[NiFe] hydrogenases catalyze the reversible oxidation of dihydrogen. The corresponding catalytic cycle involves a formidable number of redox states of the Ni-Fe active site; these can be distinguished experimentally by the IR stretching frequencies of their CN and CO ligands coordinated to iron. These spectroscopic fingerprints serve as sensitive probes for the intrinsic electronic structure of the metal core and, indirectly, for the structural composition of the active site. In this study, density functional theory (DFT) was used to calculate vibrational frequencies, by focusing on the EPR-silent intermediate states that contain divalent metal centers. By using the well-characterized Ni-C and Ni-B states as references, we identified candidates for the Ni-SIr , Ni-SIa , and Ni-R states by matching the predicted relative frequency shifts with experimental results. The Ni-SIr and Ni-SIa states feature a water molecule loosely bound to nickel and a formally vacant bridge. Both states are connected to each other through protonation equilibria; that is, in the Ni-SIa state one of the terminal thiolates is protonated, whereas in Ni-SIr this thiolate is unprotonated. For the reduced Ni-R state two feasible models emerged: in one, H2 coordinates side-on to nickel, and the second features a hydride bridge and a protonated thiolate. The Ni-SU state remains elusive as no unequivocal correspondence between the experimental data and calculated frequencies of the models was found, thus indicating that a larger structural rearrangement might occur upon reduction from Ni-A to Ni-SU and that the bridging ligand might dissociate.