Spectroscopic evidence for Ca2+ involvement in the assembly of the Mn4Ca cluster in the photosynthetic water-oxidizing complex

Alexei M. Tyryshkin, Richard K. Watt, Sergei V. Baranov, Jyotishman Dasgupta, Michael P. Hendrich, G Charles Dismukes

Research output: Contribution to journalArticle

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Abstract

Biogenesis and repair of the inorganic core (Mn4CaO xCly), in the water-oxidizing complex of photosystem II (WOC-PSII), occurs through the light-induced (re)assembly of its free elementary ions and the apo-WOC-PSII protein, a reaction known as photoactivation. Herein, we use electron paramagnetic resonance (EPR) spectroscopy to characterize changes in the ligand coordination environment of the first photoactivation intermediate, the photo-oxidized Mn3+ bound to apo-WOC-PSII. On the basis of the observed changes in electron Zeeman (geff), 55Mn hyperfine (AZ) interaction, and the EPR transition probabilities, the photogenerated Mn3+ is shown to exist in two pH-dependent forms, differing in terms of strength and symmetry of their ligand fields. The transition from an EPR-invisible low-pH form to an EPR-active high-pH form occurs by deprotonation of an ionizable ligand bound to Mn 3+, implicated to be a water molecule: [Mn3+(OH 2)] ↔ [Mn3+(OH-)]. In the absence of Ca2+, the EPR-active Mn3+ exhibits a strong pH dependence (pH ∼6.5-9) of its ligand-field symmetry (rhombicity Δδ = 10%, derived from geff) and AZ (ΔAZ = 22%), attributable to a protein conformational change. Binding of Ca2+ to its effector site eliminates this pH dependence and locks both geff and AZ at values observed in the absence of Ca2+ at alkaline pH. Thus, Ca2+ directly controls the coordination environment and binds close to the high-affinity Mn3+, probably sharing a bridging ligand. This Ca2+ effect and the pH-induced changes are consistent with the ionization of the bridging water molecule, predicting that [Mn3+-(μ-O-2)-Ca2+] or [Mn3+-(μ-OH-2)2-Ca2+] is the first light intermediate in the presence of Ca2+. The formation of this intermediate templates the apo-WOC-PSII for the subsequent rapid cooperative binding and photo-oxidation of three additional Mn2+ ions, forming the active water oxidase.

Original languageEnglish
Pages (from-to)12876-12889
Number of pages14
JournalBiochemistry
Volume45
Issue number42
DOIs
Publication statusPublished - Oct 24 2006

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Photosystem II Protein Complex
Paramagnetic resonance
Electron Spin Resonance Spectroscopy
Water
Ligands
Ions
Deprotonation
Molecules
Photooxidation
Light
Ionization
Repair
Spectroscopy
Spectrum Analysis
Electrons
Proteins

ASJC Scopus subject areas

  • Biochemistry

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Spectroscopic evidence for Ca2+ involvement in the assembly of the Mn4Ca cluster in the photosynthetic water-oxidizing complex. / Tyryshkin, Alexei M.; Watt, Richard K.; Baranov, Sergei V.; Dasgupta, Jyotishman; Hendrich, Michael P.; Dismukes, G Charles.

In: Biochemistry, Vol. 45, No. 42, 24.10.2006, p. 12876-12889.

Research output: Contribution to journalArticle

Tyryshkin, Alexei M. ; Watt, Richard K. ; Baranov, Sergei V. ; Dasgupta, Jyotishman ; Hendrich, Michael P. ; Dismukes, G Charles. / Spectroscopic evidence for Ca2+ involvement in the assembly of the Mn4Ca cluster in the photosynthetic water-oxidizing complex. In: Biochemistry. 2006 ; Vol. 45, No. 42. pp. 12876-12889.
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title = "Spectroscopic evidence for Ca2+ involvement in the assembly of the Mn4Ca cluster in the photosynthetic water-oxidizing complex",
abstract = "Biogenesis and repair of the inorganic core (Mn4CaO xCly), in the water-oxidizing complex of photosystem II (WOC-PSII), occurs through the light-induced (re)assembly of its free elementary ions and the apo-WOC-PSII protein, a reaction known as photoactivation. Herein, we use electron paramagnetic resonance (EPR) spectroscopy to characterize changes in the ligand coordination environment of the first photoactivation intermediate, the photo-oxidized Mn3+ bound to apo-WOC-PSII. On the basis of the observed changes in electron Zeeman (geff), 55Mn hyperfine (AZ) interaction, and the EPR transition probabilities, the photogenerated Mn3+ is shown to exist in two pH-dependent forms, differing in terms of strength and symmetry of their ligand fields. The transition from an EPR-invisible low-pH form to an EPR-active high-pH form occurs by deprotonation of an ionizable ligand bound to Mn 3+, implicated to be a water molecule: [Mn3+(OH 2)] ↔ [Mn3+(OH-)]. In the absence of Ca2+, the EPR-active Mn3+ exhibits a strong pH dependence (pH ∼6.5-9) of its ligand-field symmetry (rhombicity Δδ = 10{\%}, derived from geff) and AZ (ΔAZ = 22{\%}), attributable to a protein conformational change. Binding of Ca2+ to its effector site eliminates this pH dependence and locks both geff and AZ at values observed in the absence of Ca2+ at alkaline pH. Thus, Ca2+ directly controls the coordination environment and binds close to the high-affinity Mn3+, probably sharing a bridging ligand. This Ca2+ effect and the pH-induced changes are consistent with the ionization of the bridging water molecule, predicting that [Mn3+-(μ-O-2)-Ca2+] or [Mn3+-(μ-OH-2)2-Ca2+] is the first light intermediate in the presence of Ca2+. The formation of this intermediate templates the apo-WOC-PSII for the subsequent rapid cooperative binding and photo-oxidation of three additional Mn2+ ions, forming the active water oxidase.",
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T1 - Spectroscopic evidence for Ca2+ involvement in the assembly of the Mn4Ca cluster in the photosynthetic water-oxidizing complex

AU - Tyryshkin, Alexei M.

AU - Watt, Richard K.

AU - Baranov, Sergei V.

AU - Dasgupta, Jyotishman

AU - Hendrich, Michael P.

AU - Dismukes, G Charles

PY - 2006/10/24

Y1 - 2006/10/24

N2 - Biogenesis and repair of the inorganic core (Mn4CaO xCly), in the water-oxidizing complex of photosystem II (WOC-PSII), occurs through the light-induced (re)assembly of its free elementary ions and the apo-WOC-PSII protein, a reaction known as photoactivation. Herein, we use electron paramagnetic resonance (EPR) spectroscopy to characterize changes in the ligand coordination environment of the first photoactivation intermediate, the photo-oxidized Mn3+ bound to apo-WOC-PSII. On the basis of the observed changes in electron Zeeman (geff), 55Mn hyperfine (AZ) interaction, and the EPR transition probabilities, the photogenerated Mn3+ is shown to exist in two pH-dependent forms, differing in terms of strength and symmetry of their ligand fields. The transition from an EPR-invisible low-pH form to an EPR-active high-pH form occurs by deprotonation of an ionizable ligand bound to Mn 3+, implicated to be a water molecule: [Mn3+(OH 2)] ↔ [Mn3+(OH-)]. In the absence of Ca2+, the EPR-active Mn3+ exhibits a strong pH dependence (pH ∼6.5-9) of its ligand-field symmetry (rhombicity Δδ = 10%, derived from geff) and AZ (ΔAZ = 22%), attributable to a protein conformational change. Binding of Ca2+ to its effector site eliminates this pH dependence and locks both geff and AZ at values observed in the absence of Ca2+ at alkaline pH. Thus, Ca2+ directly controls the coordination environment and binds close to the high-affinity Mn3+, probably sharing a bridging ligand. This Ca2+ effect and the pH-induced changes are consistent with the ionization of the bridging water molecule, predicting that [Mn3+-(μ-O-2)-Ca2+] or [Mn3+-(μ-OH-2)2-Ca2+] is the first light intermediate in the presence of Ca2+. The formation of this intermediate templates the apo-WOC-PSII for the subsequent rapid cooperative binding and photo-oxidation of three additional Mn2+ ions, forming the active water oxidase.

AB - Biogenesis and repair of the inorganic core (Mn4CaO xCly), in the water-oxidizing complex of photosystem II (WOC-PSII), occurs through the light-induced (re)assembly of its free elementary ions and the apo-WOC-PSII protein, a reaction known as photoactivation. Herein, we use electron paramagnetic resonance (EPR) spectroscopy to characterize changes in the ligand coordination environment of the first photoactivation intermediate, the photo-oxidized Mn3+ bound to apo-WOC-PSII. On the basis of the observed changes in electron Zeeman (geff), 55Mn hyperfine (AZ) interaction, and the EPR transition probabilities, the photogenerated Mn3+ is shown to exist in two pH-dependent forms, differing in terms of strength and symmetry of their ligand fields. The transition from an EPR-invisible low-pH form to an EPR-active high-pH form occurs by deprotonation of an ionizable ligand bound to Mn 3+, implicated to be a water molecule: [Mn3+(OH 2)] ↔ [Mn3+(OH-)]. In the absence of Ca2+, the EPR-active Mn3+ exhibits a strong pH dependence (pH ∼6.5-9) of its ligand-field symmetry (rhombicity Δδ = 10%, derived from geff) and AZ (ΔAZ = 22%), attributable to a protein conformational change. Binding of Ca2+ to its effector site eliminates this pH dependence and locks both geff and AZ at values observed in the absence of Ca2+ at alkaline pH. Thus, Ca2+ directly controls the coordination environment and binds close to the high-affinity Mn3+, probably sharing a bridging ligand. This Ca2+ effect and the pH-induced changes are consistent with the ionization of the bridging water molecule, predicting that [Mn3+-(μ-O-2)-Ca2+] or [Mn3+-(μ-OH-2)2-Ca2+] is the first light intermediate in the presence of Ca2+. The formation of this intermediate templates the apo-WOC-PSII for the subsequent rapid cooperative binding and photo-oxidation of three additional Mn2+ ions, forming the active water oxidase.

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