Competitive interaction of Mn(II) and Fe(II) cations with the high-affinity Mn-binding site of the photosystem II: evolutionary aspect.

The evolutionary origin of the oxygen-evolving complex (OEC) in the photosystem II (PSII) is still unclear, as is the nature of electron source for the photosystem before the OEC had appeared. Johnson et al. (in PNAS 110:11238, 2013) speculated that Mn(II) cations were the source of electrons for transitional photosystems. However, Archean oceans also contained Fe(II) cations at concentrations comparable or higher than that of Mn(II). Fe(II) cations can bind to the high-affinity (НА) Mn-binding site in the OEC (Semin et al. in Biochemistry 41:5854, 2002). Now we have investigated the competitive interaction of Mn(II) and Fe(II) cations with the HA site in the Mn-depleted PSII membranes (PSII[-Mn]). Fe cations, oxidized under illumination, bind strongly to the HA site and, thus, prevent the interaction of Mn(II) with this site. If the Mn(II) and Fe(II) cations, at relatively equal concentration, are simultaneously present in the buffer, together with PSII(-Mn) membranes, there is competition between these two cations for the binding site, which manifests itself in partial inhibition of the Mn(II) oxidation and the blocking of the HA site by Fe(II) cations. If the concentration of Fe(II) cations is several times higher than the concentration of Mn(II), the HA site is completely blocked and the oxidation of Mn(II) cations is inhibited; under saturating light, the effectiveness of this inhibitory effect increases. This may be due to the generation of H2O2 on the acceptor side of the photosystem, which significantly accelerates the rate of the turnover reaction of Mn(II) on the HA site.