A fully optimized resting state model with a strong Fe-H delta-center dot center dot center dot H delta+-O dihydrogen bond for the active site of the third type of hydrogenase, [Fe]-hydrogenase, is proposed from density functional theory (DFT) calculations on the reformulated active site from the recent X-ray crystal structure study of C176A (Cys176 was mutated to an alanine) mutated [Fe]-hydrogenase in the presence of dithiothreitol. The computed vibrational frequencies for this new active site model possess an average error of only +/- 4.5 cm(-1) with respect to the wild-type [Fe]-hydrogenase. Based on this resting state model, a new mechanism with the following unusual aspects for hydrogen activation catalyzed by [Fe]-hydrogenase is also proposed from DFT calculations. (1) Unexpected dual pathways for H-2 cleavage with proton transfer to Cys176-sulfur or 2-pyridinol's oxygen for the formation and regeneration of the resting state with an Fe-H delta-center dot center dot center dot H delta+-O dihydrogen bond before the appearance of methenyl-H4MPT+ (MPT+). (2) The strong dihydrogen bond in this resting state structure prevents D-2/H2O exchange. (3) Only upon the arrival of MPT+ with its strong hydricle affinity can D-2/H2O exchange take place as the arrival of MPT+ triggers the breaking of the strong Fe-H delta-center dot center dot center dot H delta+-O dihydrogen bond by taking a hydride from the iron center and initiating the next H-2 (D-2) cleavage. This new mechanism is completely different than that previously proposed (J. Am. Chem. Soc. 2008, 130, 14036) which was based on an active site model related to an earlier crystal structure. Here, Fe's role is H-2 capture and hydride formation without MPT+ while the pyridone's special role involves the protection of the hydride by the dihydrogen bond.