A manganese‐chloride cluster as the functional centre of the O₂ evolving enzyme in photosynthetic systems

Abstract

Photosynthetic 0, evolution 0, evolving complex mechanism Manganese Chloride Metal clusterMany aspects of the mechanism for photosynthetic 02 evolution remain unknown despite considerable research effort over the past decades and despite the accumulation of a large amount of biochemical and biophysical knowledge about this biological process. Several excellent reviews dealing with this topic are available [l-6] so that, for the sake of brevity, this paper will be restricted to a discussion of a hypothesis for the 02 evolving centre with reference to these reviews and citing only a few other relevant individual publications.The overall reaction for photosynthetic 02 evolution is 2H20 h" -02 + 4H+ + 4e-In experiments with single turnover flashes of light it was shown [7] that the release of one 02 molecule required the sequential accumulation of four charges and the individual intermediate states were designated as S-states:(The subscripts indicate the number of positive charges accumulated.) Our model is based on and accommodates 4 well-established experimental observations: (i) the photo-oxidation of water to molecular 02 proceeds via the successive storage of four oxidising equivalents [7]; (ii) the 4 protons released for every molecule of 02 liberated during the charge accumulation occur with a stoichiometry sequence of 1, 0, 1, 2 over the successive S-states 181; (iii) 4 manganese atoms per active centre appear to be optimal [9, lo]; (iv) chloride is a necessary cofactor [ 11,121. The multiple electron transfers required, the Clinvolvement, the charging aspect of the process and the multiplicity of Mn ions all imply a manganese cluster with bridging Cl-between the Mn centres as a principal unit in the oxygen evolving system. The proposition that Cl-bridges between Mn ions was put forward years ago [13] and has been 'rediscovered' in a recent publication [14].

The effect of chloride on the thermal inactivation of oxygen evolution

“…However, the linewidths in the vicinity of the maxima at 0.3 mM and 7.0 mM C1-appear to be altered more significantly than the others. Since previously published reports have suggested that CI might function as a ligand to the catalytic Mn (Sandusky andYocum 1983, Critchley andSargeson 1984), we simultaneously examined the effect of partial Cl depletion on the heat release of Mn and the inactivation of the Hill reaction. Figures 7 and 8 show that although there is a significant effect of C1-on the loss of activity between 25 ° and 35 °C, there is no detectable Mn release in this temperature range.…”

The chloride requirement for photosynthetic oxygen evolution: Factors affecting nucleophilic displacement of chloride from the oxygen-evolving complex

“…Others [13,14] have used our proposals concerning the catalytic role of chloride in oxygen-evolution activity to construct elaborate models, which in one case (a paramagnetically inactive S 2 state) contradicts experimental results (the EPR multiline signal [19]). We prefer a simple model such as that we proposed earlier [11] as a schematic representation for a hypothetical interaction of chloride as a bridging ligand between manganese atoms.…”

Protection of photosynthetic O2 evolution against heat inactivation: the role of chloride, pH and coupling status

“…It is no longer a matter of dispute that chloride is an essential cofactor for photosynthetic oxygen evolution and it has been suggested recently to function as a bridging ligand between the manganese centers responsible for the charge accumulation in the water oxidation reaction (Sandusky and Yocum 1983, Critchley and Sargeson 1984. Inhibition of water oxidation function by heat treatment has previously been shown to be correlated with manganese loss from the membrane (Cheniae and Martin 1970), changes in chlorophyll fluorescence (Heath and Hind 1969, Schreiber andArmond 1978) and dissociation of a number of proteins from the membrane (Volger and Santarius 1981).…”