Calcium controls the assembly of the photosynthetic water-oxidizing complex: A cadmium(II) inorganic mutant of the Mn4Ca core

John E. Bartlett, Sergei V. Baranov, Gennady M. Ananyev, G Charles Dismukes

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

Perturbation of the catalytic inorganic core (Mn4Ca 1OxCly) of the photosystem II-water-oxidizing complex (PSII-WOC) isolated from spinach is examined by substitution of Ca 2+ with cadmium(II) during core assembly. Cd2+ inhibits the yield of reconstitution of O2-evolution activity, called photoactivation, starting from the free inorganic cofactors and the cofactor-depleted apo-WOC-PSII complex. Ca2+ affinity increases following photooxidation of the first Mn2+ to Mn3+ bound to the 'high-affinity' site. Ca2+ binding occurs in the dark and is the slowest overall step of photoactivation (IM1→IM 1* step). Cd2+ competitively blocks the binding of Ca2+ to its functional site with 10- to 30-fold higher affinity, but does not influence the binding of Mn2+ to its high-affinity site. By contrast, even 10-fold higher concentrations of Cd2+ have no effect on O2-evolution activity in intact PSII-WOC. Paradoxically, Cd 2+ both inhibits photoactivation yield, while accelerating the rate of photoassembly of active centres 10-fold relative to Ca2+. Cd 2+ increases the kinetic stability of the photooxidized Mn 3+ assembly intermediate(s) by twofold (mean lifetime for dark decay). The rate data provide evidence that Cd2+ binding following photooxidation of the first Mn3+, IM1→IM 1*, causes three outcomes: (i) a longer intermediate lifetime that slows IM1 decay to IM0 by charge recombination, (ii) 10-fold higher probability of attaining the degrees of freedom (either or both cofactor and protein d.f.) needed to bind and photooxidize the remaining 3 Mn2+ that form the functional cluster, and (iii) increased lability of Cd2+ following Mn4 cluster assembly results in (re)exchange of Cd2+ by Ca2+ which restores active O2-evolving centres. Prior EPR spectroscopic data provide evidence for an oxo-bridged assembly intermediate, Mn 3+(μ-O2-)Ca2+, for IM1*. We postulate an analogous inhibited intermediate with Cd2+ replacing Ca2+.

Original languageEnglish
Pages (from-to)1253-1261
Number of pages9
JournalPhilosophical Transactions of the Royal Society B: Biological Sciences
Volume363
Issue number1494
DOIs
Publication statusPublished - Mar 27 2008

Fingerprint

Photosystem II Protein Complex
Cadmium
cadmium
Calcium
calcium
mutants
Spinacia oleracea
Photooxidation
Water
Genetic Recombination
Catalytic Domain
water
photooxidation
photosystem II
Paramagnetic resonance
deterioration
Proteins
Substitution reactions
Kinetics
spinach

Keywords

  • Calcium
  • Manganese
  • Oxygen evolution
  • Photosynthesis
  • Photosystem II
  • Water oxidation

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Agricultural and Biological Sciences (miscellaneous)

Cite this

Calcium controls the assembly of the photosynthetic water-oxidizing complex : A cadmium(II) inorganic mutant of the Mn4Ca core. / Bartlett, John E.; Baranov, Sergei V.; Ananyev, Gennady M.; Dismukes, G Charles.

In: Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, No. 1494, 27.03.2008, p. 1253-1261.

Research output: Contribution to journalArticle

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abstract = "Perturbation of the catalytic inorganic core (Mn4Ca 1OxCly) of the photosystem II-water-oxidizing complex (PSII-WOC) isolated from spinach is examined by substitution of Ca 2+ with cadmium(II) during core assembly. Cd2+ inhibits the yield of reconstitution of O2-evolution activity, called photoactivation, starting from the free inorganic cofactors and the cofactor-depleted apo-WOC-PSII complex. Ca2+ affinity increases following photooxidation of the first Mn2+ to Mn3+ bound to the 'high-affinity' site. Ca2+ binding occurs in the dark and is the slowest overall step of photoactivation (IM1→IM 1* step). Cd2+ competitively blocks the binding of Ca2+ to its functional site with 10- to 30-fold higher affinity, but does not influence the binding of Mn2+ to its high-affinity site. By contrast, even 10-fold higher concentrations of Cd2+ have no effect on O2-evolution activity in intact PSII-WOC. Paradoxically, Cd 2+ both inhibits photoactivation yield, while accelerating the rate of photoassembly of active centres 10-fold relative to Ca2+. Cd 2+ increases the kinetic stability of the photooxidized Mn 3+ assembly intermediate(s) by twofold (mean lifetime for dark decay). The rate data provide evidence that Cd2+ binding following photooxidation of the first Mn3+, IM1→IM 1*, causes three outcomes: (i) a longer intermediate lifetime that slows IM1 decay to IM0 by charge recombination, (ii) 10-fold higher probability of attaining the degrees of freedom (either or both cofactor and protein d.f.) needed to bind and photooxidize the remaining 3 Mn2+ that form the functional cluster, and (iii) increased lability of Cd2+ following Mn4 cluster assembly results in (re)exchange of Cd2+ by Ca2+ which restores active O2-evolving centres. Prior EPR spectroscopic data provide evidence for an oxo-bridged assembly intermediate, Mn 3+(μ-O2-)Ca2+, for IM1*. We postulate an analogous inhibited intermediate with Cd2+ replacing Ca2+.",
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