The biodiversity of hydrogenases, the enzymes that oxidize and produce H2, is only just beginning to be explored. Here, we use direct electrochemistry to characterize two enzymes from a subgroup of group B FeFe hydrogenases, defined by the presence of three adjacent cysteine residues near the active site: the third FeFe hydrogenase from Clostridium pasteurianum (CpIII) and the second from Megasphaera elsdenii (MeII). To examine the functional role of the unusual TSCCCP motif, which is replaced with TSCCP in group A hydrogenases, we also produced a CpIII variant, where the supernumerary cysteine is deleted. CpIII and MeII inactivate under oxidative conditions in a manner that is distinct from all other previously characterized hydrogenases from group A. Our results suggest that the supernumerary cysteine allows the previously observed sulfide-independent formation of the Hinact state in these enzymes. We also evidence a second reversible oxidative inactivation process that is independent of the supernumerary cysteine. Because of their inactivation under oxidative conditions, these enzymes are inefficient H2 oxidation catalysts, but their active site itself is not tuned to make them more active in one particular direction.