This work provides new insights into local active site structural changes that yield energetics consistent with experimentally measured allosteric rate acceleration in IGPS. The hypothesized Val51 backbone flip leads to a more favorable reaction pathway via oxyanion hole stabilization, supporting the longstanding hypothesis to explain the observed allosteric effect. However, this work reveals that this is not the only plausible configuration to yield the expected catalytic effect, as the Gly52 N-H is also a capable oxyanion hole contributor. Oxyanion stabilization via Gly52 has been proposed previously, however, most studies to date have focused on the Val51 dihedral flip. When the Val51 backbone of the Active model is manually modified to mimic the Inactive structure the Gly52 N-H becomes a suitable oxyanion hole donor. These results show that multiple active site conformations are catalytically competent and reveal the positioning of the oxyanion strand is a definitive structural change required for proper oxyanion hole formation.