The structure of vanadium nitrogenase reveals an unusual bridging ligand

Abstract

Nitrogenases catalyze the reduction of N2 gas to ammonium at a complex heterometallic cofactor. Most commonly this is the FeMo cofactor (FeMoco), a [Mo:7Fe:9S:C] cluster whose exact reactivity and substrate binding mode remain unknown. Alternative nitrogenases replace molybdenum with either vanadium or iron and differ in reactivity, prominently in the ability of vanadium nitrogenase to reduce CO to hydrocarbons. Here we report the 1.35 Å structure of vanadium nitrogenase from Azotobacter vinelandii. The 240 kDa protein contains an additional α-helical subunit not present in molybdenum nitrogenase. The FeV cofactor (FeVco) is a [V:7Fe:8S:C] cluster with a homocitrate ligand to vanadium. Unexpectedly, it lacks one sulfide ion compared to FeMoco that is replaced by a bridging ligand, likely a μ-1,3-carbonate. The anion fits into a pocket within the protein that is obstructed in molybdenum nitrogenase, and its different chemical character helps to rationalize the altered chemical properties of this unique N2- and CO-fixing enzyme.

Tuning Electron Flux through Nitrogenase with Methanogen Iron Protein Homologues

“…Most interestingly, the VnfH Ma /VnfDGK Av complex adopted an energetically least favorable P group of conformations of all VnfDGK Av ‐based complexes; moreover, the P group conformations of the VnfH Ma /VnfDGK Av complex were even slightly less favored than its D group of conformations in the overall binding energy (Figure S4e, right), suggesting docking between the two component proteins at long cluster–interface distances with reduced electron‐transfer efficiencies. A closer examination of the docking models of the VnfH Ma /VnfDGK Av complex in the D group confirmed “improper” docking between these two proteins at cluster–interface distances as far as 8–9 Å with a significant deviation from the conformation of the native VnfH Av /VnfDGK Av complex (Figure a), which could account for an altered product profile of the VnfH Ma /VnfDGK Av hybrid and, most notably, a substantial decrease in the ratio between hydrocarbon‐ and H 2 ‐formation when CO was supplied as a substrate (Table S1). Spectroscopic and biochemical analyses further demonstrated capture of the substrate CO and/or intermediate(s) on VnfDGK Av with the assistance of the “imperfect” electron donor VnfH Ma , suggesting a “re‐purposing” of electrons from CO‐reduction to CO‐binding concomitant with a substantially decreased electron flux (Figure b; Figure S8 in the Supporting Information).…”

Catalytic Reduction of Molecular Dinitrogen to Ammonia and Hydrazine Using Vanadium Complexes

“…[2] Since the report of the first successful example of molybdenum-catalyzed dinitrogen reduction, [2] some successful examples of catalytic dinitrogen reduction systems using other mid-to-late transition-metal dinitrogen complexes as catalysts have been reported by other research groups. [15] Thes tructural similarity between FeMo-and FeV-nitrogenases has inspired inorganic chemists to prepare avariety of vanadium-dinitrogen complexes and investigate their stoichiometric reactivity in detail. [13,14] Arecent study disclosed that the molecular structure of the FeV nitrogenase is quite similar to that of the FeMo nitrogenase.…”

“…[13,14] Arecent study disclosed that the molecular structure of the FeV nitrogenase is quite similar to that of the FeMo nitrogenase. [15] Thes tructural similarity between FeMo-and FeV-nitrogenases has inspired inorganic chemists to prepare avariety of vanadium-dinitrogen complexes and investigate their stoichiometric reactivity in detail. [16,17] In contrast to the stoichiometric reactions of vanadium dinitrogen complexes, vanadium-catalyzed dinitrogen reduction under mild reaction conditions has not been reported to date.S chrock and coworkers previously tried to develop the catalytic conversion of molecular dinitrogen into ammonia by using their vanadium complexes as catalysts;h owever,n oa mmonia was observed from dinitrogen gas.…”

Control of electron transfer in nitrogenase

“…Schematic diagram for the three forms of nitrogenase, where M is Mo, V, or Fe (a) . Shown are the structures for the active site FeMo-cofactor [33] and FeV-cofactor [34] determined by X-ray crystallography and a proposed structure for the FeFe-cofactor (b) . It is noteworthy that some recent work is indicating that changes in the structure of FeMo-co and FeV-co can occur upon addition of electrons and/or upon binding of substrates and inhibitors, suggesting structural dynamics of the cofactor is part of the mechanism.…”