High-spin states (S≥5/2) of the photosystem II manganese complex

The Mn-4 complex which is involved in water oxidation in photosystem II (PSII) is known to exhibit two types of EPR signals in the S-2 state, one of the five redox states of the enzyme cycle: either a multiline signal (S = 1/2) or a signal at g = 4.1 (S = 3/2 or S = 5/2), The S = 1/2 state can be converted to that responsible for the g = 4.1 signal upon the absorption of near-infrared (IR) light [Boussac, A., Girerd, J.-J., and Rutherford, A. W. (1996) Biochemistry 35, 6984-6989]. It is shown here that a third state gives rise to signals at g = 10 and 6. This state is formed by LR illumination of the S = 1/2 state at 65 K, a temperature where LR illumination leads to the loss of the S = 1/2 signal but to no formation of the g = 4.1 state. On the basis of the corresponding decrease of the S = 1/2 state, the new state can be trapped in similar to 40% of the PSII centers. Wanning of the sample above 65 K, in the dark, leads to the loss of the g = 10 and 6 resonances with the corresponding appearance of the g = 4.1 signal. It is suggested that the IR-induced conversion of the S = 1/2 state into the g = 4.1 state at 150 K involves the transient formation of the new state, The new state is attributed to a S = 5/2 State of the Mn-4 complex (although a S value > 5/2 is also a possibility). Spectral simulations indicate an E/D ratio of -0.05 with \D\ less than or equal to 1 cm(-1). The resonances at g = 10 and 6 correspond to the g(z) of the +/-5/2 and +/-3/2 transition, respectively. The temperature-dependent conversion of this S = 5/2 State into the g = 4.1 state is proposed to be due to relaxation of the ligand environment around the Mn-4 cluster that leads to a change in the zero field splitting parameters, assuming an S = 5/2 value for the g = 4.1 state. The new form of the S-2 state reported here may explain some earlier data where the S-2 State was present and yet not detectable as either a S = 1/2 or a g = 4.1 EPR signal.