Ion mobility spectrometry-mass spectrometry and quantum chemical calculations are used to determine the structures and stabilities of singly protonated XaaProGlyGly peptides: HDPGG, HNPGG, HEPGG, and HQPGG. The IMS distributions are similar, suggesting the peptides adopt closely related structures in the gas phase. Quantum chemical calculations show that all conformers seen in the experimental spectrum correspond to the configuration about the Xaa-Pro peptide bond, significantly different from the behavior seen previously for HGPGG. Density functional theory and quantum theory of atoms in molecules (QTAIM) investigations uncover a silent drama as a minor conformer not observed in the HDPGG spectrum becomes the preferred conformer in HQPGG, with both conformers being coincident in collision cross section. Investigation of the highly coupled hydrogen bond network, replete with CH···O interactions and bifurcated hydrogen bonds, reveals the cause of this effect as well as the absence of conformers from the spectra. A series of generalized observations are provided to aid in enzyme and ligand design using these coupled hydrogen bond motifs.