Thermodynamics of electron transfer in oxygenic photosynthetic reaction centers: Volume change, enthalpy, and entropy of electron-transfer reactions in manganese-depleted photosystem II core complexes

We have previously reported the thermodynamic data of electron transfer in photosystem I using pulsed time-resolved photoacoustics [Hou et al. (2001) Biochemistry 40, 7109-7116]. In the present work, using preparations of purified manganese-depleted photosystem II (PS II) core complexes from Synechocystis sp. PCC 6803, we have measured the DeltaV, DeltaH, and estimated T DeltaS of electron transfer on the time scale of 1 mus. At pH 6.0, the volume contraction of PS II was determined to be -9 +/- 1 Angstrom (3). The thermal efficiency was found to be 52 +/- 5%, which corresponds to an enthalpy change of -0.9 +/- 0.1 eV for the formation of the state P-680+Q(A)(-) from P-680*. An unexpected volume expansion on pulse saturation of PS II was observed, which is reversible in the dark. At pH 9.0, the volume contraction, the thermal efficiency, and the enthalpy change were -3.4 +/- 0.5 Angstrom (3), 37 +/- 7%, and -1.15 +/- 0.13 eV, respectively. The DeltaV of PS II, smaller than that of PS I and bacterial centers, is assigned to electrostriction and analyzed using the Drude-Nernst equation. To explain the small DeltaV for the formation of P-680+Q(A)(-) or Y-Z.Q(A)(-), we propose that fast proton transfer into a polar region is involved in this reaction. Taking the free energy of charge separation of PS II as the difference between the energy of the excited-state P-680* and the difference in the redox potentials of the donor and acceptor, the apparent entropy change (T DeltaS) for charge separation of PS II is calculated to be negative, -0.1 +/- 0.1 eV at pH 6.0 (P-680+Q(A)(-)) and -0.2 +/- 0.15 eV at pH 9.0 (Y-Z.Q(A)(-)) The thermodynamic properties of electron transfer in PS II core reaction centers thus differ considerably from those of bacterial and PS I reaction centers, which have DeltaV of similar to -27 Angstrom (3), DeltaH of similar to -0.4 eV, and T DeltaS of similar to +0.4 eV.