Catalytic behaviour during Artificial Photosynthesis
Catalysis with Respect to Artificial Photosynthesis
Research Question: What characteristics are important to the development of an artificial catalyst for artificial photosynthesis?
Author: Eamon O’Connor
Table of Contents
- Introduction to artificial photosynthesis
- Summary of Catalysis
- Structure of the natural enzyme
- Photosystem II summary
- Structure of the manganese cubane core
- Role of Ca
- Role of ligands
- Reaction mechanism of water oxidation
- S-state cycle
- Oxidation states of manganese
- Summary of certain proposed mechanisms
- Questions regarding to substrate binding
- Important Characteristics
- Characteristics of manganese
- Other characteristics
Natural fossil fuels, the primary source of energy relied upon by our society, run the risk of being entirely consumed within the next 50 years. Without energy, the industrial sector falters. For this reason, we have begun to concentrate on alternative sources of energy. However, most other energy sources would not be able to be used as our primary one. Solar panels cannot produce enough energy to for our industrial needs as they are very inefficient. Nuclear power creates toxic waste which damages the environment, and wind turbines are inefficient and unreliable as they only work intermittently. At the same time, our planet is suffering from nearly irreversible climate change widely believed to be caused by the emission of carbon gases.
The amount of solar energy that hits the earth in a year is roughly 1000 times greater than the amount of energy consumed by the entire human race in that same amount of time. At the moment, plants are the only beings on our planet able to utilize this to create organic chemical energy. This process is called photosynthesis and is represented by the equation:
6CO2(g) + 12H2O(l) + photons → C6H12O6(aq) + 6O2(g) + 6H2O(l). As we can see, this process also consumes CO2, the suspected cause of global climate change and releases oxygen. Therefore artificial photosynthesis is emerging as a theoretical solution for both of these problems.
However, photosynthesis is not a simple process. The chemical reaction which forms C6H12O6 (glucose) is uphill, meaning it requires energy to drive the reaction. On top of this, the reaction requires a constant stream of electrons and protons. Water is among the most abundant compounds on our planet and was therefore chosen as the source of these subatomic particles. The photolysis of water can be represented by the half equation: 2H2O (l) → 4e- + 4H+ + O2 (g) . Unfortunately, two obstacles are present in the path to splitting water: its stability and its inertness. The bond energy of O-H is 110 kcal. Because of this stability, energy is required to effect the desired transformation. It is also extremely inert and therefore requires an effective catalyst. Therefore, scientists’ intent on developing an artificial system for photochemically splitting water must develop two parts, an effective photon harvester to transform the sun’s energy into usable chemical energy and an effective artificial catalyst to accelerate the rate of oxygen evolution, and to lower the minimum amount of required energy for this reaction to occur.
Catalysis is the process in which the rate of a chemical reaction is accelerated by means of a substance known as a catalyst. A catalyst helps achieve this accelerated rate by providing an alternative reaction mechanism involving a lower activation energy. Hence, the use of a catalyst will result in more molecular collisions with the energy required to reach the transition state and complete the reaction. Alternatively, catalysis can help reactions run at a lower temperature, or with less required energy, as in the case of photosynthesis.
Catalysts are classified into two categories: homogeneous catalysts and heterogeneous catalysts. The latter is in a different phase then the reactants. Heterogeneous catalysts create an intermediate compound with a reactant through adsorption on one of its active sites. Some sort of interaction occurs at the active site that results in increased reactivity of the reactant depending on how the adsorption takes place. For example, in the synthesis of nitrogen and hydrogen to ammonia, the reacting gases adsorb onto the active sites of finely divided iron particles. These intermediate compounds result in a weakening of the bonds of the reacting molecules. Hence, the strong bonds present in N3 are weakened and hydrogen and nitrogen combine with decreased activation energy. A homogeneous catalyst is a catalyst in the same phase as the reactants. It is consumed in the process and therefore changes the reaction mechanism, but is reproduced somewhere along the reaction.
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Catalysts are present in living organisms as enzymes. Enzymes are biomolecules composed of many proteins that increase the rate of chemical reactions. Nearly all processes in biological cells require enzymes to occur at significant rates. Enzymes differ from other catalysts in that they are much more specific. They are also extremely efficient, for example, carbonic anhydrase increases the rate of its natural reaction by 107 times. Enzymes, however, function only in very specific conditions and are very fragile if removed from their natural environment. Enzymes function like heterogeneous catalysts in that they form an intermediate compound with the reactants.
Structure of the Natural Catalyst
The enzyme responsible for water oxidation and oxygen evolution in nature uses light to generate enough oxidizing power to remove electrons from water and deliver them to plastoquinone which replaces the electrons lost due to excitation in the first step of photosynthesis. The enzyme can therefore be defined as a water/plastoquinone photo-oxidoreductase. It is referred to as PSII. The PSII reaction center is composed of many different subunits, but the one I will be examining is known as D1 (D for ‘diffuse’ bands on polyacrylamide gels), where the catalytic site for the oxidation of water is located. The other subunit involved strongly in the water/plastoquinone redox reactions is D2, which is involved in the reduction of plastoquinone.
It has been established that an oxo-bridged manganese and calcium cubane aggregate, found in nature as inorganic crystals of hollandite or rancieite, is the active site for the catalysis of the oxidation of water. The first good evidence for the involvement of a polynuclear Mn cluster was the observation of an EPR signal (Dismukes and Siderer 1981). This signal showed over 18 hyperfine lines known to be caused by at least two manganese nuclei. Since then, there have been several recent X-ray crystal structures of PSII at 3.8Å resolution (Zouni et al. 2001), at 3.7Å (Kamiya and Shen 2003), at 3.5Å resolution (Ferreira et al. 2004), and most recently at 3.0Å (Loll et al. 2005). The oxygen evolving complex is now modeled as a Mn3CaO4 cuboid tetramer. There is a fourth manganese ion attached to the exterior of the cuboid to a μ4 oxide ion. It is believed to be positioned in this location so that its coordination sphere is near that of calcium.
The calcium in the catalytic site is believed to function as a Lewis acid. It has been proven that calcium acts as more than just a structural component by G.W. Brudvig. He states that there is a great number of metal ions competing for the position of the Ca2+ ion, but that only Ca2+ and Sr2+ containing PSII enzymes support oxygen evolution. If the calcium ion was purely a structural component, then it would be expected that other metal ions of the same size and charge would be able to act as substitutes, but this is not the case. Cd2+ replaces Ca2+ in many proteins without large structural perturbations. This is due to their very similar sizes (0.97Å and 0.99 Å), and their identical charges. Despite this, Cd2+ substituted PSII is inactive. Two properties are therefore important in the choice of ion used: the ionic radius and the pKa of the aqua ion, as it is believed to act as a Lewis base. The following table tabulates many of the ions that can be substituted for Ca2+.
The similarity between the two ions that create functional catalytic sites is the pKa value, not the radius. However, due to its larger radius, Sr2+ does not a fit ideally in the compound, as the bond between it and the oxygen evolving complex is not as tight as with cakcium. The result of an incorrect Lewis acidity is a coordinated water which is too strong or too weak a Brønsted acid, if water is too strong an acid then it deprotonates to form an unreactive metal cation-bound OH-. The protonation state of the Ca2+ bound water is H2O. Therefore calcium ions are found in natural PSII. Other ions fail to support oxygen evolution as their Lewis activity is out of the range required for activity or are unable a bond in the proper site due to improper ionic size. It is believed that calcium has the structural role of stabilizing the Mn cluster, but also the important mechanistic role of restricting access of substrate water to the Mn site. Therefore, the calcium ion plays a crucial role in the formation of the O-O bond and is more than just a structural component.
In attempts at creating artificial manganese catalysts, it has been found that not only is the structure of the core very important to obtaining an active and effective catalyst, but so are the oxide ligands that surround it. Scientists originally focused on synthesizing basic catalysts such as MnO2 or Mn2O3 or Mn network polymers with certain forms (spinel structure among others). However, they soon found that, as stated by Ruttinger and Dismukes, these compounds are not active as water-oxidation catalysts without the disruption of the solid structures as in colloids or freshly precipitated manganese (hydr)oxides. The reduction potentials of these oxides to form Mn(II) are also insufficient for the very demanding oxidation water. The reduction potential of Mn (IV) and Mn(III) to Mn(II)are only 0.6 V and 0.2V respectively which falls far short of the natural enzyme’s 1.1V value. Another major issue with current artificial catalysts is a low selectivity rate, very few catalysts have one of over 90%, which results in oxidation and destruction of the system. Therefore, the natural enzyme must be able to increase the reduction potential by coordination of certain protein ligands but above all else, stabilize the catalyst and increase its selectivity.
The manganese core of the enzyme is situated in between two symmetrically arranged proteins called 43 and 47 kDa which are known to play a role in light collection as they contain chlorophyll. These polypeptides contain two large loops which are electron donors which act as insulators to contain the reducing effects of the active site and are believed to contribute to the binding site of the Mn cluster. Cytochrome b559 also plays a role in protecting the reaction center against oxidative damage by transferring certain electrons to prevent oxidation or repair its effects. There are three extrinsic polypeptides, the 33, 23 and 17 kDa polypeptides that serve to insulate the catalytic site from reductive attack and to maintain Ca2+ (23 kDa) and Cl-(33, 23 and 17 kDa (C. Goussias et al.). In other words these proteins stabilize the enzyme by limiting the destructive reducing capabilities to the water molecules and to these proteins themselves. There are many other amino acids and polypeptides which play crucial roles in the evolution of water but are difficult to replicate as most are still unknown.
The oxidation of water into hydrogen and oxygen requires the removal of four electrons. Therefore, in principle, it is possible that several reaction centers share the same catalytic site and thus four electrons would be removed from water nearly simultaneously. However, in reality, PSII functions on a one photon per oxidizing equivalent system. This was first discovered by Joliot who used bright flashes of light to produce one charge separation per reaction center. If there was only one step in the oxidation of water, then there would be a turnover of oxygen beginning after the first flash. However, Joliot found that four photochemical turnovers were necessary to produce O2 and therefore that each catalytic site were connected to only one reaction center. In other words, four photons must react with each reaction center before there is a chemical turnover of O2. From this principle, Kok developed a model known as the s-state cycle to illustrate the kinetics of the oxidation of water.
In this diagram, each s-state represents an oxidation state of H2O. As we can see, the energy from 4 photons (hv) is necessary to produce one O2 molecule. Kok noted that this pattern showed no O2 evolution on the first or second flash, a maximal yield after the third and a substantial yield after the fourth. He then found that the maximal yield repeated on every fourth flash. Kok explained these results by stating that the oxygen evolving complex could exist in 5 states: S0 – S4. He explained that one photochemical turnover was necessary for each state from S0 – S4 and that S4 would spontaneously decay to S0 with the release of O2. To account for the maximal yield on the third flash, Kok explained that the major stable state in the dark was the S1 state. To account for the turnover on the fourth flash, he said that the S0 state was also a stable state in the dark, but less common than the S1 state.
During the S state cycle, charge is known to accumulate on the Mn cluster. In steps S0 to S1 and S1 to S2, one oxidizing equivalent is stored on the Mn cluster. The most likely Mn valence values for each of these states are Mn(II) Mn(III) Mn(IV) Mn(IV) on S0, Mn(III) Mn(III) Mn(IV) Mn(IV) on S1 and Mn(III) Mn(IV) Mn(IV) Mn(IV) for S2. As we can see, the catalyst attempts to equalize the valence changes on each atom as it accumulates electrons. Unlike the previous states, the valence of the Mn atoms in the S3 state has not been able to be proven. The simplest answer to this problem would be that Mn underwent another straightforward oxidation from S2 to S3. However, opinion is divided between this and the possibility that a different moiety such as histidine or a bridging oxo group in the cluster undergoes oxidation. The S3 to S4 to S0 state changes cause the reduction of a tyrosyl radical when oxygen is produced. The S4 state is transient and temporary and therefore valences have not yet been resolved in spectroscopic studies.
Due to the large number of proposed mechanisms, I will only review important truths that have been proven along with some likely complete mechanisms. It has been proven by mass spectrometry that the lower S states (up until S3) contain a non-exchangeable form of water, is part of the enzyme and could not yet exist on its own. Therefore, the O-O bond must be formed in a later stage, perhaps S4. I will review proposals which are based on the assumption that due to the presence of Mn in the core, Mn redox chemistry will occur as will water chemistry so long as the molecule is bound to the enzyme. Within this larger group, there are two major or classes that proposed mechanisms can be placed into. The first involves the O-O bond formation due to a coupling of µ-oxo ligands. The second involves the coupling reaction of an oxyl radical which surfaced after it was theorized that the Mn cluster may not undergo oxidation in the S2-S3 step.
The first proposed mechanism for O-O bond formation was published by Brudvig and Crabtree in 1986. This mechanism suggests that a structural conversion from Mn4O6 to Mn4O4 results in the formation of the oxygen bond. In this mechanism, the S0 to S4 states each involve the removal of one electron from the manganese by the light driven turnover of PSII. The oxygen is then released in the spontaneous conversion from S4 back to S0. It also states that one proton is removed in both the S0 to S1 and S2 to S3 steps and that two more are removed in the steps S3 to S0. The release of these protons could be interpreted by either the deprotonation of an OH- ligand to O2- or the deprotonation of a protein functional group. This suggests that the oxidations of Mn4O4 leads to a sufficient electron deficiency that the manganese coordinates two more water molecules to form a Mn4O6 adamantane ligand. The O-O bond then formed between what were bridging oxos within the Mn cubane. This theory has now been proven to be false through X-ray spectroscopy which eliminated the possibility of the proposed structures. However, this was an important proposal as it introduced the bridging of oxos to form the O-O bond which is now considered a very probable possibility. A distorted cubane model in the high S states has also begun to be reconsidered due to suggestions by EPR studies.
Due to the lack of an X-ray absorption edge change from the S2-S3 states, it has been proposed that a bridging oxo radical undergoes oxidation in this step. It was then suggested that the bridged oxo group undergoes oxidation in the following step which results in the O-O bond formation. The O2 is then released with one oxygen atom originating from the core complex as well as one from the bridging radical.
One of the most important questions regarding the mechanism of oxygen evolution is the nature of substrate binding during catalysis. This is determined by the site and mode of binding, what is bound to what in which way. Unfortunately, this is still very unclear and there is evidence which points to many different theories. Some authors suggest terminal water binding, which supports the first proposed mechanism, while others suggest conversion of substrate water into a µ-oxo bridge, which supports the second reviewed mechanism. Solving this question would obviously result in a significant advancement in narrowing the possible reaction path and thus move us along the path to finding an effective artificial catalysis.
Important Characteristics of Artificial Catalysts
The ultimate goal of researching the mechanism of water oxidation and the structure of the natural oxygen evolving complex is to help with the understanding of the characteristics necessary for the creation of an efficient, long lived system for splitting water to H2 and O2. Efficiency is the ratio of energy received to energy produced and conserved. Thus, if the hydrogen and oxygen produced by 10 J worth of incident photons have a fuel value of 1 J, the efficiency is 10%. A long lived system is defined as a system that does not need consistent repairs or replacement of materials or catalysts used. For this to be true, the catalyst used must be very stable so as not to oxidize the system itself to inactivity, and thus requiring replacement.
It is important that the catalytic site be composed of a substance with multiple oxidation states to guarantee activity. Manganese is used in nature as it has very many consecutive stable oxidation states (7, 6, 4, 3, 2, 0, -1), important due to the necessity that manganese be oxidized consecutively in each turnover. While carbon and oxygen both have more (nine and eight, respectively), it is important that the majority of the oxidation states be positive as the element is undergoing oxidation and thus they are not used in nature. Other elements which have been considered by researchers are Fe-, Co- and Ru- hydroxides which, as transition metals, also have a wide set of stable consecutive oxidation states. Another important characteristic of manganese is the proximity of various oxidation degrees (G.L. Elizarova et al.) which distinguishes it from other similar compounds. It is believed that the closeness of these electrochemical potentials leads to the smoothing of the energy relief and a consistent rate of supply of electrons and protons per photon. It is also important that the compound have a polynuclear core. This will be able to accomplish a straight four electron redox reaction more effectively as it will also help smooth the energy relief. This table also suggests that Mn3+ does not require as many strong oxidants as Fe3+ or Co3+
The accessibility and affinity of the catalytic sites are also very important. It is important to have a developed surface, to maximize the number of accessible sites. If in an aqueous solution, it is very important that the catalyst has the greatest affinity for the medium so as to ensure that other molecules do not interfere with the water and the reaction. As mentioned before, a catalyst’s ligands are very important, however these ligands must not be easily oxidized, otherwise there may be side processes which occupy important active sites and slow down the reaction or even destroy the system.
As we can see, it is very difficult to determine an effective catalyst theoretically without more information and certainty about the reaction mechanism in the natural enzyme. Researchers have developed many different catalysts which are active, albeit function very inefficiently or are very instable, mainly with manganese, iron or ruthenium cores. We understand the shape of the active core and therefore are able to build other manganes-oxo cubanes, such as done by Ruettinger and Dismukes, however, we are unable to identify all of the important steps of oxidation in the S-state cycle and therefore are unable to deduce an accurate mechanism. This hinders our ability to properly stabilize and optimize the catalyst. It may seem that the simplest way to create an effective catalyst would be to imitate exactly the structure of PSII, however, the synthesis of this structure in nature is equally as mysterious to us as the mechanism of oxidation of water itself.
Nature has spent millennia perfecting the phenomenon of photosynthesis through a process of trial and error known as evolution, and therefore for the human race to speed this process, we need to theorize the ideal catalyst and certain necessary characteristics. Therefore in our goal to optimize a catalyst for this reaction, researchers must continue to observe the mechanism and most importantly deduce the oxidation state of the manganese core during the S3 stage. However, another possible manner of deducing the mechanism is through studying the steps in artificial catalysts, which may lead to confirming the energetically and structurally most efficient manner of oxidizing water, be it the same manner as nature or not.
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Table of data and Information from G.W. Brudvig 2008
G.W. Elizarova et al. 2000