Vibrational Pertubation of the FeFe Hydrogenase H-Cluster Revealed by a C2H ADT

Vladimir Pelmenschikov (1) , James A. Birrell (2) , Leland B. Gee (3) , Casseday P. Richers (4) , Edward J. Reijerse (2) , Hongxin Wang (5) , Simon Arragain (6) , Nakul Mishra (7) , Yoshitaka Yoda (8) , Hiroaki Matsuura (9) , Lei Li (8) , Kenji Tamasaku (8) , Thomas B. Rauchfuss (4) , Wolfgang Lubitz (2) , Stephen Cramer (5)

1 Institut für Chemie [TUB Berlin]
2 Max Planck Institute for Chemical Energy Conversion
3 Department of Chemistry [Stanford]
4 School of Chemical Sciences
5 SETI Institute
6 IFPEN - IFP Energies nouvelles
7 UC - University of California
8 JASRI - Japan Synchrotron Radiation Research Institute [Hyogo]
9 RIKEN RSC - RIKEN SPring-8 Center [Hyogo]

[FeFe] hydrogenases are highly active catalysts for the interconversion of molecular hydrogen with protons and electrons. Here, we use a combination of isotopic labeling, 57Fe nuclear resonance vibrational spectroscopy (NRVS), and density functional theory (DFT) calculations to observe and characterize the vibrational modes involving motion of the 2-azapropane-1,3-dithiolate (ADT) ligand bridging the two iron sites in the [2Fe]H subcluster. A −13C2H2– ADT labeling in the synthetic diiron precursor of [2Fe]H produced isotope effects observed throughout the NRVS spectrum. The two precursor isotopologues were then used to reconstitute the H-cluster of [FeFe] hydrogenase from Chlamydomonas reinhardtii (CrHydA1), and NRVS was measured on samples poised in the catalytically crucial Hhyd state containing a terminal hydride at the distal Fe site. The 13C2H isotope effects were observed also in the Hhyd spectrum. DFT simulations of the spectra allowed identification of the 57Fe normal modes coupled to the ADT ligand motions. Particularly, a variety of normal modes involve shortening of the distance between the distal Fe–H hydride and ADT N–H bridgehead hydrogen, which may be relevant to the formation of a transition state on the way to H2 formation.

Keywords: hydrogenase; 2-azapropane-1; 3-dithiolate; catalysis; NRVS; DFT

Domains: Chemical Sciences; Environmental Sciences

Vladimir Pelmenschikov, James A. Birrell, Leland B. Gee, Casseday P. Richers, Edward J. Reijerse, et al.. Vibrational Pertubation of the FeFe Hydrogenase H-Cluster Revealed by a C2H ADT. Journal of the American Chemical Society, 2021, 143 (22), pp.8237-8243. ⟨10.1021/jacs.1c02323⟩. ⟨hal-03291508⟩