Lubitz, Reijerse & Messinger have published a fascinating review into the intricacies of photosystem II and hydrogenases that produce hydrogen – Note the marvels within Darwn’s blob of “protoplasm”. It is most interesting that Lubitz et al. address the design principles that we can learn from “nature” and apply to creating synthetic photochemical biosynthetic water splitting systems.Though attributed to “nature”, recognizing design principles and applying them are easily understood at the Max Planck Institut für Bioanorganische Chemie. I wonder when No. America will catch up? From the very detailed complexity described, I highly expect some “irreducibly complex” systems are present. Any candidates? Following are a few extracts from this excellent review.
Wolfgang Lubitz, Edward J. Reijerse and Johannes Messinger
Max Planck Institut für Bioanorganische Chemie, Germany.
Energy Environ. Sci., 2008 DOI: 10.1039/b808792j
This review aims at presenting the principles of water-oxidation in photosystem II and of hydrogen production by the two major classes of hydrogenases in order to facilitate application for the design of artificial catalysts for solar fuel production. . . .
. . .A promising way for light-driven water splitting would be to mimic the molecular and supramolecular organization of the natural photosynthetic system, i.e. artificial photosynthesis.12,13 . . .
. . .Light-induced water-splitting and release of oxygen and protons is performed in nature in oxygenic photosynthesis by green plants, algae and cyanobacteria. The responsible highly complex enzyme is called photosystem (PS) II.14 Many green algae and cyanobacteria also contain an enzyme that can convert the released protons into dihydrogen. This enzyme is called hydrogenase.15,16 The process is depicted in Fig. 1, together with a view of the respective protein complexes17,18 and a possible scheme mimicking the natural process in vitro.19 . . .
. . .Knowledge of the basic principles of water oxidation and hydrogen conversion in nature is a goal of major importance both for basic research and possible application in our society. This would allow us to use the organisms – or the isolated enzymes – in biotechnological processes.20–23 Furthermore, it would provide the foundation for designing biomimetic – or bioinspired – artificial catalysts for large-scale water splitting and hydrogen production in the future. . . .
. . .It is therefore surprising that evolution has, in contrast to for example hydrogenases (see below), created only one unique catalyst capable of performing light-induced water-splitting, which is known as photosystem II (PSII). It is also remarkable that so far only very minor differences have been found on the level of the water-splitting complex between different organisms such as higher plants, green algae and cyanobacteria. This uniqueness underpins the high level of complexity that is required to perform this strongly oxidizing reaction within a protein matrix. . . .
. . .Photosynthetic organisms have devised an efficient repair mechanism to solve this problem. By this mechanism the most damage sensitive part, the D1 protein, is selectively exchanged against a newly synthesized replacement protein. Then the Mn4OxCa cluster is reassembled via a light-driven process known as photo-activation.73. . .
. . .From the above text the following seven principles of photosynthetic water splitting can be extracted:
1. The components of the primary photo-reactions as well as the Mn4OxCa cluster are supported by protective components and, once destroyed, automatically replaced by the organism by a specific repair mechanism.
2. A multimeric transition metal complex (Mn4OxCa cluster) is employed to couple the very fast one–electron photochemistry with several orders of magnitude slower four electron water-splitting chemistry.
3. The water-splitting catalyst is located in a sequestered environment; channels exist for substrate entry and product release.
4. The matrix (protein) around the Mn4OxCa cluster is highly important for the coupling of proton and electron transfer reactions. This feature is essential for achieving about equal redox potentials for all oxidation steps that match the oxidizing potential of the light-generated primary oxidant.
5. Point 4 leads to a decoupling of the release of the two products O2 and H+ from the catalytic site.
6. The substrate water molecules are stepwise prepared for O–O bond formation by binding to the Mn4OxCa cluster and by (partial) deprotonation. The concerted oxidation of the activated substrate occurs then either in two 2 e? or one concerted 4 e? reaction step(s). This avoids high energy intermediates.
7. The Mn4OxCa cluster undergoes several structural changes during the Kok cycle, which are probably significant for the mechanism. The surrounding matrix therefore needs to be flexible enough to support such changes.
For a better understanding of the design principles of native hydrogenases a comparison of the two major hydrogenases is useful.
The two groups of hydrogenases have a completely different genetic background. Whereas the [NiFe] group is widely distributed in prokaryotes (mostly sulfur reducing bacteria), the [FeFe] group is less widely distributed but occurs in both prokaryots and eukaryots (algae, yeast). In fact, the genetic signature of the H-cluster is found in many higher organisms, even in homo sapiens. The [FeFe] hydrogenases are, in general, most active in H2 production while [NiFe] hydrogenases are more tuned to H2 oxidation. Both types are however bidirectional. Organisms employing [NiFe] hydrogenases are found in regions with higher oxygen levels than those using [FeFe] hydrogenase. This is because [FeFe] hydrogenases are extremely oxygen sensitive and will be inhibited irreversibly under O2. [NiFe] hydrogenases are, in general, more oxygen tolerant and some enzymes even evolve H2 under O2.
On the other hand, there are many similarities between the basic structures of the active site in both enzymes:
1. Both enzymes employ a bimetallic center where the chemistry is taking place.
2. Both active sites have a butterfly-shaped core in which the two metals are bridged by SR-ligands.
3. Only one of these metal atoms is redox active (Ni in [NiFe] and Fed in [FeFe] hydrogenase) and they both have a d7 configuration (Ni(III) and Fe(I), respectively) in their active states.
4. In both catalytic sites the Fe atom is kept at a low valence by the strongly donating ligands CN? and CO.
5. The metal-metal distance in both structures is short (2.5–2.9 ), indicating a metal–metal bond.
6. One metal with an open coordination site can be identified in both active states. This is the site where H2 is believed to bind or is being released.
7. The H/D-isotope effect shows that in both cases the H2 splitting is heterolytic
8. In both active sites a sulfur or nitrogen/oxygen ligand probably acts as base to accept or donate the H+.
9. For both enzymes the catalytic activity is often inhibited by O2 and CO.
These features can serve as guidelines for the construction of biomimetic hydrogenase models. . . .
See full article: Solar water-splitting into H2 and O2: design principles of photosystem II and hydrogenases