Scientists Determine Structure of Third Hydrogenase Enzyme; Insights Could Lead to Better Hydrogen Catalysts
|Superimposed active-site structure of the three phylogenetically unrelated hydrogenases: [NiFe]-hydrogenase, [FeFe]-hydrogenase, and [Fe]-hydrogenase. Click to enlarge. Credit: Shima et al. (2008), Science|
Some microbes use hydrogenases (enzymes) in their energy metabolism to catalyze H2/H+ interconversion reactions (H2 ⇋ 2H+ +2e–); these hydrogenases are more efficient catalysts than platinum, which is commonly used industrially to catalyze hydrogenation. There are three known and phylogenetically unrelated types of hydrogenases: [NiFe]-hydrogenases, [FeFe]-hydrogenases, and [Fe]-hydrogenase.
The structures of the first two hydrogenases—which have a pair of metal atoms (either two iron atoms or an iron and a nickel atom) at their active sites—were known. Now, scientists in Germany have discovered the structure of the third type of hydrogenase—which has but the single iron atom at the active site—and shown that all three known hydrogenases have obvious structural similarities, including active sites that contain an iron atom linked to a CO group. Their work is reported in the 25 July issue of the journal Science.
The related iron ligation pattern of hydrogenases exemplifies convergent evolution and presumably plays an essential role in H2 activation. This finding may stimulate the ongoing synthesis of catalysts that could substitute for platinum in applications such as fuel cells.—Shima et al. (2008)
The team, lead by led by Seigo Shima at the Max-Planck-Institut für Terrestrische Mikrobiologie and Ulrich Ermler at the Max-Planck-Institut für Biophysik, found several common structural features among the three different hydrogenases:
All three types contain a redox-inactive low-spin iron that is asymmetrically ligated by five or six ligands arranged as a distorted square pyramid or octahedron.
Three π-accepting ligands comprising CO, cyanide, or pyridinol (considered as a cyanide functional analog) are oriented perpendicular to each other in a geometrically related manner, and a thiolate sulfur always coordinates the iron trans to a diatomic molecule.
All three iron centers act together with a redox-active partner—methenyl-H4MPT+ in the case of [Fe]-hydrogenase, the distal iron in the case of [FeFe]-hydrogenase, and nickel in the case of [NiFe] hydrogenase—whose spatial position relative to the other ligands is also similar.
Apparently, these related iron centers, with unusual nonproteinaceous ligands thought to be synthesized by three different enzymatic machineries and embedded into three architecturally different hydrogenase structures, evolved independently. Remarkably, hydrogenases are the only metalloenzymes that use toxic CO and cyanide (or pyridinol) as metal ligands. Thus, hydrogenases are an impressive example of convergent evolutionary development as a consequence of specific biological and/or chemical restraints. However, the intrinsic physicochemical properties of the unique iron ligation pattern are not yet understood, nor are their implications for the technologically important H2 activation reaction.—Shima et al. (2008)
The researchers also found that although there are structural similarities among the three, the [Fe]-hydrogenase uses a fundamentally different enzymatic mechanism from the other two because of the different nature of the redox-active partner and the accompanying electron delivery mode.
The [Fe]-hydrogenase reported by Shima et al. is different, because the hydride generated by splitting H2 is transferred directly to an electrophilic organic center in methenyl-tetrahydromethanopterin (methenyl-H4MPT), accomplishing a key stage in the reduction of CO2 to CH4...Only one metal is required for catalysis, which does not seem to require any formal change in oxidation state. In the classic [FeFe]- and [NiFe]-hydrogenases, the presumed role of the second metal is to orchestrate, in part or in full, the two one-electron transfers that subsequently convert H- to H+. The [Fe]-hydrogenase is thus very important for our understanding of H2 biocatalysis in general because it fulfills all the requirements for its activation and scission, the first stages of H2 oxidation by the classic hydrogenases.
...The remarkable convergent evolution that resulted in the presence of a common active-site Fe(CO)x(RS-) unit in all three classes of hydrogenases deserves a comment. The π-acceptor nature of CO (and hydrogen-bonded CN-) stabilizes low-spin, low-valence Fe with catalytic and hydride-binding properties that are normally found in second- and third-row transition metals, most notably platinum. Presumably, such metals were not available during evolution, and nature found a solution involving the much more common Fe ion and the abundant ligands CO and CN-.—Armstrong and Fontecilla-Camps (2008)
Seigo Shima, Oliver Pilak, Sonja Vogt, Michael Schick, Marco S. Stagni, Wolfram Meyer-Klaucke, Eberhard Warkentin, Rudolf K. Thauer, Ulrich Ermler (2008) The Crystal Structure of [Fe]-Hydrogenase Reveals the Geometry of the Active Site. Science 25 July 2008: Vol. 321. no. 5888, pp. 572 - 575 doi: 10.1126/science.1158978
Fraser A. Armstrong and Juan C. Fontecilla-Camps (2008) A Natural Choice for Activating Hydrogen. Science 25 July 2008: Vol. 321. no. 5888, pp. 498 - 499 doi: 10.1126/science.1161326