Ion mobility spectrometry-mass spectrometry and quantum chemical calculations are used to determine the structures and stabilities of singly protonated XaaProGlyGly peptides: H(+)DPGG, H(+)NPGG, H(+)EPGG, and H(+)QPGG. 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 cis configuration about the Xaa-Pro peptide bond, significantly different from the behavior seen previously for H(+)GPGG. Density functional theory and quantum theory of atoms in molecules (QTAIM) investigations uncover a silent drama as a minor conformer not observed in the H(+)DPGG spectrum becomes the preferred conformer in H(+)QPGG, with both conformers being coincident in collision cross section. Investigation of the highly coupled hydrogen bond network, replete with CH center dot center dot center dot O interactions and bifurcated hydrogen bonds, reveals the cause of this effect as well as the absence of trans conformers from the spectra. A series of generalized observations are provided to aid in enzyme and ligand design using these coupled hydrogen bond motifs.