Bicarbonate coordinates to Mn3+ during photo-assembly of the catalytic Mn4Ca core of photosynthetic water oxidation

EPR characterization

Jyotishman Dasgupta, Alexei M. Tyryshkin, Sergei V. Baranov, G Charles Dismukes

Research output: Contribution to journalArticle

14 Citations (Scopus)

Abstract

Assembly of the catalytic cluster, Mn4CaOxCly, comprising the water-oxidizing complex (WOC) of photosystem II (PSII), occurs during biogenesis in the presence of the apo-WOC-PSII complex, Mn2+, Ca2+ and Cl- cofactors under weak illumination. The in vitro assembly process known as photo-activation involves several intermediates that have been resolved in previous kinetic studies. (Bi)carbonate has been shown to stimulate the rate of formation and yield of the first stable light-induced Mn3+ assembly intermediate (IM1) from Mn2+ bound to the high-affinity assembly site in apo-WOC-PSII. 13C electron spin echo envelope modulation has previously revealed that (bi)carbonate is a ligand to this Mn2+. Herein, we use parallel-mode electron paramagnetic resonance (EPR) spectroscopy to characterize the Mn3+ photoproduct, which exists as a ternary complex with carbonate at the high-affinity assembly site (in the absence of Ca2+) formulated as [CO3-Mn3+-apo-WOC-PSII]. The EPR-derived spectral parameters of IM1 (the g value, 55Mn hyperfine coupling constant (AZ) and the ligand-field splitting parameters D/E) are independent of solution pH, in marked contrast to their strong pH dependence in the absence of bicarbonate. (Bi)carbonate coordination "chemically isolates" the IM1 from external pH changes, much like that caused by Ca2+ coordination, revealing similar roles in photo-assembly. The cumulative results reveal that (bi)carbonate and Ca2+ coordination control the ligand field strength and symmetry around the initial high-affinity Mn3+, consistent with the possible formation of a μ2-oxide bridge in IM1, [Mn3+(O2-)Ca2+]. These events greatly improve the quantum yield of subsequent steps in photo-assembly.

Original languageEnglish
Pages (from-to)137-150
Number of pages14
JournalApplied Magnetic Resonance
Volume37
Issue number1
DOIs
Publication statusPublished - 2010

Fingerprint

carbonates
electron paramagnetic resonance
assembly
oxidation
water
affinity
ligands
biological evolution
electron spin
field strength
echoes
envelopes
illumination
activation
modulation
oxides
kinetics
symmetry
spectroscopy

ASJC Scopus subject areas

  • Atomic and Molecular Physics, and Optics

Cite this

Bicarbonate coordinates to Mn3+ during photo-assembly of the catalytic Mn4Ca core of photosynthetic water oxidation : EPR characterization. / Dasgupta, Jyotishman; Tyryshkin, Alexei M.; Baranov, Sergei V.; Dismukes, G Charles.

In: Applied Magnetic Resonance, Vol. 37, No. 1, 2010, p. 137-150.

Research output: Contribution to journalArticle

@article{ef7204d5b42f48b2855728af830efe81,
title = "Bicarbonate coordinates to Mn3+ during photo-assembly of the catalytic Mn4Ca core of photosynthetic water oxidation: EPR characterization",
abstract = "Assembly of the catalytic cluster, Mn4CaOxCly, comprising the water-oxidizing complex (WOC) of photosystem II (PSII), occurs during biogenesis in the presence of the apo-WOC-PSII complex, Mn2+, Ca2+ and Cl- cofactors under weak illumination. The in vitro assembly process known as photo-activation involves several intermediates that have been resolved in previous kinetic studies. (Bi)carbonate has been shown to stimulate the rate of formation and yield of the first stable light-induced Mn3+ assembly intermediate (IM1) from Mn2+ bound to the high-affinity assembly site in apo-WOC-PSII. 13C electron spin echo envelope modulation has previously revealed that (bi)carbonate is a ligand to this Mn2+. Herein, we use parallel-mode electron paramagnetic resonance (EPR) spectroscopy to characterize the Mn3+ photoproduct, which exists as a ternary complex with carbonate at the high-affinity assembly site (in the absence of Ca2+) formulated as [CO3-Mn3+-apo-WOC-PSII]. The EPR-derived spectral parameters of IM1 (the g value, 55Mn hyperfine coupling constant (AZ) and the ligand-field splitting parameters D/E) are independent of solution pH, in marked contrast to their strong pH dependence in the absence of bicarbonate. (Bi)carbonate coordination {"}chemically isolates{"} the IM1 from external pH changes, much like that caused by Ca2+ coordination, revealing similar roles in photo-assembly. The cumulative results reveal that (bi)carbonate and Ca2+ coordination control the ligand field strength and symmetry around the initial high-affinity Mn3+, consistent with the possible formation of a μ2-oxide bridge in IM1, [Mn3+(O2-)Ca2+]. These events greatly improve the quantum yield of subsequent steps in photo-assembly.",
author = "Jyotishman Dasgupta and Tyryshkin, {Alexei M.} and Baranov, {Sergei V.} and Dismukes, {G Charles}",
year = "2010",
doi = "10.1007/s00723-009-0053-z",
language = "English",
volume = "37",
pages = "137--150",
journal = "Applied Magnetic Resonance",
issn = "0937-9347",
publisher = "Springer Wien",
number = "1",

}

TY - JOUR

T1 - Bicarbonate coordinates to Mn3+ during photo-assembly of the catalytic Mn4Ca core of photosynthetic water oxidation

T2 - EPR characterization

AU - Dasgupta, Jyotishman

AU - Tyryshkin, Alexei M.

AU - Baranov, Sergei V.

AU - Dismukes, G Charles

PY - 2010

Y1 - 2010

N2 - Assembly of the catalytic cluster, Mn4CaOxCly, comprising the water-oxidizing complex (WOC) of photosystem II (PSII), occurs during biogenesis in the presence of the apo-WOC-PSII complex, Mn2+, Ca2+ and Cl- cofactors under weak illumination. The in vitro assembly process known as photo-activation involves several intermediates that have been resolved in previous kinetic studies. (Bi)carbonate has been shown to stimulate the rate of formation and yield of the first stable light-induced Mn3+ assembly intermediate (IM1) from Mn2+ bound to the high-affinity assembly site in apo-WOC-PSII. 13C electron spin echo envelope modulation has previously revealed that (bi)carbonate is a ligand to this Mn2+. Herein, we use parallel-mode electron paramagnetic resonance (EPR) spectroscopy to characterize the Mn3+ photoproduct, which exists as a ternary complex with carbonate at the high-affinity assembly site (in the absence of Ca2+) formulated as [CO3-Mn3+-apo-WOC-PSII]. The EPR-derived spectral parameters of IM1 (the g value, 55Mn hyperfine coupling constant (AZ) and the ligand-field splitting parameters D/E) are independent of solution pH, in marked contrast to their strong pH dependence in the absence of bicarbonate. (Bi)carbonate coordination "chemically isolates" the IM1 from external pH changes, much like that caused by Ca2+ coordination, revealing similar roles in photo-assembly. The cumulative results reveal that (bi)carbonate and Ca2+ coordination control the ligand field strength and symmetry around the initial high-affinity Mn3+, consistent with the possible formation of a μ2-oxide bridge in IM1, [Mn3+(O2-)Ca2+]. These events greatly improve the quantum yield of subsequent steps in photo-assembly.

AB - Assembly of the catalytic cluster, Mn4CaOxCly, comprising the water-oxidizing complex (WOC) of photosystem II (PSII), occurs during biogenesis in the presence of the apo-WOC-PSII complex, Mn2+, Ca2+ and Cl- cofactors under weak illumination. The in vitro assembly process known as photo-activation involves several intermediates that have been resolved in previous kinetic studies. (Bi)carbonate has been shown to stimulate the rate of formation and yield of the first stable light-induced Mn3+ assembly intermediate (IM1) from Mn2+ bound to the high-affinity assembly site in apo-WOC-PSII. 13C electron spin echo envelope modulation has previously revealed that (bi)carbonate is a ligand to this Mn2+. Herein, we use parallel-mode electron paramagnetic resonance (EPR) spectroscopy to characterize the Mn3+ photoproduct, which exists as a ternary complex with carbonate at the high-affinity assembly site (in the absence of Ca2+) formulated as [CO3-Mn3+-apo-WOC-PSII]. The EPR-derived spectral parameters of IM1 (the g value, 55Mn hyperfine coupling constant (AZ) and the ligand-field splitting parameters D/E) are independent of solution pH, in marked contrast to their strong pH dependence in the absence of bicarbonate. (Bi)carbonate coordination "chemically isolates" the IM1 from external pH changes, much like that caused by Ca2+ coordination, revealing similar roles in photo-assembly. The cumulative results reveal that (bi)carbonate and Ca2+ coordination control the ligand field strength and symmetry around the initial high-affinity Mn3+, consistent with the possible formation of a μ2-oxide bridge in IM1, [Mn3+(O2-)Ca2+]. These events greatly improve the quantum yield of subsequent steps in photo-assembly.

UR - http://www.scopus.com/inward/record.url?scp=71149100652&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=71149100652&partnerID=8YFLogxK

U2 - 10.1007/s00723-009-0053-z

DO - 10.1007/s00723-009-0053-z

M3 - Article

VL - 37

SP - 137

EP - 150

JO - Applied Magnetic Resonance

JF - Applied Magnetic Resonance

SN - 0937-9347

IS - 1

ER -