Location of chlorophyll(Z) in photosystem II

D. Koulougliotis, J. B. Innes, Gary W Brudvig

Research output: Contribution to journalArticle

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Abstract

Saturation-recovery and progressive microwave power saturation EPR spectroscopies have been used to probe the location of the chlorophyll(Z)+ (Chl(Z)+) radical species in Mn-depleted photosystem II (PSII). The spin- lattice relaxation transients of Chl(Z)+ were non-single-exponential due to a dipole-dipole interaction with one of the other paramagnetic centers in PSII. Measurements on CN--treated, Mn-depleted PSII membrane samples, in which the non-heme Fe(II) is converted into its low-spin, diamagnetic form, confirmed that the non-heme Fe(II) caused the dipolar relaxation enhancement of Chl(Z)+. The saturation-recovery EPR data were fit to a dipolar model [Hirsh, D. J., Beck, W. F., Innes, J. B., and Brudvig, G. W. (1992) Biochemistry 31, 532] which takes into account the isotropic (scalar) and orientation-dependent (dipolar) contributions to the spin-lattice relaxation of the radical. The temperature dependence of the dipolar rate constants of Chl(Z)+ was identical to the temperature dependencies recently observed for the stable tyrosine radical, Y(D)·, and the special pair bacteriochlorophyll radical, (BChla)2 +, in PSII and in reaction centers from Rhodobacter sphaeroides, respectively. Because the non-heme Fe(II) is known to cause a dipolar relaxation enhancement of the radicals in both of the latter cases, this result provides further evidence that the non-heme Fe(II) causes the dipolar relaxation enhancement of Chl(Z)+ and, moreover, demonstrates that the magnetic properties of the non-heme Fe(II) in PSII and in reaction centers from Rhodobacter sphaeroides are very similar. By using the known Fe(II)-(BChla)2 + distance for calibration, we estimate the Fe(II)-Chl(Z)+ distance to be 39.5 ± 2.5 Å. The theory of dipolar relaxation enhancement of a free radical caused by exogenous Dy3+ complexes [Innes, J. B., and Brudvig, G. W. (1989) Biochemistry 28, 1116] has also been applied to determine the location of Chl(Z)+ relative to the PSII protein surfaces. Chl(Z)+ was found to be located at approximately equal distances from both the luminal and stromal protein surfaces in extrinsic polypeptide-depleted PSII membranes. These results provide the first direct evidence against the assignment of Chl(Z) to a Chl monomer analogous to the 'voyeur' BChl in the bacterial reaction center and point to histidines-118 in the D1 and D2 proteins as potential ligands of Chl(Z).

Original languageEnglish
Pages (from-to)11814-11822
Number of pages9
JournalBiochemistry
Volume33
Issue number39
DOIs
Publication statusPublished - 1994

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Photosystem II Protein Complex
Chlorophyll
Bacteriochlorophylls
Rhodobacter sphaeroides
Biochemistry
Spin-lattice relaxation
Paramagnetic resonance
Membrane Proteins
Membranes
Recovery
Temperature
Microwaves
Histidine
Calibration
Free Radicals
Rate constants
Spectrum Analysis
Magnetic properties
Monomers
Spectroscopy

ASJC Scopus subject areas

  • Biochemistry

Cite this

Location of chlorophyll(Z) in photosystem II. / Koulougliotis, D.; Innes, J. B.; Brudvig, Gary W.

In: Biochemistry, Vol. 33, No. 39, 1994, p. 11814-11822.

Research output: Contribution to journalArticle

Koulougliotis, D, Innes, JB & Brudvig, GW 1994, 'Location of chlorophyll(Z) in photosystem II', Biochemistry, vol. 33, no. 39, pp. 11814-11822. https://doi.org/10.1021/bi00205a018
Koulougliotis, D. ; Innes, J. B. ; Brudvig, Gary W. / Location of chlorophyll(Z) in photosystem II. In: Biochemistry. 1994 ; Vol. 33, No. 39. pp. 11814-11822.
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N2 - Saturation-recovery and progressive microwave power saturation EPR spectroscopies have been used to probe the location of the chlorophyll(Z)+ (Chl(Z)+) radical species in Mn-depleted photosystem II (PSII). The spin- lattice relaxation transients of Chl(Z)+ were non-single-exponential due to a dipole-dipole interaction with one of the other paramagnetic centers in PSII. Measurements on CN--treated, Mn-depleted PSII membrane samples, in which the non-heme Fe(II) is converted into its low-spin, diamagnetic form, confirmed that the non-heme Fe(II) caused the dipolar relaxation enhancement of Chl(Z)+. The saturation-recovery EPR data were fit to a dipolar model [Hirsh, D. J., Beck, W. F., Innes, J. B., and Brudvig, G. W. (1992) Biochemistry 31, 532] which takes into account the isotropic (scalar) and orientation-dependent (dipolar) contributions to the spin-lattice relaxation of the radical. The temperature dependence of the dipolar rate constants of Chl(Z)+ was identical to the temperature dependencies recently observed for the stable tyrosine radical, Y(D)·, and the special pair bacteriochlorophyll radical, (BChla)2 +, in PSII and in reaction centers from Rhodobacter sphaeroides, respectively. Because the non-heme Fe(II) is known to cause a dipolar relaxation enhancement of the radicals in both of the latter cases, this result provides further evidence that the non-heme Fe(II) causes the dipolar relaxation enhancement of Chl(Z)+ and, moreover, demonstrates that the magnetic properties of the non-heme Fe(II) in PSII and in reaction centers from Rhodobacter sphaeroides are very similar. By using the known Fe(II)-(BChla)2 + distance for calibration, we estimate the Fe(II)-Chl(Z)+ distance to be 39.5 ± 2.5 Å. The theory of dipolar relaxation enhancement of a free radical caused by exogenous Dy3+ complexes [Innes, J. B., and Brudvig, G. W. (1989) Biochemistry 28, 1116] has also been applied to determine the location of Chl(Z)+ relative to the PSII protein surfaces. Chl(Z)+ was found to be located at approximately equal distances from both the luminal and stromal protein surfaces in extrinsic polypeptide-depleted PSII membranes. These results provide the first direct evidence against the assignment of Chl(Z) to a Chl monomer analogous to the 'voyeur' BChl in the bacterial reaction center and point to histidines-118 in the D1 and D2 proteins as potential ligands of Chl(Z).

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