PsbU provides a stable architecture for the oxygen-evolving system in cyanobacterial photosystem II

PsbU is a lumenal peripheral protein in the photosystem II (PS II) complex of cyanobacteria and red algae. It is thought that PsbU is replaced functionally by PsbP or PsbQ in plant chloroplasts. After the discovery of PsbP and PsbQ homologues in cyanobacterial PS II [Thornton et al. (2004) Plant Cell 16, 2164-2175], we investigated the function of PsbU using a psbU deletion mutant (ΔPsbU) of Synechocystis 6803. In contrast to the wild type, ΔPsbU did not grow when both Ca²⁺ and Cl^- were eliminated from the growth medium. When only Ca²⁺ was eliminated, ΔPsbU grew well, whereas when Cl^- was eliminated, the growth rate was highly suppressed. Although ΔPsbU grew normally in the presence of both ions under moderate light, PS II-related disorders were observed as follows. (1) The mutant cells were highly susceptible to photoinhibition. (2) Both the efficiency of light utilization under low irradiance and the chlorophyll-specific maximum rate of oxygen evolution in ΔPsbU cells were 60% lower than those of the wild type. (3) The decay of the S2 state in ΔPsbU cells was decelerated. (4) In isolated PS II complexes from ΔPsbU cells, the amounts of the other three lumenal extrinsic proteins and the electron donation rate were drastically decreased, indicating that the water oxidation system became significantly labile without PsbU. Furthermore, oxygen-evolving activity in ΔPsbU thylakoid membranes was highly suppressed in the absence of Cl ^-, and 60% of the activity was restored by NO₃^- but not by SO₄^2-, indicating that PsbU had functions other than stabilizing Cl^-. On the basis of these results, we conclude that PsbU is crucial for the stable architecture of the water-splitting system to optimize the efficiency of the oxygen evolution process.