Bicarbonate May Be Required for Ligation of Manganese in the Oxygen-Evolving Complex of Photosystem II

Abstract

It was previously shown in the photosystem II membrane preparation DT-20 that photoxidation of the oxygen-evolving manganese cluster was blocked by 0.1 mM formate, unless 0.2 mM bicarbonate was present as well [Wincencjusz, H., Allakhverdiev, S. I., Klimov, V. V., and Van Gorkom, H. J. (1996) Biochim. Biophys. Acta 1273, 1-3]. Here it is shown by measurements of EPR signal II that oxidation of the secondary electron donor, YZ, is not inhibited. However, the reduction of is greatly slowed and occurs largely by back reaction with reduced acceptors. Bicarbonate is shown to prevent the loss of fast electron donation to . The release of about one or two free Mn2+ per photosystem II during formate treatment, and the fact that these effects are mimicked by Mn-depletion, suggests that formate may act by replacing a bicarbonate which is essential for Mn binding. Irreversible light-induced rebinding in an EPR-silent form of Mn2+ that was added to Mn-depleted DT-20 was indeed found to depend on the presence of bicarbonate, as did the reconstitution in such material of both the fast electron donation to and the UV absorbance changes characteristic of a functional oxygen-evolving complex. It is concluded that bicarbonate may be an essential ligand of the functional Mn cluster.

The origin of atmospheric oxygen on Earth: The innovation of oxygenic photosynthesis

“…Importantly, they found that bicarbonate increases the binding affinity and photooxidation rate of the first two Mn II ions, implicating a high affinity pair of Mn II ions involved in bicarbonate-dependent electron transfer from Mn II (27). They also found definitive evidence for bicarbonate enhancing the rate of light-induced charge separation within the intact holo-WOC-PSII at a site on the donor side of PSII, as well as for stabilizing the holo-WOC-PSII against thermal deactivation (27)(28)(29). We speculate that this greater thermal stability could have provided an evolutionary advantage to PSII precursors in the Archean period when ambient temperatures are predicted to have been substantially greater than today (1).…”

Solar water-splitting into H2 and O2: design principles of photosystem II and hydrogenases

“…Hydrogencarbonate (bicarbonate), which is important during the photo-assembly of the Mn 4 O x Ca cluster, 58 was recently proven not to be a tightly bound constituent of the functional complex.…”

Carbonic anhydrase activity of integral-functional complexes of thylakoid membranes of spinach chloroplasts

“…There is an evidence that PS II-associated CA generates bicarbonate ions at a rate sufficient to bound protons released in the inner space of thylakoid in the process of photosynthetic oxidation of water [9]. Hence, CA prevents acidic denaturation of manganese cluster of PS II, as critical increase in local H + concentration may damage the active centers of the complex and result in their destruction with manganese release in liquid environment [10,11].…”