The use of de novo designed peptides is a powerful strategy to elucidate Hg^II-protein interactions and to gain insight into the chemistry of Hg^II in biological systems. Cysteine derivatives of the designed -helical peptides of the TRI family [Ac-G-(L_aK_bA_cL_dE_eE_fK_g)₄-G-NH₂] bind Hg^II at high pH values and at peptide/Hg^II ratios of 3:1 with an unusual trigonal thiolate coordination mode. The resulting Hg^II complexes are good water-soluble models for Hg^II binding to the protein MerR. We have carried out a parallel study using ¹⁹⁹Hg NMR and ^199mHg perturbed angular correlation (PAC) spectroscopy to characterize the distinct species that are generated under different pH conditions and peptide TRI L9C/Hg^II ratios. These studies prove for the first time the formation of [Hg{(TRI L9C)₂-(TRI L9CH)}], a dithiolate-Hg^II complex in the hydrophobic interior of the three-stranded coiled coil (TRI L9C)₃. ¹⁹⁹Hg NMR and ^199mHg PAC data demonstrate that this dithiolate-Hg^II complex is different from the dithiolate [Hg(TRI L9C)₂], and that the presence of third -helix, containing a protonated cysteine, breaks the symmetry of the coordination environment present in the complex [Hg(TRI L9C)₂]. As the pH is raised, the deprotonation of this third cysteine generates the trigonal thiolate-Hg^II complex Hg(TRI L9C)₃^- on a timescale that is slower than the NMR timescale (0.01-10 ms). The formation of the species [Hg{(TRI L9C)₂(TRI L9CH)}] is the result of a compromise between the high affinity of Hg^II to form dithiolate complexes and the preference of the peptide to form a three-stranded coiled coil.