The Psb27 Assembly Factor and Histidine-252 of the D1 Protein Modify Energy Transfer to Photosystem II in Synechocystis sp. PCC 6803

Photosystem II (PS II) is responsible for light-driven water splitting in oxygenic photosynthesis. The Psb27 protein, an assembly factor required for biogenesis of PS II, is found associated with hydrophilic regions of the CP43 core antenna protein in the thylakoid lumen. CP43 and the D1 reaction center protein provide ligands for the Mn4CaO5 oxygen-evolving complex (OEC). Release of Psb27 coincides with conformational changes that enable successful light-driven assembly of the OEC. This stage in biogenesis also requires changes to allow electron transfer between plastoquinone electron acceptors on the opposite side of the membrane. We have introduced charge-swap mutations to target the binding of Psb27 to CP43 during assembly. Here, we show that perturbation of the Psb27-CP43 interaction results in elevated fluorescence, indicating enhanced energy transfer to PS II in fully assembled complexes. In a Psb27:Arg78 to Glu mutant, D1:His252 spontaneously mutated to Gln. D1:His252 is in the DE loop that contributes to quinone binding and protonation. Mutations targeting D1:His252 produced mutants with elevated PS II-specific fluorescence that exceeded that observed in our Psb27 mutants and this was attenuated when the Psb27 charge-swap mutations were introduced into H252Q cells. Perturbation of Psb27 binding to CP43 therefore modified structural changes on the opposite side of the membrane resulting from mutation of D1:His252. The peripheral phycobilisome antenna is lost during thylakoid isolation and thylakoids from our mutants did not display the increased PS II-specific fluorescence. Hence Psb27 binding to CP43 during photoassembly of the OEC can modify phycobilisome-dependent energy transfer into PS II.