title: Evolutionary origins of the photosynthetic water oxidation cluster: bicarbonate permits Mn(2+) photo-oxidation by anoxygenic bacterial reaction centers.
abstract: 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.
authors.affiliation: Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, 142290 (Russia).
authors.forename: Andrei
authors.initials: A
authors.lastname: Khorobrykh
authors.forename: Jyotishman
authors.initials: J
authors.lastname: Dasgupta
authors.forename: Derrick R J
authors.initials: DR
authors.lastname: Kolling
authors.forename: Vasily
authors.initials: V
authors.lastname: Terentyev
authors.forename: Vyacheslav V
authors.initials: VV
authors.lastname: Klimov
authors.forename: G Charles
authors.initials: GC
authors.lastname: Dismukes
mesh_terms: D001639:Bicarbonates / Q000737:chemistry*; D055162:Biocatalysis; D055664:Electrochemical Techniques; D004578:Electron Spin Resonance Spectroscopy; D019143:Evolution, Molecular; D008027:Light; D008345:Manganese / Q000737:chemistry*; D010084:Oxidation-Reduction; D045332:Photosystem II Protein Complex / Q000737:chemistry / Q000378:metabolism*; D041903:Rhodovulum / Q000378:metabolism; D013816:Thermodynamics; D014867:Water / Q000737:chemistry*
chemical_list: D001639:Bicarbonates; D045332:Photosystem II Protein Complex; D014867:Water; D008345:Manganese
keywords: bacterial reaction centers; bicarbonate; evolution; manganese; oxygenic photosynthesis; photosystem II