The P-cluster is a unique iron-sulfur center that likely functions as a dynamic electron (e(-)) relay site between the Fe-protein and the catalytic FeMo-cofactor in nitrogenase. The P-cluster has been shown to undergo large conformational changes upon 2-e(-) oxidation which entail the coordination of two of the Fe centers to a Ser Side chain and a backbone amide N, respectively. Yet, how and if this 2-e(-) oxidized state (P-ox) is involved in catalysis by nitrogenase is not well established. Here, we present the crystal structures of reduced and oxidized MoFe-protein (MoFeP) from Gluconacetobacter diazotrophicus (Gd), which natively possesses an Ala residue in the position of the Ser ligand to the P-cluster. While reduced GdMoFeP is structurally idential to previously characterized counterparts around the FeMo-cofactor, oxidized GdMoFeP features an unusual Tyr coordination: to its P-cluster along with ligation by a backbone amide nitrogen. EPR analysis of the oxidized Gd-MoFeP P-cluster confirmed that it is a 2-e- oxidized, integer-spin species. Importantly, we have found that the sequence positions, corresponding to the Ser and Tyr ligands are almost completely covariant among Group I nitrogenases. These findings strongly support the possibility that the Pox state is functionally relevant in nitrogenase catalysis and that a hard, O-based anionic ligand serves to stabilize this state in a switchable fashion.