Seminar: Computational Bioinorganic Chemistry | January 13 | 4 p.m.-5 p.m. | Zoom
Ragnar Björnsson, Researcher, Laboratoire Chimie et Biologie des Métaux, CEA Grenoble, France.
New insights into the electronic structure basis of biological nitrogen reduction
Host: Nuno A. G. Bandeira
Zoom: https://videoconf-colibri.zoom.us/j/97493983798?pwd=ajV5bE0yS29WNGhvNDN3VzRVOXpEdz09
The nitrogenase enzymes catalyze the difficult redox reaction of dinitrogen to ammonia. The mode of action of these enzymes remains poorly understood, however, despite decades of detailed structural characterization studies. The MoFe protein of molybdenum nitrogenase contains a metal-sulfur cluster, FeMoco, where N2 binding and reduction takes place. The resting state of FeMoco (E0) has been characterized by crystallography, multiple spectroscopic techniques (XAS, Mössbauer, EPR) and theory (broken-symmetry DFT). The highly complex electronic structure, involving spin coupling of 8 high-spin metal ions, delocalized electrons and weak metal-metal bonding, is not completely understood [1-4] and even less is known about the other redox states of the cofactor (E1-E8). Spectroscopic studies have proposed hydrides to be present in E2-E4, importantly prior to binding of dinitrogen, and reductive elimination of H2 via these hydrides explains the obligatory H2 formation upon N2 binding. Our theoretical studies for the past few years are aimed at characterizing in electronic-structure detail the redox states of FeMoco. Our QM/MM BS-DFT protocol gives a calculated E0 structure of FeMoco in excellent agreement with the high-resolution crystal structure, and reveals a strong sensitivity to both redox state and spin-coupling treatment [4]. Recently, we have shown that the strong sensitivity of FeMoco metal-metal distances on DFT approximations is also found in simpler [Fe2S2] dimers and can be traced back to the calculated covalency the Fe-S bond [5]. The potential energy surfaces of the E2 and E4 redox states have been explored by QM/MM calculations [6,7]. Bridging hydrides are found to be preferentially stabilized between belt Fe ions due to the hemilability of protonated belt sulfides. Interestingly, our model for the E4 state reveals favorable N2 binding and offers a chemically intuitive explanation for why N2 binding occurs in this state and not in others. Furthermore, the geometry of the N2-bound state reveals a plausible reductive elimination step (H2 elimination via hydrides) leading to a reduced FeMoco state that partially activates N2 for protonation [7]. Finally a systematic study of the mechanism of CO inhibition has recently been described [8].
References
[1] R. Bjornsson, F. A. Lima, T. Spatzal, T. Weyhermüller, P. Glatzel, E. Bill, O. Einsle, F. Neese, S. DeBeer, Chem. Sci. 2014, 5 , 3096-3103.
[2] R. Bjornsson, F. Neese, R. R. Schrock, O. Einsle, S. DeBeer, J. Biol. Inorg. Chem. 2015, 20, 447-460.
[3] R. Bjornsson, F. Neese, S. DeBeer, Inorg. Chem. 2017, 56, 1470-1477.
[4] B. Benediktsson, R. Bjornsson, Inorg. Chem. 2017, 56, 13417-13429.
[5] B. Benediktsson, R. Bjornsson, J. Chem. Theory Comput. 2022, 18, 1437-1457.
[6] A. Th. Thorhallsson, R. Bjornsson, Chem. Eur. J., 2021, 67, 16788-16800.
[7] A. Th. Thorhallsson, B. Benediktsson, R. Bjornsson, Chem. Sci. 2019, 10, 11110-11124.
[8] N. Spiller, F. Neese, R. Bjornsson, S. DeBeer, Inorg. Chem. 2021, 60, 18031-18047.