Intracellular Cu^I is controlled by the transcriptional regulator CueR, which effectively discriminates between monovalent and divalent metal ions. It is intriguing that Hg^II does not activate transcription, as bis-thiolate metal sites exhibit high affinity for Hg^II. Here the binding of Hg^II to CueR and a truncated variant, ΔC7-CueR, without the last 7 amino acids at the C-terminus including a conserved CCHH motif is explored. ESI-MS demonstrates that up to two Hg^II bind to CueR, while ΔC7-CueR accommodates only one Hg^II. ^199mHg PAC and UV absorption spectroscopy indicate HgS₂ structure at both the functional and the CCHH metal site. However, at sub-equimolar concentrations of Hg^II at pH 8.0, the metal binding site displays an equilibrium between HgS₂ and HgS₃, involving cysteines from both sites. We hypothesize that the C-terminal CCHH motif provides auxiliary ligands that coordinate to Hg^II and thereby prevents activation of transcription.