Electronic interactions between iron and the bound semiquinones in bacterial photosynthesis. EPR spectroscopy of oriented cells of Rhodopseudomonas viridis

G. Charles Dismukes, Harry A. Frank, Richard Friesner, Kenneth Sauer

Research output: Contribution to journalArticlepeer-review

44 Citations (Scopus)

Abstract

Electron paramagnetic resonance (EPR) spectroscopy of the iron-semiquinone complex in photosynthetic bacterial cells and chromatophores of Rhodopseudomonas viridis is reported. Magnetic fields are used to orient the prolate ellipsoidal-shaped cells which possess a highly ordered internal structure, consisting of concentric, nearly cylindrical membranes. The field-oriented suspension of cells exhibits a highly dichroic EPR signal for the iron-semiquinone complex, showing that the iron possesses a low-symmetry ligand field and exists in a preferred orientation within the native reaction-center membrane complex. The EPR spectrum is analyzed utilizing a spin hamiltonian formalism to extract physical information describing the electronic structure of the iron and the nature of its interaction with the semiquinones. Exact numerical solutions and analytical expressions for the transition frequencies and intensities derived from a perturbation theory expansion are presented, and a computer-simulated spectrum is given. It has been found that, for a model which assumes no preferred orientation within the plane of the membranes, the orientation of the Fe2+ ligand axis of largest zero-field splitting (Z, the principal magnetic axis) is titled 64±6° from the membrane normal. The ligand field for Fe2+ has low symmetry, with zero-field splitting parameters of |D1|=7.0±1.3 cm-1 and |E1|=1.7±0.5 cm-1 and | E1 D1|=0.26 for the redox state Q1-Fe2+Q2-. The rhombic character of the ligand field is increased in the redox state Q1Fe2+Q-2, where 0.33>| E2 D2|>0.26. This indicates that the redox state of the quinones can influence the ligand field symmetry and splitting of the Fe2+. There exists an electron-spin exchange interaction between Fe2+ and Q-1 and Q-2, having magnitudes |J1|=0.12±0.03 cm-1 and |J2|{reversed tilde equals}0.06 cm-1, respectively. Such weak interactions indicate that a proper electronic picture of the complex is as a pair of immobilized semiquinone radicals having very little orbital overlap (probably fostered by superexchange) with the Fe2+ orbitals. The exchange interaction is analyzed by comparison with model systems of paramagnetic metals and free radicals to indicate an absence of direct coordination between Fe2+ and Q-1 and Q-2. Selective line-broadening of some of the EPR transitions, involving Q- coupling to the magnetic sublevels of the Fe2+ ground state, is interpreted as arising from an electron-electron dipolar interaction. Analysis of this line-broadening indicates a distance of 6.2-7.8 Ȧ between Fe2+ and Q-1, thus placing Q1 outside the immediate coordination shell of Fe2+.

Original languageEnglish
Pages (from-to)253-271
Number of pages19
JournalBBA - Bioenergetics
Volume764
Issue number3
DOIs
Publication statusPublished - Mar 30 1984

Keywords

  • (Rps. viridis)
  • Bacterial photosynthesis
  • ESR
  • Electron transport
  • Iron - semiquinone

ASJC Scopus subject areas

  • Biophysics
  • Biochemistry
  • Cell Biology

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