Experimental data from ion mobility measurements and electron transfer dissociation were combined with extensive computational analysis of ion structures and dissociation energetics for Gly-Leu-Gly-Gly-Lys cations and cation radicals. Experimental and computational collision cross sections of (GLGGK + 2H)(2+) ions pointed to a dominant folding motif that is represented in all low free-energy structures. The local folding motifs were preserved in several fragment ions produced by electron transfer dissociation. Gradient optimizations of (GLGGK + 2H)(+center dot) cation-radicals revealed local energy minima corresponding to distonic zwitterionic structures as well as aminoketyl radicals. Both of these structural types can isomerize to low-energy tautomers that are protonated at the radical-containing amide group forming a new type of intermediates, -(CO-NH2+)-O-center dot- and -C-center dot(OH)-NH2+-, respectively. Extensive mapping with B3LYP, M06-2X, and MP2(frozen core) calculations of the potential energy surface of the ground doublet electronic state of (GLGGK + 2H)(+center dot) provided transition-state and dissociation energies for backbone cleavages of the N-C-a and amide C-N bonds leading to ion molecule complexes. The complexes can undergo facile prototropic migrations that are catalyzed by the Lys ammonium group and isomerize enolimine c-type fragments to the more stable amide tautomers. In contrast, interfragment hydrogen atom migrations in the complexes were found to have relatively high transition energies and did not compete with fragment separation. The extensive analysis of the intermediate and transition-state energies led to the conclusion that the observed dissociations cannot proceed competitively on the same potential energy surface. The reactive intermediates for the dissociations originate from distinct electronic states that are accessed by electron transfer.