The Central Photochemical Event: Light-Driven Electron Flow:- Water Is Split by the Oxygen-Evolving Complex
The ultimate source of the electrons passed to NADPH in plant (oxygenic) photosynthesis is water. Having given up an electron to pheophytin, P680 (of PSII) must acquire an electron to return to its ground state in preparation for capture of another photon. In principle, the required electron might come from any number of organic or inorganic compounds. Photosynthetic bacteria use a variety of electron donors for this purpose— acetate, succinate, malate, or sulfide—depending on what is available in a particular ecological niche. About 3 billion years ago, evolution of primitive photosynthetic bacteria (the progenitors of the modern cyanobacteria) produced a photosystem capable of taking electrons from a donor that is always available—water. Two water molecules are split, yielding four electrons, four protons, and molecular oxygen:
2H2O → 4H++4e-+O2
A single photon of visible light does not have enough energy to break the bonds in water; four photons are required in this photolytic cleavage reaction. The four electrons abstracted from water do not pass directly to P680+, which can accept only one electron at a time. Instead, a remarkable molecular device, the oxygen-evolving complex (also called the water splitting complex), passes four electrons one at α time to P680 (Fig. 19–56). The immediate electron donor to P680 is a Tyr residue (often designated Z or Tyrz) in protein subunit D1 of the PSII reaction center. The Tyr residue loses both a proton and an electron, generating the electrically neutral Tyr free radical, Tyr:
4P680++4 Tyr → 4P680+4 Tyr (19–13)
The Tyr radical regains its missing electron and proton by oxidizing a cluster of four manganese ions in the water-splitting complex. With each single-electron transfer, the Mn cluster becomes more oxidized; four single-electron transfers, each corresponding to the ab sorption of one photon, produce a charge of +4 on the Mn complex (Fig. 19–56):
4 Tyr+[Mn complex]0→4 Tyr+ [Mn complex]4+(19–14)
In this state, the Mn complex can take four electrons from a pair of water molecules, releasing 4 H+ and O2:
[Mn complex]4++2H2O→ [Mn complex]0+4H++O2(19–15)
Because the four protons produced in this reaction are released into the thylakoid lumen, the oxygen-evolving complex acts as a proton pump, driven by electron transfer. The sum of Equations 19–12 through 19–15 is
2H2O+2PQB+4 photons → O2+2PQBH2 (19–16)
The water-splitting activity associated with the PSII reaction center has proved exceptionally difficult to purify. A peripheral membrane protein (Mr 33,000) on the lumenal side of the thylakoid membrane is believed to stabilize the Mn complex. In the crystal structure (PDB ID 1FE1; see Fig. 19–50), four Mn ions are clustered with precise geometry near a Tyr residue on the D1 sub unit, presumably the one involved in water oxidation. Manganese can exist in stable oxidation states from +2 to +7, so a cluster of four Mn ions can certainly donate or accept four electrons. The mechanism shown in Fig ure 19–56 is consistent with the experimental facts, but until the exact chemical structures of all the intermediates of the Mn cluster are known, the detailed mechanism remains elusive.
FIGURE 19–56 Water-splitting activity of the oxygen-evolving com plex. Shown here is the process that produces a four-electron oxidizing agent—believed to be a multinuclear center with several Mn ions— in the water-splitting complex of PSII. The sequential absorption of four photons (excitons), each absorption causing the loss of one electron from the Mn center, produces an oxidizing agent that can remove four electrons from two molecules of water, producing O2. The electrons lost from the Mn center pass one at a time to an oxidized Tyr residue in a PSII protein, then to P680+.
