Conversion of the g = 4.1 EPR signal to the multiline conformation during the S2 to S3 transition of the oxygen evolving complex of Photosystem II

The oxygen evolving complex of Photosystem II undergoes four light-induced oxidation transitions, S0–S1,…,S3–(S4)S0 during its catalytic cycle. The oxidizing equivalents are stored at a (Mn)4Ca cluster, the site of water oxidation. EPR spectroscopy has yielded valuable information on the S states. S2 shows a notable heterogeneity with two spectral forms; a g = 2 (S = 1/2) multiline, and a g = 4.1 (S = 5/2) signal. These oscillate in parallel during the period-four cycle. Cyanobacteria show only the multiline signal, but upon advancement to S3 they exhibit the same characteristic g = 10 (S = 3) absorption with plant preparations, implying that this latter signal results from the multiline configuration. The fate of the g = 4.1 conformation during advancement to S3 is accordingly unknown. We searched for light-induced transient changes in the EPR spectra at temperatures below and above the half-inhibition temperature for the S2 to S3 transition (ca 230 K). We observed that, above about 220 K the g = 4.1 signal converts to a multiline form prior to advancement to S3. We cannot exclude that the conversion results from visible-light excitation of the Mn cluster itself. The fact however, that the conversion coincides with the onset of the S2 to S3 transition, suggests that it is triggered by the charge-separation process, possibly the oxidation of tyr Z and the accompanying proton relocations. It therefore appears that a configuration of (Mn)4Ca with a low-spin ground state advances to S3.