Analysis of the Reaction Coordinate of Photosynthetic Water Oxidation by Kinetic Measurements of 355 nm Absorption Changes at Different Temperatures in Photosystem II Preparations Suspended in Either H₂O or D₂O

Abstract

Flash-induced absorption changes at 355 nm were measured at different temperatures within the range of 2 degrees C </= theta </= 25 degrees C in dark-adapted PS II core complexes from spinach [O2 evolution rate: 1500 +/- 100 micromol of O2 (mg of Chl)-1 h-1] that were dissolved either in H2O- or in D2O-containing buffer. Comparative measurements were performed at 20 degrees C in H2O- or D2O-containing suspensions of PS II membrane fragments [O2 evolution rate: 600 +/- 40 micromol of O2 (mg of Chl)-1 h-1]. The results obtained reveal the following: (a) The activation energies of the individual redox steps in the water oxidizing complex (WOC) are dependent on the redox state Si with EA(S1-->S2) = 14 kJ/mol, EA(S2-->S3) = 35 kJ/mol, and EA(S3-->-->S0 + O2) = 21 kJ/mol for theta > 11 degrees C, 67 kJ/mol for theta < 11 degrees C in PS II core complexes dissolved in H2O; (b) replacement of exchangeable protons by deuterons causes only minor changes (</=15%) of the activation energies; and (c) the rate constants of these reactions in PS II core complexes are characterized by H/D isotope ratios, ki(H)/ki(D), of 1.6, 2.3, and 1.5 for the transitions S1 --> S2, S2 --> S3, and S3 -->--> S0 + O2, respectively. The corresponding values of PS II membrane fragments are 1.3, 1.3, and 1. 4. Based on these results and corresponding EA data reported in the literature for PS II membrane fragments from spinach [Renger, G., & Hanssum, B. (1992) FEBS Lett. 299, 28-32] and PS II particles from the thermophilic cyanobacterium Synechococcus vulcanus Copeland [Koike, H., Hanssum, B., Inoue, Y., & Renger, G. (1987) Biochim. Biophys. Acta 893, 524-533], the reaction coordinate of the redox sequence in the WOC is inferred to be almost invariant to the evolutionary development from cyanobacteria to higher plants. Furthermore, the rather high activation energy of the S2 --> S3 transition provides evidence for a significant structural change coupled with this reaction. Implications for the mechanism of photosynthetic water oxidation are discussed.

Time-resolved vibrational spectroscopy detects protein-based intermediates in the photosynthetic oxygen-evolving cycle

“…Through x-ray measurements, similar half-times were reported and assigned to Mn redox reactions (11), except that a lag time of 200 s was detected before Mn reduction during the S 4 -to-S 0 transition. The 2 H 2 O isotope effects on the S state transitions have been reported in the range of 1.3-to 1.4-fold (38).…”

Tyrosine-Z in Oxygen-Evolving Photosystem II: A Hydrogen-Bonded Tyrosinate

“…The activation energy was very low, about 10 kJ mol -1 (37,38). Taking the gross kinetical ruler of Moser et al (82) at face value and using the observed rate of electron transfer between Y Z and P 680 + , about 5 × 10 7 s -1 in oxygen-evolving PSII (8,37,(83)(84)(85)(86), we calculated a reorganization energy of about 0.5 eV (123,124). An even higher reorganization energy, 0.7 eV, has been obtained, for instance, for the electron transfer (in ∼200 ps) from bacteriopheophytin to Q A in the bacterial reaction center (see ref 82 and references therein).…”

Structural Change of the Mn Cluster during the S2→S3 State Transition of the Oxygen-Evolving Complex of Photosystem II. Does It Reflect the Onset of Water/Substrate Oxidation? Determination by Mn X-ray Absorption Spectroscopy

“…[67][68][69] The activation energy increases by a factor of about 3 for S 2 →S 3 compared to that for the S 1 →S 2 transition. The authors attribute this marked difference in activation energy to the involvement of a significant structural change in the S 2 →S 3 transition that is absent in the S 1 →S 2 transition.…”