A Structural Model for the Charge Separated State in Photosystem I from the Orientation of the Magnetic Interaction Tensors

Abstract

The charge separated state P 700•+ A 1•-(P 700 ) primary electron donor, A 1 ) phylloquinone electron acceptor) in photosystem I of oxygenic photosynthesis has been investigated by EPR spectroscopy in frozen solution and single crystals. The transient EPR spectra of P 700•+ A 1 •recorded in frozen solution of fully deuterated samples at X-, Q-, and W-band frequencies are shown to contain sufficient information to yield the orientation of the g-tensors of both A 1•and P 700•+ with respect to the axis connecting both spins. So far incomplete information on the orientation of A 1•relative to the membrane plane has been complemented by data from time-resolved EPR on single crystals measured at Q-band. The phylloquinone headgroup orientation evaluated from the EPR data in the charge-separated state P 700•+ A 1 •is compared with the presently available X-ray structural model. The g-tensor of P 700 •+ has also been determined from cw-EPR experiments at W-band on single crystals, independent of the orientational data of the P 700 •+ g-tensor from the time-resolved EPR experiments.The direction of the principal axes of g(P 700•+ ) differ from the molecular axes system of the chlorophylls comprising P 700 as found previously in the case of P 865•+ in bacterial reaction centers. The implications of the complete structural model from the A 1 •and P 700•+ molecular magnetic interaction tensors in the active charge separated state P 700•+ A 1 •in PS I are discussed.

Recruitment of a Foreign Quinone into the A1 Site of Photosystem I

“…Note that the total spectral width is lower for P 700 ⅐ϩ AQ ⅐ Ϫ . This is consistent with the smaller g-tensor anisotropy of AQ and the absence of the partially resolved methyl hyperfine coupling (hfc), which represents a major contribution to the spectral width of the X-band spectrum of P 700 ⅐ϩ PhQ ⅐ Ϫ in native PS I (37)(38)(39)(40). The methyl hfc is strongest along the C-CH 3 bond, which is close to the principal y axis of the PhQ ⅐ Ϫ g-tensor.…”

“…These differences provide a sensitive indicator for the asymmetry of the spin density distribution in the different environments, and from this observed asymmetry the asymmetry of hydrogen bonding can be deduced (20,41,42). A dominant hydrogen bond to the carbonyl group ortho to the phytyl tail and meta to the methyl group leads to an increased hfc constant for the methyl protons (35,39,40). In the A 1 site, AQ is expected to bind with the same highly asymmetric bond scheme as PhQ.…”

Redox Potential of Quinones in Both Electron Transfer Branches of Photosystem I

“…Time-resolved EPR spectroscopy identified the appearance of this radical state A 1 Ϫ with the charge-separated state P700 ϩ A 1 Ϫ (69). However, the measurements were sensitive only for times longer than a few 10 Ϫ8 s such that a faster phase observed in UV-visible spectroscopic studies could be not detected (70). In conclusion, both branches are probably ET active, and the redox potential difference by 155 mV between A 1A and A 1B leads to a biphasic ET process, which is fast in the B-branch and slow in the A-branch.…”

DFT insight into o-semiquinone radicals and Ca2+ ion interaction: structure, g tensor, and stability

“…Electron paramagnetic resonance (EPR) spectroscopy has established its important position in investigation of semiquinone radicals in laboratory conditions and in their natural surroundings [8][9][10][11][12][13][14]. Also, the formation of a complex between diamagnetic metal ions and semiquinone radicals can be efficiently investigated using the EPR techniques since the g and A tensors are sensitive to the radical-metal ions interaction [5,6,[15][16][17][18].…”