A possible evolutionary origin for the Mn4 cluster of the photosynthetic water oxidation complex from natural MnO2 precipitates in the early ocean

Abstract

The photosynthetic water oxidation complex consists of a cluster of four Mn atoms bridged by O atoms, associated with Ca2+ 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 CaMn4O9 cluster. A variety of MnO2 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+, Mg2+, Ca2+, Ba2+, H+, and even Mn2+) 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.

Figure 1

The Kok cycle of S-state transitions in photosynthetic water oxidation. After four light-induced steps in which electrons are extracted by PS II, the metastable state S₄ is reached, which results in the release of O₂ within milliseconds. Proposed oxidation states of the four Mn atoms in each S-state are based on electron paramagnetic resonance and x-ray spectroscopic analysis.

Figure 2

(a) End-on view of the birnessite lattice (layer type) consisting of Mn (red) and O (blue) atoms. There is only one kind of bridging O atom (sp³-like between the Mn atoms; one of them is shown in vertical stripes). Mg²⁺ cations (gray) are located between the manganese and oxygen layers. The water molecules between the layers are shown as ○. (b) Oblique view of the lattice showing the mode of apical bridging of the O atoms among three Mn atoms.

Figure 3

(a) End-on view of the hollandite lattice (tunnel type) consisting of Mn (red) and O (blue) atoms and showing the proposed location of Ba²⁺ cations (gray) in the 2 × 2 tunnels (57, 58). There are two kinds of bridging O atoms, and one of each kind is designated by vertical stripes (sp³-like) or horizontal stripes (sp²-like). (b) Oblique view of the hollandite lattice shows the difference in the mode of bridging of the sp³-like (apical) and sp²-like (planar) O atoms between three Mn atoms. (c) Expanded oblique view shows more clearly the differences between the sp³-like (vertical stripes) and sp²-like (horizontal stripes) bridging O atoms.

Figure 4

Some possible Mn₄ clusters and oxygens extracted from the hollandite lattice (a) in categories that are incompatible with that present in the OEC, and (b) those that are compatible with that associated with the OEC. Structures are organized according to A, the number of 2.8-Å Mn-Mn vectors, and B, the number of 3.4-Å vectors, and given the designation (A, B). Only the bridging O atoms are shown.