Long-range electron spin-spin interactions in the bacterial photosynthetic reaction center

Donald J. Hirsh, Gary W Brudvig

Research output: Contribution to journalArticle

32 Citations (Scopus)

Abstract

The electron spin-lattice relaxation behavior of the oxidized bacteriochlorophyll a dimer in reaction centers from Rhodobacter sphaeroides has been examined by the method of saturation-recovery EPR over the temperature range 3.8 K ≤ T ≤ 22 K. Its spin-lattice relaxation is nonexponential due to an orientation-dependent dipolar interaction with the non-heme Fe(II) of the reaction center. The saturation-recovery EPR traces were fit by using an equation which models the recovery in terms of a sum of isotropic (scalar) and orientation-dependent (dipolar) rate constants. The center-to-center distance between the bacteriochlorophyll a dimer and the non-heme Fe(II) is 28 Å and it is found that the Heisenberg exchange interaction is too small to make a measurable contribution to the scalar relaxation rate of the oxidized bacteriochlorophyll a dimer. The scalar relaxation rates for the oxidized bacteriochlorophyll a dimer show a T1 temperature dependence which differs significantly from that of model porphyrin radicals. It appears that the unusually rigid protein environment surrounding the bacteriochlorophyll a dimer produces a strong coupling between the spin transitions of the radical and the low-frequency vibrational modes of the lattice. The dipolar rate constants of the oxidized bacteriochlorophyll a dimer and those of the stable tyrosine radical, YD , in Mn-depleted photosystem II show the same temperature dependence. This confirms the assignment of the non-heme Fe(II) as the source of relaxation enhancement for YD in Mn-depleted photosystem II and shows that the spin relaxation properties of the non-heme Fe(II) species in the two proteins are very similar. Using the relative magnitudes of the dipolar rate constants in the two proteins and the distance between the bacteriochlorophyll a dimer and the non-heme Fe(II) in the bacterial reaction center, we calculate a YD -Fe(II) distance of 37 ± 5 Å in photosystem II. This agrees well with the distance predicted from the structure of the bacterial reaction center.

Original languageEnglish
Pages (from-to)13216-13222
Number of pages7
JournalJournal of Physical Chemistry
Volume97
Issue number50
Publication statusPublished - 1993

Fingerprint

Photosynthetic Reaction Center Complex Proteins
Bacteriochlorophylls
electron spin
Dimers
dimers
Electrons
Photosystem II Protein Complex
Rate constants
interactions
Spin-lattice relaxation
recovery
scalars
proteins
Proteins
Recovery
spin-lattice relaxation
Paramagnetic resonance
saturation
temperature dependence
tyrosine

ASJC Scopus subject areas

  • Physical and Theoretical Chemistry

Cite this

Long-range electron spin-spin interactions in the bacterial photosynthetic reaction center. / Hirsh, Donald J.; Brudvig, Gary W.

In: Journal of Physical Chemistry, Vol. 97, No. 50, 1993, p. 13216-13222.

Research output: Contribution to journalArticle

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abstract = "The electron spin-lattice relaxation behavior of the oxidized bacteriochlorophyll a dimer in reaction centers from Rhodobacter sphaeroides has been examined by the method of saturation-recovery EPR over the temperature range 3.8 K ≤ T ≤ 22 K. Its spin-lattice relaxation is nonexponential due to an orientation-dependent dipolar interaction with the non-heme Fe(II) of the reaction center. The saturation-recovery EPR traces were fit by using an equation which models the recovery in terms of a sum of isotropic (scalar) and orientation-dependent (dipolar) rate constants. The center-to-center distance between the bacteriochlorophyll a dimer and the non-heme Fe(II) is 28 {\AA} and it is found that the Heisenberg exchange interaction is too small to make a measurable contribution to the scalar relaxation rate of the oxidized bacteriochlorophyll a dimer. The scalar relaxation rates for the oxidized bacteriochlorophyll a dimer show a T1 temperature dependence which differs significantly from that of model porphyrin radicals. It appears that the unusually rigid protein environment surrounding the bacteriochlorophyll a dimer produces a strong coupling between the spin transitions of the radical and the low-frequency vibrational modes of the lattice. The dipolar rate constants of the oxidized bacteriochlorophyll a dimer and those of the stable tyrosine radical, YD •, in Mn-depleted photosystem II show the same temperature dependence. This confirms the assignment of the non-heme Fe(II) as the source of relaxation enhancement for YD • in Mn-depleted photosystem II and shows that the spin relaxation properties of the non-heme Fe(II) species in the two proteins are very similar. Using the relative magnitudes of the dipolar rate constants in the two proteins and the distance between the bacteriochlorophyll a dimer and the non-heme Fe(II) in the bacterial reaction center, we calculate a YD •-Fe(II) distance of 37 ± 5 {\AA} in photosystem II. This agrees well with the distance predicted from the structure of the bacterial reaction center.",
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AB - The electron spin-lattice relaxation behavior of the oxidized bacteriochlorophyll a dimer in reaction centers from Rhodobacter sphaeroides has been examined by the method of saturation-recovery EPR over the temperature range 3.8 K ≤ T ≤ 22 K. Its spin-lattice relaxation is nonexponential due to an orientation-dependent dipolar interaction with the non-heme Fe(II) of the reaction center. The saturation-recovery EPR traces were fit by using an equation which models the recovery in terms of a sum of isotropic (scalar) and orientation-dependent (dipolar) rate constants. The center-to-center distance between the bacteriochlorophyll a dimer and the non-heme Fe(II) is 28 Å and it is found that the Heisenberg exchange interaction is too small to make a measurable contribution to the scalar relaxation rate of the oxidized bacteriochlorophyll a dimer. The scalar relaxation rates for the oxidized bacteriochlorophyll a dimer show a T1 temperature dependence which differs significantly from that of model porphyrin radicals. It appears that the unusually rigid protein environment surrounding the bacteriochlorophyll a dimer produces a strong coupling between the spin transitions of the radical and the low-frequency vibrational modes of the lattice. The dipolar rate constants of the oxidized bacteriochlorophyll a dimer and those of the stable tyrosine radical, YD •, in Mn-depleted photosystem II show the same temperature dependence. This confirms the assignment of the non-heme Fe(II) as the source of relaxation enhancement for YD • in Mn-depleted photosystem II and shows that the spin relaxation properties of the non-heme Fe(II) species in the two proteins are very similar. Using the relative magnitudes of the dipolar rate constants in the two proteins and the distance between the bacteriochlorophyll a dimer and the non-heme Fe(II) in the bacterial reaction center, we calculate a YD •-Fe(II) distance of 37 ± 5 Å in photosystem II. This agrees well with the distance predicted from the structure of the bacterial reaction center.

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