Evolutionary origins of the photosynthetic water oxidation cluster: Bicarbonate permits mn2+ photo-oxidation by anoxygenic bacterial reaction centers

Andrei Khorobrykh, Jyotishman Dasgupta, Derrick R J Kolling, Vasily Terentyev, Vyacheslav V. Klimov, G Charles Dismukes

Research output: Contribution to journalArticle

14 Citations (Scopus)

Abstract

The enzyme that catalyzes water oxidation in oxygenic photosynthesis contains an inorganic cluster (Mn4CaO5) 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 Mn2+ to Mn3+, but only in the presence of bicarbonate concentrations that allows the formation of (bRC2)Mn2+(bicarbonate)1-2 complexes. Parallel-mode EPR spectroscopy was used to characterize the photoproduct, (bRC2)Mn3+(CO3 2-), based on the g tensor and 55Mn hyperfine splitting. (Bi)carbonate coordination extends the lifetime of the Mn3+ photoproduct by slowing charge recombination. Prior electrochemical measurements show that carbonate complexation thermodynamically stabilizes the Mn3+ 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.

Original languageEnglish
Pages (from-to)1725-1731
Number of pages7
JournalChemBioChem
Volume14
Issue number14
DOIs
Publication statusPublished - Sep 2013

Fingerprint

Photooxidation
Bicarbonates
Carbonates
Oxidation
Water
Photobacterium
Photosystem II Protein Complex
Photosynthesis
Complexation
Oxidants
Genetic Recombination
Tensors
Paramagnetic resonance
Spectrum Analysis
Iron
Spectroscopy
Ligands
Catalysts
Enzymes

Keywords

  • Bacterial reaction centers
  • Bicarbonate
  • Evolution
  • Manganese
  • Oxygenic photosynthesis
  • Photosystem II

ASJC Scopus subject areas

  • Biochemistry
  • Organic Chemistry
  • Molecular Medicine
  • Molecular Biology

Cite this

Evolutionary origins of the photosynthetic water oxidation cluster : Bicarbonate permits mn2+ photo-oxidation by anoxygenic bacterial reaction centers. / Khorobrykh, Andrei; Dasgupta, Jyotishman; Kolling, Derrick R J; Terentyev, Vasily; Klimov, Vyacheslav V.; Dismukes, G Charles.

In: ChemBioChem, Vol. 14, No. 14, 09.2013, p. 1725-1731.

Research output: Contribution to journalArticle

Khorobrykh, Andrei ; Dasgupta, Jyotishman ; Kolling, Derrick R J ; Terentyev, Vasily ; Klimov, Vyacheslav V. ; Dismukes, G Charles. / Evolutionary origins of the photosynthetic water oxidation cluster : Bicarbonate permits mn2+ photo-oxidation by anoxygenic bacterial reaction centers. In: ChemBioChem. 2013 ; Vol. 14, No. 14. pp. 1725-1731.
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