Photoassembly of the Water-Oxidizing Complex in Photosystem II - PubMed (original) (raw)

Photoassembly of the Water-Oxidizing Complex in Photosystem II

Jyotishman Dasgupta et al. Coord Chem Rev. 2008 Feb.

Abstract

The light-driven steps in the biogenesis and repair of the inorganic core comprising the O(2)-evolving center of oxygenic photosynthesis (photosystem II water-oxidation complex, PSII-WOC) are reviewed. These steps, known collectively as photoactivation, involve the photoassembly of the free inorganic cofactors to the cofactor-depleted PSII-(apo-WOC) driven by light and produce the active O(2)-evolving core comprised of Mn(4)CaO(x)Cl(y). We focus on the functional role of the inorganic components as seen through the competition with non-native cofactors ("inorganic mutants") on water oxidation activity, the rate of the photoassembly reaction, and on structural insights gained from EPR spectroscopy of trapped intermediates formed in the initial steps of the assembly reaction. A chemical mechanism for the initial steps in photoactivation is given that is based on these data. Photoactivation experiments offer the powerful insights gained from replacement of the native cofactors, which together with the recent X-ray structural data for the resting holoenzyme provide a deeper understanding of the chemistry of water oxidation. We also review some new directions in research that photoactivation studies have inspired that look at the evolutionary history of this remarkable catalyst.

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Figures

Fig 1

Fig 1

XRD structural model of the water oxidizing complex (WOC) in Photosystem II adapted from Ferriera et.al.(2004) at 3.5 Å resolution. In the center is the CaMn4O4-core surrounded by its direct ligands (purple = Ca, grey = Mn, red = O). All amino acids named in a yellow box belong to the D1 subunit, while those in a green box come from subunit CP43. Dashed lines are shown for visual guidance only.

Fig 2

Fig 2

Scheme summarizing the methodology for removal of Mn4Ca cluster by high pH treatment, eg., isolation of apo-WOC-PSII particles from isolated spinach PSII membranes, and reconstitution by photoactivation.

Fig 3

Fig 3

(Left side) Kinetics of reconstitution of O2 evolution capacity by photoactivation of the apo-WOC-PSII membranes in the presence of (1) 0 mM, and (2) 1.2 mM, added bicarbonate. Assay conditions are pH 6.0, 1 μM apo-WOC-PSII, 100 μM MnCl2, 100 mM CaCl2, and 1.8 mM K3Fe(CN)6. The insert expands the first 40 flashes (3 s repetition rate). The vertical dashed lines represent the lag time _t_lag for each experiment, as derived from fitting the entire kinetics (Baranov et.al. (2004)). (Right side) Two-site model for bicarbonate acceleration of the rate of the first step of photoactivation. (A) The high-affinity bicarbonate site: When the high affinity Mn2+ site is unoccupied at low Mn2+ concentrations ([Mn2+] < 30 μM = KD [61]), (B) The low affinity bicarbonate site: At high Mn2+ concentrations ([Mn2+] > 30 μM = KD), bicarbonate binds directly to the high-affinity Mn2+ binding site (Baranov et.al.)(Dasgupta et al., submitted).

Fig 4

Fig 4

Schematic representation of the trapped intermediates in the first steps of photoactivation in presence of Ca2+. Protein-derived and non-changing water ligands to Mn2+/Mn3+ are not shown. Brackets [ ] represent the high-affinity Mn2+ site of apo-WOC-PSII. The CW EPR signals from [Mn3+-O2−- Ca2+] in red and [Mn2+-O2− - Ca2+] in blue is shown. See text for details.

Fig 5

Fig 5

The sequence of kinetic intermediates (top) formed during assembly of the inorganic core of the WOC by photoactivation (A, B,C). (Bottom) Proposed chemical formulation for intermediates.

Scheme 1

Scheme 1

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