore, and J. T. M. Kennis. 2006. A simple artificial light-harvesting dyad as a model for excess energy dissipation in oxygenic photosynthesis. Proc. Natl. Acad. Sci. USA. 103:5343-5348.
52. Premvardhan, L., E. Papagiannakis, R. G. Hiller, and R. van Grondelle. 2005. The charge-transfer character of the S0→S2 transition in the carotenoid peridinin is revealed by Stark spectroscopy. J. Phys. Chem. B Condens Matter Mater Surf Interfaces Biophys. 109:15589-15597.
53. Frese, R. 2003. Symmetry in photosynthesis. PhD thesis. Vrije Unversiteit, Amsterdam.
54. Salverda, J. M. 2003. Interacting pigments in light-harvesting complexes studied with nonlinear spectroscopy. PhD thesis. Vrije Universiteit, Amsterdam. Chapter 6.
55. Carbonera, D., G. Giacometti, U. Segre, E. Hofmann, and R. G. Hiller. 1999. Structure-based calculations of the optical spectra of the light-harvesting peridinin-chlorophyll-protein complexes from Amphidinium carterae and Heterocapsa pygmaea. J. Phys. Chem. B. 103:6349-6356.
56. Papagiannakis, E., J. T. M. Kennis, I. H. M. van Stokkum, R. J. Cogdell, and R. van Grondelle. 2002. An alternative carotenoid-to-bacteriochlorophyll energy transfer pathway in photosynthetic light harvesting. Proc. Natl. Acad. Sci. USA. 99:6017-6022.
57. Gradinaru, C. C., J. T. M. Kennis, E. Papagiannakis, I. H. M. van Stokkum, R. J. Cogdell, G. R. Fleming, R. A. Niederman, and R. van Grondelle. 2001. An unusual pathway of excitation energy deactivation in carotenoids: singlet-to-triplet conversion on an ultrafast timescale in a photosynthetic antenna. Proc. Natl. Acad. Sci. USA. 98:2364-2369.
58. Papagiannakis, E., S. K. Das, A. Gall, I. H. M. van Stokkum, B. Robert, R. van Grondelle, H. A. Frank, and J. T. M. Kennis. 2003. Light harvesting by carotenoids incorporated into the B850 light-harvesting complex from Rhodobacter sphaeroides R-26.1: excited-state relaxation, ultrafast triplet formation, and energy transfer to bacteriochlorophyll. J. Phys. Chem. B. 107:5642-5649.
59. Papagiannakis, E., M. Vengris, D. S. Larsen, I. H. M. van Stokkum, R. G. Hiller, and R. van Grondelle. 2006. Use of ultrafast dispersed pump-dump-probe and pump-repump-probe spectroscopies to explore the light-induced dynamics of peridinin in solution. J. Phys. Chem. B. 110:512-521.
60. Billsten, H. H., J. X. Pan, S. Sinha, T. Pascher, V. Sundstrom, and T. Polivka. 2005. Excited-state processes in the carotenoid zeaxanthin after excess energy excitation. J. Phys. Chem. A. 109:6852-6859.
61. Bittl, R., E. Schlodder, I. Geisenheimer, W. Lubitz, and R. J. Cogdell. 2001. Transient EPR and absorption studies of carotenoid triplet formation in purple bacterial antenna complexes. J. Phys. Chem. B. 105:5525-5535.
62. Schö del, R., K. D. Irrgang, J. Voigt, and G. Renger. 1998. Rate of carotenoid triplet formation in solubilized light-harvesting complex II (LHCII) from spinach. Biophys. J. 75:3143-3153.