Advanced Electron Paramagnetic Resonance and Density Functional Theory Study of a {2Fe3S} Cluster Mimicking the Active Site of [FeFe] Hydrogenase

• Published in: Journal of the American Chemical Society 2010-12, Vol.132 (49), p.17578-17587
• Main Authors: Silakov, Alexey, Shaw, Jennifer L, Reijerse, Eduard J, Lubitz, Wolfgang
• Format: Article
• Language: English
• Subjects: Biomimetic Materials - chemistry; Catalytic Domain; Clostridium - chemistry; Clostridium - enzymology; Desulfovibrio desulfuricans - chemistry; Desulfovibrio desulfuricans - enzymology; Electron Spin Resonance Spectroscopy; Ferric Compounds - chemistry; Hydrogenase - chemistry; Models, Molecular; Quantum Theory; Sulfur Compounds - chemistry
• ISSN: 0002-7863; 1520-5126
• DOI: 10.1021/ja107793e

Despite extensive investigations of the active site of the [FeFe] hydrogenases, many details concerning the properties of the ”hydrogen converting cluster” are not yet fully understood. The complexity of the so-called H-cluster is one of the main difficulties in studying the properties of its components. The present study is aimed at the mixed-valence EPR active [Fe2(μ-CO)(CO)3(CN)2{MeSCH2C(Me)(CH2S)2}]1− that is structurally closely related to the redox active binuclear part of the H-cluster in its CO-inhibited oxidized state. In this work, we present a characterization of this compound by advanced pulse EPR methods. The accurate determination of the 57Fe, 1H, 2H, 14N, and 15N electron nuclear hyperfine interactions provided a very detailed picture of the electronic structure of this complex. A theoretical study using density functional theory (DFT) calculations identified possible isomers of the compound and further refined the knowledge about its properties. It was found that upon one electron oxidation of the parent Fe(I)−Fe(I) complex, the dominant mixed-valence Fe(I)−Fe(II) species is the one in which the CN ligand of the iron center that is distal to the thioether moves from the basal to the apical position. The unpaired spin distribution of the model complex is found to be clearly different from that of the native H-cluster. These differences are discussed and provide new insight into the functional features of the [FeFe] hydrogenase active site.