Facilitated hydride binding in an Fe-Fe hydrogenase active-site biomimic revealed by X-ray absorption spectroscopy and DFT calculations.
Iron-only hydrogenases are high-efficiency biocatalysts for the synthesis and cleavage of molecular hydrogen. Their active site is a diiron center, which carries CO and CN ligands. Remarkably, the two iron atoms likely are connected by a non-protein azadithiolate (adt = S-CH2-NH-CH2-S). To dwell on the role of the adt in H2 catalysis, a specific biomimetic diiron compound, 1 = [Fe2(mu-adt-CH2-Ph)(CO)4(PMe3)2], with unprecedented positive reduction potential, has been synthesized and crystallized previously. It comprises two protonation sites, the N-benzyl-adt nitrogen that can hold a proton (H) and the Fe-Fe bond that will formally carry a hydride (Hy). We investigated changes in the solution structure of 1 in its four different protonation states (1', [1H]+, [1HHy]2+, and [1Hy]+) by X-ray absorption spectroscopy at the iron K-edge. EXAFS reveals that already protonation at the adt nitrogen atom causes a change of the ligand geometry involving a significant lengthening of the Fe-Fe distance and CO and PMe3 repositioning, respectively, thereby facilitating the subsequent binding of a bridging hydride. Hydride binding clearly is discernible in the XANES spectra of [1HHy]2+ and [1Hy]+. DFT calculations are in excellent agreement with the experimentally derived structural parameters and provide complementary insights into the electronic structure of the four protonation states. In the iron-only hydrogenases, protonation of the putative adt ligand may cause the bridging CO to move to a terminal position, thereby preparing the active site for hydride binding en route to H2 formation.
Freie Universität Berlin, Institut für Experimentalphysik, Arnimallee 14, 14195, Berlin, Germany.
Simone
S
Löscher
Lennart
L
Schwartz
Matthias
M
Stein
Sascha
S
Ott
Michael
M
Haumann
D001665:Binding Sites; D032701:Biomimetics; D004583:Electrons; D006859:Hydrogen / Q000737:chemistry* / Q000378:metabolism*; D006864:Hydrogenase / Q000737:chemistry* / Q000378:metabolism*; D007501:Iron / Q000737:chemistry*; D007506:Iron-Sulfur Proteins / Q000737:chemistry* / Q000378:metabolism*; D008024:Ligands; D015394:Molecular Structure; D013053:Spectrophotometry; D014965:X-Rays
D007506:Iron-Sulfur Proteins; D008024:Ligands; D006859:Hydrogen; D007501:Iron; C118830:iron hydrogenase; D006864:Hydrogenase