Evolutionary origins of the photosynthetic water oxidation cluster: bicarbonate permits Mn(2+) photo-oxidation by anoxygenic bacterial reaction centers

• Published in: Chembiochem : a European journal of chemical biology Vol. 14; no. 14; pp. 1725 - 1731
• Main Authors: Khorobrykh, Andrei, Dasgupta, Jyotishman, Kolling, Derrick R J, Terentyev, Vasily, Klimov, Vyacheslav V, Dismukes, G Charles
• Format: Journal Article
• Language: English
• Published: Germany 23.09.2013
• Subjects: Bicarbonates - chemistry; Biocatalysis; Electrochemical Techniques; Electron Spin Resonance Spectroscopy; Evolution, Molecular; Light; Manganese - chemistry; Oxidation-Reduction; Photosystem II Protein Complex - chemistry; Photosystem II Protein Complex - metabolism; Rhodovulum - metabolism; Thermodynamics; Water - chemistry; photosystem II; oxygenic photosynthesis; bicarbonate; evolution; bacterial reaction centers; manganese
• ISSN: 1439-7633
• DOI: 10.1002/cbic.201300355

The enzyme that catalyzes water oxidation in oxygenic photosynthesis contains an inorganic cluster (Mn4 CaO5 ) that is universally conserved in all photosystem II (PSII) protein complexes. Its hypothesized precursor is an anoxygenic photobacterium containing a type 2 reaction center as photo-oxidant (bRC2, iron-quinone type). Here we provide the first experimental evidence that a native bRC2 complex can catalyze the photo-oxidation of Mn(2+) to Mn(3+) , but only in the presence of bicarbonate concentrations that allows the formation of (bRC2)Mn(2+) (bicarbonate)1-2 complexes. Parallel-mode EPR spectroscopy was used to characterize the photoproduct, (bRC2)Mn(3+) (CO3 (2-) ), based on the g tensor and (55) Mn hyperfine splitting. (Bi)carbonate coordination extends the lifetime of the Mn(3+) photoproduct by slowing charge recombination. Prior electrochemical measurements show that carbonate complexation thermodynamically stabilizes the Mn(3+) product by 0.9-1 V relative to water ligands. A model for the origin of the water oxidation catalyst is presented that proposes chemically feasible steps in the evolution of oxygenic PSIIs, and is supported by literature results on the photoassembly of contemporary PSIIs.