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Evolutionary Origins of the Photosynthetic Water Oxidation Cluster: Bicarbonate Permits Mn 2+ Photo‐oxidation by Anoxygenic Bacterial Reaction Centers
Author(s) -
Khorobrykh Andrei,
Dasgupta Jyotishman,
Kolling Derrick R. J.,
Terentyev Vasily,
Klimov Vyacheslav V.,
Dismukes G. Charles
Publication year - 2013
Publication title -
chembiochem
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.05
H-Index - 126
eISSN - 1439-7633
pISSN - 1439-4227
DOI - 10.1002/cbic.201300355
Subject(s) - anoxygenic photosynthesis , photosystem ii , bicarbonate , chemistry , oxygen evolution , photochemistry , oxygen evolving complex , redox , photosynthesis , artificial photosynthesis , carbonate , water splitting , electron paramagnetic resonance , photosynthetic reaction centre , catalysis , electrochemistry , inorganic chemistry , electron transfer , photocatalysis , phototroph , organic chemistry , biochemistry , physics , electrode , nuclear magnetic resonance
The enzyme that catalyzes water oxidation in oxygenic photosynthesis contains an inorganic cluster (Mn 4 CaO 5 ) 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+ (CO 3 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.