In plants, algae and cyanobacteria, Photosystem II (PSII) catalyzes the light-
driven splitting of water at a protein-bound Mn4CaO5-cluster, the water-
oxidizing complex (WOC). In the photosynthetic organisms, the light-driven
formation of the WOC from dissolved metal ions is a key process because it is
essential in both initial activation and continuous repair of PSII. Structural
information is required for understanding of this chaperone-free metal-cluster
assembly. For the first time, we obtained a structure of PSII from
Thermosynechococcus elongatus without the Mn4CaO5-cluster. Surprisingly,
cluster-removal leaves the positions of all coordinating amino acid residues
and most nearby water molecules largely unaffected, resulting in a pre-
organized ligand shell for kinetically competent and error-free photo-assembly
of the Mn4CaO5-cluster. First experiments initiating (i) partial disassembly
and (ii) partial re-assembly after complete depletion of the Mn4CaO5-cluster
agree with a specific bi-manganese cluster, likely a di-µ-oxo bridged pair of
Mn(III) ions, as an assembly intermediate