A functional role for tyrosine-D in assembly of the inorganic core of the water oxidase complex of photosystem II and the kinetics of water oxidation

G. M. Ananyev, I. Sakiyan, B. A. Diner, G Charles Dismukes

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Abstract

The role of D2-Tyr160 (YD), a photooxidizable residue in the D2 reaction center polypeptide of photosystem II (PSII), was investigated in both wild type and a mutant strain (D2-Tyr160Phe) in which phenylalanine replaces YD in the cyanobacterium Synechocystis sp. (strain PCC 6803). YD is the symmetry-related tyrosine that is homologous to the essential photoactive Tyr161(Yz) of the D1 polypeptide of PSII. We compared the flash-induced yield of O2 in intact, functional PSII centers from both wild-type and mutant PSII core complexes. The yield of O2 in the intact holo-enzyme was found to be identical in the mutant and wild-type PSII cores using long (saturating) pulses or continuous illumination, but was observed to be appreciably reduced in the mutant using short (nonsaturating) light pulses (4Ca1Clx, core required for O2 evolution. We show that the D2-Tyr160Phe mutant cores can assemble a functional WOC from the free inorganic cofactors, but at a much slower rate and with reduced quantum efficiency vs wild-type PSII cores. Both of these observations imply that the presence of YDleads to a more efficient photooxidation of the Mn cluster relative to deactivation (reductive processes). One possible explanation for this behavior is that the phenolic proton on YD is retained within the reaction center following YD oxidation. The positive charge, likely shared by D2-His 189 and other residues, raises the reduction potential of P680 +/P680, thereby increasing the driving force for the oxidation of Mn4YZ. There is, therefore, a competitive advantage to organisms that retain the YD residue, possibly explaining its retention in all sequences of psbD (encoding the D2 polypeptide) known to date. We also find that the sequence of metal binding steps during assembly of apo-WOC-PSII centers in cyanobacteria cores differs from that in higher plants. This is seen by a reduced calcium affinity at its effector site and reduced competition for binding to the Mn(II) site, resulting in acceleration of the initial lagtime by Ca2+, in contrast to retardation in spinach. Ca2+ binding to its effector site promotes the stability of the photointermediates (IM1 and above) by suppressing unproductive decay.

Original languageEnglish
Pages (from-to)974-980
Number of pages7
JournalBiochemistry
Volume41
Issue number3
DOIs
Publication statusPublished - Jan 22 2002

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Photosystem II Protein Complex
Tyrosine
Oxidation
Kinetics
Water
Cyanobacteria
Peptides
Synechocystis
Spinacia oleracea
Photooxidation
Lighting
Phenylalanine
Quantum efficiency
Protons
Metals
Calcium
Light
Enzymes

ASJC Scopus subject areas

  • Biochemistry

Cite this

A functional role for tyrosine-D in assembly of the inorganic core of the water oxidase complex of photosystem II and the kinetics of water oxidation. / Ananyev, G. M.; Sakiyan, I.; Diner, B. A.; Dismukes, G Charles.

In: Biochemistry, Vol. 41, No. 3, 22.01.2002, p. 974-980.

Research output: Contribution to journalArticle

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abstract = "The role of D2-Tyr160 (YD), a photooxidizable residue in the D2 reaction center polypeptide of photosystem II (PSII), was investigated in both wild type and a mutant strain (D2-Tyr160Phe) in which phenylalanine replaces YD in the cyanobacterium Synechocystis sp. (strain PCC 6803). YD is the symmetry-related tyrosine that is homologous to the essential photoactive Tyr161(Yz) of the D1 polypeptide of PSII. We compared the flash-induced yield of O2 in intact, functional PSII centers from both wild-type and mutant PSII core complexes. The yield of O2 in the intact holo-enzyme was found to be identical in the mutant and wild-type PSII cores using long (saturating) pulses or continuous illumination, but was observed to be appreciably reduced in the mutant using short (nonsaturating) light pulses (4Ca1Clx, core required for O2 evolution. We show that the D2-Tyr160Phe mutant cores can assemble a functional WOC from the free inorganic cofactors, but at a much slower rate and with reduced quantum efficiency vs wild-type PSII cores. Both of these observations imply that the presence of YDleads to a more efficient photooxidation of the Mn cluster relative to deactivation (reductive processes). One possible explanation for this behavior is that the phenolic proton on YD is retained within the reaction center following YD oxidation. The positive charge, likely shared by D2-His 189 and other residues, raises the reduction potential of P680 +/P680, thereby increasing the driving force for the oxidation of Mn4YZ. There is, therefore, a competitive advantage to organisms that retain the YD residue, possibly explaining its retention in all sequences of psbD (encoding the D2 polypeptide) known to date. We also find that the sequence of metal binding steps during assembly of apo-WOC-PSII centers in cyanobacteria cores differs from that in higher plants. This is seen by a reduced calcium affinity at its effector site and reduced competition for binding to the Mn(II) site, resulting in acceleration of the initial lagtime by Ca2+, in contrast to retardation in spinach. Ca2+ binding to its effector site promotes the stability of the photointermediates (IM1 and above) by suppressing unproductive decay.",
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T1 - A functional role for tyrosine-D in assembly of the inorganic core of the water oxidase complex of photosystem II and the kinetics of water oxidation

AU - Ananyev, G. M.

AU - Sakiyan, I.

AU - Diner, B. A.

AU - Dismukes, G Charles

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N2 - The role of D2-Tyr160 (YD), a photooxidizable residue in the D2 reaction center polypeptide of photosystem II (PSII), was investigated in both wild type and a mutant strain (D2-Tyr160Phe) in which phenylalanine replaces YD in the cyanobacterium Synechocystis sp. (strain PCC 6803). YD is the symmetry-related tyrosine that is homologous to the essential photoactive Tyr161(Yz) of the D1 polypeptide of PSII. We compared the flash-induced yield of O2 in intact, functional PSII centers from both wild-type and mutant PSII core complexes. The yield of O2 in the intact holo-enzyme was found to be identical in the mutant and wild-type PSII cores using long (saturating) pulses or continuous illumination, but was observed to be appreciably reduced in the mutant using short (nonsaturating) light pulses (4Ca1Clx, core required for O2 evolution. We show that the D2-Tyr160Phe mutant cores can assemble a functional WOC from the free inorganic cofactors, but at a much slower rate and with reduced quantum efficiency vs wild-type PSII cores. Both of these observations imply that the presence of YDleads to a more efficient photooxidation of the Mn cluster relative to deactivation (reductive processes). One possible explanation for this behavior is that the phenolic proton on YD is retained within the reaction center following YD oxidation. The positive charge, likely shared by D2-His 189 and other residues, raises the reduction potential of P680 +/P680, thereby increasing the driving force for the oxidation of Mn4YZ. There is, therefore, a competitive advantage to organisms that retain the YD residue, possibly explaining its retention in all sequences of psbD (encoding the D2 polypeptide) known to date. We also find that the sequence of metal binding steps during assembly of apo-WOC-PSII centers in cyanobacteria cores differs from that in higher plants. This is seen by a reduced calcium affinity at its effector site and reduced competition for binding to the Mn(II) site, resulting in acceleration of the initial lagtime by Ca2+, in contrast to retardation in spinach. Ca2+ binding to its effector site promotes the stability of the photointermediates (IM1 and above) by suppressing unproductive decay.

AB - The role of D2-Tyr160 (YD), a photooxidizable residue in the D2 reaction center polypeptide of photosystem II (PSII), was investigated in both wild type and a mutant strain (D2-Tyr160Phe) in which phenylalanine replaces YD in the cyanobacterium Synechocystis sp. (strain PCC 6803). YD is the symmetry-related tyrosine that is homologous to the essential photoactive Tyr161(Yz) of the D1 polypeptide of PSII. We compared the flash-induced yield of O2 in intact, functional PSII centers from both wild-type and mutant PSII core complexes. The yield of O2 in the intact holo-enzyme was found to be identical in the mutant and wild-type PSII cores using long (saturating) pulses or continuous illumination, but was observed to be appreciably reduced in the mutant using short (nonsaturating) light pulses (4Ca1Clx, core required for O2 evolution. We show that the D2-Tyr160Phe mutant cores can assemble a functional WOC from the free inorganic cofactors, but at a much slower rate and with reduced quantum efficiency vs wild-type PSII cores. Both of these observations imply that the presence of YDleads to a more efficient photooxidation of the Mn cluster relative to deactivation (reductive processes). One possible explanation for this behavior is that the phenolic proton on YD is retained within the reaction center following YD oxidation. The positive charge, likely shared by D2-His 189 and other residues, raises the reduction potential of P680 +/P680, thereby increasing the driving force for the oxidation of Mn4YZ. There is, therefore, a competitive advantage to organisms that retain the YD residue, possibly explaining its retention in all sequences of psbD (encoding the D2 polypeptide) known to date. We also find that the sequence of metal binding steps during assembly of apo-WOC-PSII centers in cyanobacteria cores differs from that in higher plants. This is seen by a reduced calcium affinity at its effector site and reduced competition for binding to the Mn(II) site, resulting in acceleration of the initial lagtime by Ca2+, in contrast to retardation in spinach. Ca2+ binding to its effector site promotes the stability of the photointermediates (IM1 and above) by suppressing unproductive decay.

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