IR spectroelectrochemistry of Fe4{Me(CH2S)3}2(CO)8 (4Fe6S) in the nu(CO) region shows that the neutral and anion forms have all their CO groups terminally bound to the Fe atoms; however, for the dianion there is a switch of the coordination mode of at least one of the CO groups. The available structural and nu(CO) spectra are closely reproduced by density-functional theory calculations. The calculated structure of 4Fe6S2- closely mirrors that of the diiron subsite of the [Fe-Fe] hydrogenase H cluster with a bridging CO group and an open coordination site on the outer Fe atom of pairs of dithiolate-bridged Fe0FeII subunits connected by two bridging thiolates. Geometry optimization based on the all-terminal CO isomer of 4Fe6S2- does not give a stable structure but reveals a second-order saddle point ca. 11.53 kcal mol(-1) higher in energy than the CO-bridged form. Spectroelectrochemical studies of electrocatalytic proton reduction by 4Fe6S show that slow turnover from the primary reduction process (E1/2'=-0.71 V vs Ag/AgCl) involves rate-limiting protonation of 4Fe6S- followed by reduction to H:4Fe6S-. Rapid electrocatalytic proton reduction is obtained at potentials sufficient to access 4Fe6S2-, where the rate of dihydrogen elimination from the FeIIFeII core of 4Fe6S is ca. 500 times faster than that from the FeIFeI core of Fe2(mu-S(CH2)3S)(CO)6. The dramatically increased rate of electrocatalysis obtained from 4Fe6S over all previously identified model compounds appears to be related to the features uniquely common between it and the H-cluster, namely, that turnover involves the same formal redox states of the diiron unit (FeIFeII and Fe0FeII), the presence of an open site on the outer Fe atom of the Fe0FeII unit, and the thiolate-bridge to a second one-electron redox unit.