Orientation resolving dipolar high-field EPR spectroscopy on disordered solids: II. Structure of spin-correlated radical pairs in photosystem i

A. Savitsky, J. Niklas, J. H. Golbeck, K. Möbius, W. Lubitz

Research output: Contribution to journalArticle

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Abstract

The distance and relative orientation of functional groups within protein domains and their changes during chemical reactions determine the efficiency of biological processes. In this work on electron transfer proteins, we report the results of orientation resolving dipolar high-field EPR spectroscopy on the charge-separated state P700•+A1•- (P700, primary electron donor; A1, phylloquinone electron acceptor) in Photosystem I (PS I). Pulsed high-field EPR spectroscopy at W-band (95 GHz, 3.4 T) with extensions to PELDOR (pulsed electron-electron double resonance) and RIDME (relaxation-induced dipolar modulation enhancement) was utilized to obtain the parameters describing the three-dimensional structure of the laser-flash-induced transient radical pair P700•+A1•- in a frozen solution of deuterated PS I from the cyanobacterium Synechocystis sp. PCC 6803, which is performing oxygenic photosynthesis. The measured distances and relative orientations of the weakly coupled radical ions in the radical pair P700•+A1•- are compared with previously reported geometries and with those of the precursor cofactors P700 and A1 known from X-ray crystallography. Cyclic electron transfer was found to proceed exclusively via the A-branch of the cofactor chain of PS I at cryogenic temperature. The position and orientation of the reduced phylloquinone coincide with those of the precursor, revealing that no substantial orientational changes of the phylloquinone molecule upon charge separation occur. Several distinct orientations of the P700•+ g-tensor axes with respect to the molecular frame of the primary donor were found experimentally, which we explain by several conformational substates of the P700•+ radical structure having slightly different electron spin density distributions.

Original languageEnglish (US)
Pages (from-to)11184-11199
Number of pages16
JournalJournal of Physical Chemistry B
Volume117
Issue number38
DOIs
StatePublished - Sep 26 2013

Fingerprint

phylloquinone
Paramagnetic resonance
Spectroscopy
Vitamin K 1
Electrons
Photosystem I Protein Complex
spectroscopy
electron transfer
electrons
proteins
photosynthesis
polarization (charge separation)
cryogenic temperature
Proteins
electron spin
crystallography
flash
density distribution
chemical reactions
Photosynthesis

All Science Journal Classification (ASJC) codes

  • Physical and Theoretical Chemistry
  • Surfaces, Coatings and Films
  • Materials Chemistry

Cite this

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title = "Orientation resolving dipolar high-field EPR spectroscopy on disordered solids: II. Structure of spin-correlated radical pairs in photosystem i",
abstract = "The distance and relative orientation of functional groups within protein domains and their changes during chemical reactions determine the efficiency of biological processes. In this work on electron transfer proteins, we report the results of orientation resolving dipolar high-field EPR spectroscopy on the charge-separated state P700•+A1•- (P700, primary electron donor; A1, phylloquinone electron acceptor) in Photosystem I (PS I). Pulsed high-field EPR spectroscopy at W-band (95 GHz, 3.4 T) with extensions to PELDOR (pulsed electron-electron double resonance) and RIDME (relaxation-induced dipolar modulation enhancement) was utilized to obtain the parameters describing the three-dimensional structure of the laser-flash-induced transient radical pair P700•+A1•- in a frozen solution of deuterated PS I from the cyanobacterium Synechocystis sp. PCC 6803, which is performing oxygenic photosynthesis. The measured distances and relative orientations of the weakly coupled radical ions in the radical pair P700•+A1•- are compared with previously reported geometries and with those of the precursor cofactors P700 and A1 known from X-ray crystallography. Cyclic electron transfer was found to proceed exclusively via the A-branch of the cofactor chain of PS I at cryogenic temperature. The position and orientation of the reduced phylloquinone coincide with those of the precursor, revealing that no substantial orientational changes of the phylloquinone molecule upon charge separation occur. Several distinct orientations of the P700•+ g-tensor axes with respect to the molecular frame of the primary donor were found experimentally, which we explain by several conformational substates of the P700•+ radical structure having slightly different electron spin density distributions.",
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Orientation resolving dipolar high-field EPR spectroscopy on disordered solids : II. Structure of spin-correlated radical pairs in photosystem i. / Savitsky, A.; Niklas, J.; Golbeck, J. H.; Möbius, K.; Lubitz, W.

In: Journal of Physical Chemistry B, Vol. 117, No. 38, 26.09.2013, p. 11184-11199.

Research output: Contribution to journalArticle

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T2 - II. Structure of spin-correlated radical pairs in photosystem i

AU - Savitsky, A.

AU - Niklas, J.

AU - Golbeck, J. H.

AU - Möbius, K.

AU - Lubitz, W.

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