The oxygen-evolving complex (OEC), also known as the water-splitting complex, is the portion of
photosystem II where
photo-oxidation of water occurs during the
light reactions of
photosynthesis
Photosynthesis is a process used by plants and other organisms to convert light energy into chemical energy that, through cellular respiration, can later be released to fuel the organism's activities. Some of this chemical energy is stored i ...
. The OEC is surrounded by four core protein subunits of photosystem II at the membrane-lumen interface.
In the overall water oxidation reaction, four
electron
The electron ( or ) is a subatomic particle with a negative one elementary electric charge. Electrons belong to the first generation of the lepton particle family,
and are generally thought to be elementary particles because they have no ...
s are extracted from two
water
Water (chemical formula ) is an inorganic, transparent, tasteless, odorless, and nearly colorless chemical substance, which is the main constituent of Earth's hydrosphere and the fluids of all known living organisms (in which it acts as a ...
molecules so that four
protons and one
O2 molecule are produced.
The molecular machinery for oxidizing water requires the ability to store the oxidizing potential resulting from three light-induced charge separations before the fourth provides sufficient oxidizing power for water
oxidation
Redox (reduction–oxidation, , ) is a type of chemical reaction in which the oxidation states of substrate change. Oxidation is the loss of electrons or an increase in the oxidation state, while reduction is the gain of electrons or a ...
.
Species distribution and subcellular location
The OEC and Photosystem II are only found in
chloroplasts and
cyanobacteria
Cyanobacteria (), also known as Cyanophyta, are a phylum of gram-negative bacteria that obtain energy via photosynthesis. The name ''cyanobacteria'' refers to their color (), which similarly forms the basis of cyanobacteria's common name, blu ...
. Within the chloroplasts, Photosystem II spans the
thylakoid membrane
Thylakoids are membrane-bound compartments inside chloroplasts and cyanobacteria. They are the site of the light-dependent reactions of photosynthesis. Thylakoids consist of a thylakoid membrane surrounding a thylakoid lumen. Chloroplast thyla ...
, composed of both granal thylakoids and stromal thylakoids.
Structure
The OEC has a metalloenzyme core containing both
manganese
Manganese is a chemical element with the symbol Mn and atomic number 25. It is a hard, brittle, silvery metal, often found in minerals in combination with iron. Manganese is a transition metal with a multifaceted array of industrial alloy use ...
and
calcium
Calcium is a chemical element with the symbol Ca and atomic number 20. As an alkaline earth metal, calcium is a reactive metal that forms a dark oxide-nitride layer when exposed to air. Its physical and chemical properties are most similar t ...
, with the empirical formula in the S
1 state for the inorganic core of Mn
4O
5Ca.
This cluster is coordinated by amino acid side chains of the D1 and CP43 subunits and is stabilized by
peripheral membrane protein
Peripheral membrane proteins, or extrinsic membrane proteins, are membrane proteins that adhere only temporarily to the biological membrane with which they are associated. These proteins attach to integral membrane proteins, or penetrate the perip ...
s.
These peripheral membrane proteins include OEE1 (PsbO), OEE2 (PsbP) and OEE3 (PsbQ); a fourth PsbR peptide is associated nearby. For other characteristics, see.
The Mn
4O
5Ca cluster is assembled within the Photosystem II protein in a light-driven process called photoactivation. Mn
2+ ions diffuse into the active site and are oxidized there by the same components responsible for water oxidation: the redox-active tyrosine of D1, which is oxidized by light-generated P680
+. The oxo bridges of the cluster derive from water molecules bound to the metal ions. The quantum efficiency of photoactivation is low. The process is not well understood.
Mechanism
The OEC transfers four electrons, one at a time, to P680
+. A
tyrosine
-Tyrosine or tyrosine (symbol Tyr or Y) or 4-hydroxyphenylalanine is one of the 20 standard amino acids that are used by cells to synthesize proteins. It is a non-essential amino acid with a polar side group. The word "tyrosine" is from the G ...
residue of the D1 polypeptide, Y
Z, is the immediate electron donor to P680
+.
According to the model proposed in 1970 by Bessel Kok,
the complex can exist in five states: S
0 to S
4, S
0 being the least oxidized and S
4 the most oxidized. Photons absorbed by photosystem II move the system in four steps from state S
0 to S
4. S
4 is unstable and it releases molecular
oxygen
Oxygen is the chemical element with the symbol O and atomic number 8. It is a member of the chalcogen group in the periodic table, a highly reactive nonmetal, and an oxidizing agent that readily forms oxides with most elements as wel ...
. For the complex to reset to the lowest state, S
0, it binds two new water molecules to enable the cycle to repeat.
Currently, although the mechanism of water oxidation by the complex is not completely understood, the main features of the mechanism have been uncovered. The roles of Cl
− and the membrane proteins surrounding the metal cluster are not fully understood. Much of what is known has been deduced from flash experiments, EPR, and x-ray spectroscopy.
The Mn
4O
5Ca cluster is the most striking feature of the OEC. It is crucial because it stores the three oxidizing equivalents in going from S
0 to S
3, and it binds the two substrate water molecules in such proximity that the oxygen-oxygen bond can be formed and in such a way that the protons of the water molecules can be extracted.
Because of its obvious importance, some authors use the term oxygen-evolving complex to refer to the Mn
4O
5Ca cluster.
The question of which manganese oxidation states are present in the cluster has been the subject of many investigations. This matter may have been decided by experiments that made use of the photoactivation process. Starting from Mn
2+ ions, molecular oxygen was produced starting after nine flashes of light, which implies that in the S
3 state all four manganese atoms have attained the Mn(IV) oxidation state. Working backward, S
0 is Mn(III)
3Mn(IV) and so on for the other S states.
Binding the substrate water molecules is a second function of the Mn
4O
5Ca cluster. In S
1, the best characterized state of the cluster, it has five oxo bridges, and two water molecules are bound to each of Mn4 and the calcium atom.
Oxygen isotope exchange experiments showed that both substrate oxygen atoms are exchangeable and that one exchanges more readily than the other.
It has been suggested that the more slowly exchanging oxygen atom is O5, which is a bridging ligand to Mn2, Mn3 and Ca. It binds already in S
0, possibly as a hydroxo ligand.
The second substrate water molecule is bound in S2,
likely to Mn4, which in S
2 is five coordinate Mn(III). During the S
2 to S
3 transition, Mn4 becomes a six-coordinate Mn(IV) with a new water-derived ligand as the substrate oxygen atom moves to a position much nearer to O5. These motions are described as a carousel mechanism for delivery of the substrate water molecule into the position where it can be incorporated into the product. The crystal structure of S
3 suggests that the two substrate oxygen atom nuclei are within 2 Å of each other. Close proximity of the two substrate oxygen atoms is essential for forming the O-O bond in the S
3 to S
4 to S
0 transition.
In addition to the dioxygen product for which the OEC is named, the other products are four hydrogen ions. These are delivered to the enclosed interior of the thylakoid membrane where they contribute to the driving force for ADP → ATP phosphorylation. Several channels containing water molecules and hydrophilic amino acid site chains have been identified in the protein which may enable the protons to escape from the active site.
Research
The details of how the substrate protons are separated from the substrate oxygens bound to the Mn
4O
5Ca cluster have not been established. One point of view holds that the protons are shed from the cluster in response to its oxidation by Y
Z• where this redox reaction is thought of as electron transfer from the cluster to Y
Z•. An alternative proposal is that the protons are given up by Y
Z as it is oxidized by P
680+and that Y
Z• extracts both a proton and an electron from the cluster on each transition. Because protons are so numerous in the samples and are not observable in crystal studies, this question may eventually be decided by computational methods.
Another question that may be decided by computational methods is the nature of oxygen-oxygen bond forming reaction. This question is of great interest because the reaction is unique in biology and because the answer may help in designing artificial catalysts for water splitting. From experimental work on the S
3 to S
4 to S
0 transition, it is known that the time course of Y
Z• reduction roughly matches the time course of O
2 release. This means that any potential intermediates in the process can have only very short lifetimes, making them undetectable.
Extensive computational investigations using
density functional theory
Density-functional theory (DFT) is a computational quantum mechanical modelling method used in physics, chemistry and materials science to investigate the electronic structure (or nuclear structure) (principally the ground state) of many-body ...
have been carried out to map out the entire S-state cycle and especially to probe the S
3 to S
0 transition; for example, see. Hybrid methods melding quantum mechanics with
molecular mechanics
Molecular mechanics uses classical mechanics to model molecular systems. The Born–Oppenheimer approximation is assumed valid and the potential energy of all systems is calculated as a function of the nuclear coordinates using Force field (chemi ...
calculations are also being used.
The results of such efforts are not always in agreement. There is still much to be learned about the mechanism of photosynthetic water oxidation.
References
Further reading
* - outlines a possible route for the evolution of the OEC.
{{refend
Photosynthesis
Light reactions