Pulsed high-frequency EPR study on the location of carotenoid and chlorophyll cation radicals in photosystem II

K. V. Lakshmi, Oleg G. Poluektov, Michael J. Reifler, Arlene M. Wagner, Marion C. Thurnauer, Gary W. Brudvig

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Abstract

When the primary electron-donation pathway from the water-oxidation complex in photosystem II (PS II) is inhibited, chlorophyll (ChlZ and ChlD), β-carotene (Car) and cytochrome b559 are alternate electron donors that are believed to function in a photoprotection mechanism. Previous studies have demonstrated that high-frequency EPR spectroscopy (at 130 GHz), together with deuteration of PS II, yields resolved Car+ and Chl+ EPR signals (Lakshmi et al. J. Phys. Chem. B 2000, 104, 10 445-10 448). The present study describes the use of pulsed high-frequency EPR spectroscopy to measure the location of the carotenoid and chlorophyll radicals relative to other paramagnetic cofactors in Synechococcus lividus PS II. The spin-lattice relaxation rates of the Car+ and Chl+ radicals are measured in manganese-depleted and manganese-depleted, cyanide-treated PS II; in these samples, the non-heme Fe(II) is high-spin (S = 2) and low-spin (S = 0), respectively. The Car+ and Chl+ radicals exhibit dipolar-enhanced relaxation rates in the presence of high-spin (S = 2) Fe(II) that are eliminated when the Fe(II) is low-spin (S = 0). The relaxation enhancements of the Car+ and Chl+ by the non-heme Fe(II) are smaller than the relaxation enhancement of TyrD· and P865 + by the non-heme Fe(II) in PS II and in the reaction center from Rhodobacter sphaeroides, respectively, indicating that the Car+-Fe(II) and Chl+-Fe(II) distances are greater than the known TyrD·-Fe(II) and P865 +-Fe(II) distances. The Car+ radical exhibits a greater relaxation enhancement by Fe(II) than the Chl+ radical, consistent with Car being an earlier electron donor to P680 + than Chl. On the basis of the distance estimates obtained in the present study and by analogy to carotenoid-binding sites in other pigment-protein complexes, possible binding sites are discussed for the Car cofactors in PS II. The relative location of Car+ and Chl+ radicals determined in this study provides valuable insight into the sequence of electron transfers in the alternate electron-donation pathways of PS II.

Original languageEnglish
Pages (from-to)5005-5014
Number of pages10
JournalJournal of the American Chemical Society
Volume125
Issue number17
Publication statusPublished - Apr 30 2003

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Photosystem II Protein Complex
Chlorophyll
Carotenoids
Paramagnetic resonance
Cations
Positive ions
Electrons
Binding sites
Manganese
Spectrum Analysis
Binding Sites
Spectroscopy
Synechococcus
Proteins
Rhodobacter sphaeroides
Spin-lattice relaxation
Cyanides
Pigments

ASJC Scopus subject areas

  • Chemistry(all)

Cite this

Lakshmi, K. V., Poluektov, O. G., Reifler, M. J., Wagner, A. M., Thurnauer, M. C., & Brudvig, G. W. (2003). Pulsed high-frequency EPR study on the location of carotenoid and chlorophyll cation radicals in photosystem II. Journal of the American Chemical Society, 125(17), 5005-5014.

Pulsed high-frequency EPR study on the location of carotenoid and chlorophyll cation radicals in photosystem II. / Lakshmi, K. V.; Poluektov, Oleg G.; Reifler, Michael J.; Wagner, Arlene M.; Thurnauer, Marion C.; Brudvig, Gary W.

In: Journal of the American Chemical Society, Vol. 125, No. 17, 30.04.2003, p. 5005-5014.

Research output: Contribution to journalArticle

Lakshmi, KV, Poluektov, OG, Reifler, MJ, Wagner, AM, Thurnauer, MC & Brudvig, GW 2003, 'Pulsed high-frequency EPR study on the location of carotenoid and chlorophyll cation radicals in photosystem II', Journal of the American Chemical Society, vol. 125, no. 17, pp. 5005-5014.
Lakshmi, K. V. ; Poluektov, Oleg G. ; Reifler, Michael J. ; Wagner, Arlene M. ; Thurnauer, Marion C. ; Brudvig, Gary W. / Pulsed high-frequency EPR study on the location of carotenoid and chlorophyll cation radicals in photosystem II. In: Journal of the American Chemical Society. 2003 ; Vol. 125, No. 17. pp. 5005-5014.
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N2 - When the primary electron-donation pathway from the water-oxidation complex in photosystem II (PS II) is inhibited, chlorophyll (ChlZ and ChlD), β-carotene (Car) and cytochrome b559 are alternate electron donors that are believed to function in a photoprotection mechanism. Previous studies have demonstrated that high-frequency EPR spectroscopy (at 130 GHz), together with deuteration of PS II, yields resolved Car+ and Chl+ EPR signals (Lakshmi et al. J. Phys. Chem. B 2000, 104, 10 445-10 448). The present study describes the use of pulsed high-frequency EPR spectroscopy to measure the location of the carotenoid and chlorophyll radicals relative to other paramagnetic cofactors in Synechococcus lividus PS II. The spin-lattice relaxation rates of the Car+ and Chl+ radicals are measured in manganese-depleted and manganese-depleted, cyanide-treated PS II; in these samples, the non-heme Fe(II) is high-spin (S = 2) and low-spin (S = 0), respectively. The Car+ and Chl+ radicals exhibit dipolar-enhanced relaxation rates in the presence of high-spin (S = 2) Fe(II) that are eliminated when the Fe(II) is low-spin (S = 0). The relaxation enhancements of the Car+ and Chl+ by the non-heme Fe(II) are smaller than the relaxation enhancement of TyrD· and P865 + by the non-heme Fe(II) in PS II and in the reaction center from Rhodobacter sphaeroides, respectively, indicating that the Car+-Fe(II) and Chl+-Fe(II) distances are greater than the known TyrD·-Fe(II) and P865 +-Fe(II) distances. The Car+ radical exhibits a greater relaxation enhancement by Fe(II) than the Chl+ radical, consistent with Car being an earlier electron donor to P680 + than Chl. On the basis of the distance estimates obtained in the present study and by analogy to carotenoid-binding sites in other pigment-protein complexes, possible binding sites are discussed for the Car cofactors in PS II. The relative location of Car+ and Chl+ radicals determined in this study provides valuable insight into the sequence of electron transfers in the alternate electron-donation pathways of PS II.

AB - When the primary electron-donation pathway from the water-oxidation complex in photosystem II (PS II) is inhibited, chlorophyll (ChlZ and ChlD), β-carotene (Car) and cytochrome b559 are alternate electron donors that are believed to function in a photoprotection mechanism. Previous studies have demonstrated that high-frequency EPR spectroscopy (at 130 GHz), together with deuteration of PS II, yields resolved Car+ and Chl+ EPR signals (Lakshmi et al. J. Phys. Chem. B 2000, 104, 10 445-10 448). The present study describes the use of pulsed high-frequency EPR spectroscopy to measure the location of the carotenoid and chlorophyll radicals relative to other paramagnetic cofactors in Synechococcus lividus PS II. The spin-lattice relaxation rates of the Car+ and Chl+ radicals are measured in manganese-depleted and manganese-depleted, cyanide-treated PS II; in these samples, the non-heme Fe(II) is high-spin (S = 2) and low-spin (S = 0), respectively. The Car+ and Chl+ radicals exhibit dipolar-enhanced relaxation rates in the presence of high-spin (S = 2) Fe(II) that are eliminated when the Fe(II) is low-spin (S = 0). The relaxation enhancements of the Car+ and Chl+ by the non-heme Fe(II) are smaller than the relaxation enhancement of TyrD· and P865 + by the non-heme Fe(II) in PS II and in the reaction center from Rhodobacter sphaeroides, respectively, indicating that the Car+-Fe(II) and Chl+-Fe(II) distances are greater than the known TyrD·-Fe(II) and P865 +-Fe(II) distances. The Car+ radical exhibits a greater relaxation enhancement by Fe(II) than the Chl+ radical, consistent with Car being an earlier electron donor to P680 + than Chl. On the basis of the distance estimates obtained in the present study and by analogy to carotenoid-binding sites in other pigment-protein complexes, possible binding sites are discussed for the Car cofactors in PS II. The relative location of Car+ and Chl+ radicals determined in this study provides valuable insight into the sequence of electron transfers in the alternate electron-donation pathways of PS II.

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