The conversion of atmospheric nitrogen to ammonia is a crucial process for life on earth. Ammonia is needed in the production of fertilizers, as well as for the manufacturing of a wide range of products ranging from household cleaning products to explosives. From a more fundamental biological perspective, nitrogen atoms are also constituents of amino acids and nucleic acids, which constitute the building blocks of proteins and nucleic acids in all organisms.
The biological conversion of nitrogen to bioavailable ammonia utilizes an iron-molybdenum cofactor found in the nitrogenase enzyme. This enigmatic complex cluster has motivated considerable efforts in understanding its structure and its relation to nitrogen reduction. Prof. DeBeer’s group (Department of Inorganic Spectroscopy) has been studying the geometric and electronic structure of this cofactor utilizing a wide range of X-ray-based spectroscopic methods for nearly a decade. The recent application of an advanced technique called X-ray Magnetic Circular Dichroism (XMCD) spectroscopy has provided an answer to a hypothesis first proposed in 2014 based on computational approaches in collaboration with the group of Prof. Frank Neese (MPI für Kohlenforschung). Dr. Ragnar Björnsson, currently group leader in the department of Inorganic Spectroscopy, suggested an unusual electron spin orientation at the single Mo atom present in the cofactor, with two out of three electron spins being oriented down and one up (Bjornsson et al. (2014). Chemical Science 5, 3096-3103). Now, this unusual electronic structure finally has experimental support.
"The whole project was from the beginning very challenging. We not only needed a bright light source like synchrotron radiation to probe one atom in large complex, but we also used its’ polarization advantage that allowed us to effectively excite spin-up or spin-down electrons separately. In a simple picture, we could tune the energy of the light to probe either iron or molybdenum atoms in the FeMo cofactor or a molecular model complex and detect electron spins of different orientation. Luckily, such measurements were possible at one of the unique beamlines at Advanced Photon Source in Argonne, USA. In our measurements, we focused on the FeMo cubane that is a structural mode complex of the FeMo cofactor, and as a reference, we used a well-characterized molecular compound with three electron spins up at the molybdenum atom. We got very different spectra from these complexes although both possess a molybdenum atom in a +3 oxidation state. On this basis, we could not only provide evidence for different electronic structure of the Mo atom in this compounds, but also for the first time support the proposed non-Hund configuration at the Mo atom in the FeMo cubane complex” explains Dr. Joanna Kowalska, former postdoctoral fellow in Prof. DeBeer’s group.
These findings demonstrate the in-depth information regarding electronic structure that can be achieved only by utilizing XMCD and form a foundation for future selective studies of different biological catalysts. This information might help to design future effective catalysts based on lessons learned from Nature.
The results of this study were recently published in Angewandte Chemie International Edition and chosen by the Editor as “Hot Paper” for its “importance in a rapidly evolving field of high current interest” and also featured as inside cover.
The paper was also highlighted by the Argonne National Laboratory.
Publication: Kowalska, J.K., Henthorn, J.T., Van Stappen, C., Trncik, C., Einsle, O., Keavney, D., DeBeer, S. (2019). X‐ray Magnetic Circular Dichroism Spectroscopy Applied to Nitrogenase and Related Models: Experimental Evidence for a Spin‐Coupled Mo(III) Center Angewandte Chemie International Edition 58(28), 9373-9377. https://doi.org/10.1002/anie.201901899