The inorganic biochemistry of photosynthetic oxygen evolution/water oxidation

Abstract

At the request of the organizer of this special edition, we have attempted to do several things in this manuscript: (1) we present a mini-review of recent, selected, works on the light-induced inorganic biogenesis (photoactivation), composition and structure of the inorganic core responsible for photosynthetic water oxidation; (2) we summarize a new proposal for the evolutionary origin of the water oxidation catalyst which postulates a key role for bicarbonate in formation of the inorganic core; (3) we summarize published studies and present new results on what has been learned from studies of 'inorganic mutants' in which the endogenous cofactors (Mn(n+), Ca2+, Cl-) are substituted; (4) the first DeltapH changes measured during the photoactivation process are reported and used to develop a model for the stepwise photo-assembly process; (5) a comparative analysis is given of data in the literature on the kinetics of substrate water exchange and peroxide binding/dismutation which support a mechanistic model for water oxidation in general; (6) we discuss alternative interpretations of data in the literature with a view to forecast new avenues where progress is needed.

Photoassembly of the water-oxidizing complex in photosystem II

“…No other metal ions have been found to date that can replace it. We have examined several metal ions as potential surrogates for Mn 2+ in the assembly process of spinach apo-WOC-PSII [11]. These studies were conducted by replacing Mn 2+ , while keeping all other components fixed at the optimal concentrations for Mn-dependent photoactivation (Cl − , Ca 2+ and the electron acceptor ferricyanide).…”

“…If Ca 2+ is left out of the solution, binding and photooxidation of many more Mn 2+ occurs (up to 20) to the apo-WOC-PSII protein and no O 2 evolution activity is observable [45,58]. The relative binding affinities of various divalent metals (Mg 2+ , Ca 2+ , Mn 2+ , Sr 2+ ), and the oxo-cation UO 2 2+ have been characterized [11,59,60]. At low Ca/RC concentrations measurements of the kinetics of photoactivation reveal that the Ca 2+ binding affinity increases following photooxidation of the first Mn 2+ → Mn 3+ , during which 1 Ca 2+ binds per PSII [55].…”

“…Later it was found that there is a kinetic advantage for uptake of Sr 2+ versus Ca 2+ at the Ca-effector site during assembly of the apo-WOC enzyme and it was determined how each of the three rate constants measured by photoactivation are affected [11]. Sr 2+ was shown to be five times more effective than Ca 2+ in accelerating the rate of the first two assembly steps (k 1 and k 2 ) and two times better in retarding the deactivation step (k −1 ).…”

“…Unlike the reasonably well understood principles of single-electron and single-proton transfer chemistry, complex multi-electron/proton reactions control the overall energetics and thus the allowed pathway for catalysis [8,9,10]. Interested readers should also consult other recent reviews that cover in vitro and in vivo photoactivation of the WOC [11,12,13]. …”

Spectroscopic Evidence for Ca2+Involvement in the Assembly of the Mn4Ca Cluster in the Photosynthetic Water-Oxidizing Complex

“…If Ca 2+ is not included during photoactivation, a large excess of Mn 2+ is photo-oxidized and O 2 evolution is not restored (27). This inactivation process can be reversed by adding Ca 2+ , which restores a normal Mn 4 O x core, clearly establishing a role for calcium in guiding the assembly of the catalytically active Mn 4 O x core and restructuring the inactive polymanganese-oxo cluster (18,28,29).…”