The catalytic center of the oxygen-evolving complex (OEC) in the oxygenic photosynthetic organisms carries out one of the most important bioenergetic reactions - water oxidation and molecular oxygen synthesis. The catalytic center consists of 4 Mn and 1 Ca2+ cations connected to each other by 5 oxygen bridges [1,2]. Metal cluster have four molecules of water, two of which are bound to Mn4 cation and the other two bound to Ca2+ cation. One of the Ca2+-bound water molecules is presumably a substrate molecule, which is involved in formation of molecular oxygen [3,4] although the mechanism of Ca2+ function in water oxidation might be different. For example, Ca2+ can be responsible for an “adjustment” of the redox potential of a manganese cluster [[5], [6], [7]].

The Ca2+ cation can be extracted from OEC of photosystem II (PSII) with high ionic strength medium (1–2 M NaCl) [8] or low pH citrate buffer [9]. This procedure is accompanied by a loss of oxygen-evolving activity: the residual rate of oxygen evolution is about 12%. The activity of Ca-depleted PSII membranes (PSII(Ca)) can be restored up to 70% by addition of Ca2+ in high concentrations (10–30 mM) [10]. A number of metal cations have been investigated as a substitute for Ca2+ in OEC [11]. However, the only metal ion which could functionally substitute Ca2+ is Sr2+ [12]. The binding of some other metal ions, including lanthanides (Ln3+) [13,14] and Cd2+ [15], to the Ca-binding site is competitive with Ca2+. Lanthanides irreversibly bind to the Ca-binding site in intact membrane preparations of the PSII, displacing Ca2+ cation from the OEC [13], as well as to free Ca-binding site in Ca-depleted PSII membranes [14].

However, the mechanism of interaction of lanthanides cations with PSII membranes might be more complex than simply binding to the Ca-binding site of the OEC. The essence is that the PSII contains, in addition to Ca2+ cation, 4 Mn cations, which can be extracted from OEC together with Ca2+ cation and extrinsic proteins. The Mn-depleted PSII samples (PSII(Mn)) contain single Mn-binding site [16,17], which binds Mn2+ cations with high efficiency. This high-affinity site (HAS) is located at the position denoted by Mn4 [1] in the native crystal structure. The HAS was assigned to axial ligands Asp170 and Glu333 in the D1 polypeptide of the native PSII membranes [17]. This site can presumably bind Fe2+ cations with a comparable to Mn2+ efficiency [18]. Recently, a detailed study of the photoactivation process in cyanobacterial membranes led the authors to a conclusion that there is a second Mn-binding site in the apo-PSII membranes [19]. This was confirmed by Mino and Asada (2022) using the pulsed electron–electron double resonance [20]. The authors suggested that the position between Asp170 and Glu189 in the D1 polypeptide is a good candidate for the initial high-affinity site for photoactivation.

In our previous work [21], we found that La3+ and Tb3+ cations effectively inhibited the reduction of artificial electron acceptor 2,6-dichlorophenolindophenol (DCPIP) supported by oxidation of Mn2+ cations at the Mn-binding HAS in the Mn-depleted PSII membranes. The Ki values are equal to 2 μM for Tb3+ and 8 μM for La3+, which is close to the concentration of Fe2+ cations (3 μM) that blocks the oxidation of Mn2+ cations through the HAS [18]. In contrast, the Ki inhibition of the Ca-binding site in PSII(Ca) membranes (200 μM) is much greater [14]. These facts suggest that the lanthanide cations inhibit the oxidation of Mn2+ cations bound to the HAS, blocking the binding of Mn2+ cations, which is similar to the Mn2+ oxidation blocking by iron cations [18]. In this work, we continued to study the mechanism of Ln3+ cations interaction with the HAS by EPR method. The obtained results confirm the fact of highly effective binding of lanthanide cations to the Mn-binding HAS in the PSII(Mn) membrane preparations. We found that irreversible binding of the lanthanide cation to the Ca-binding site in the Ca-depleted PSII membranes leads to a partial inhibition of the high-affinity Mn-binding site.