A possible evolutionary origin for the Mn(4) cluster of the photosynthetic water oxidation complex from natural MnO(2) precipitates in the early ocean

The photosynthetic water oxidation complex consists of a cluster of four Mn atoms bridged by O atoms, associated with Ca(2+) and Cl(−), and incorporated into protein. The structure is similar in higher plants and algae, as well as in cyanobacteria of more ancient lineage, dating back more than 2.5 billion years ago on Earth. It has been proposed that the proto-enzyme derived from a component of a natural early marine manganese precipitate that contained a CaMn(4)O(9) cluster. A variety of MnO(2) minerals are found in nature. Three major classes are spinels, sheet-like layered structures, and three-dimensional networks that contain parallel tunnels. These relatively open structures readily incorporate cations (Na(+), Li(+), Mg(2+), Ca(2+), Ba(2+), H(+), and even Mn(2+)) and water. The minerals have different ratios of Mn(III) and Mn(IV) octahedrally coordinated to oxygens. Using x-ray spectroscopy we compare the chemical structures of Mn in the minerals with what is known about the arrangement in the water oxidation complex to define the parameters of a structural model for the photosynthetic catalytic site. This comparison provides for the structural model a set of candidate Mn(4) clusters—some previously proposed and considered and others entirely novel.