Technological advances have facilitated the generation of artificial proteins that possess the capabilities of recognizing and binding to inorganic solids and/or controlling nucleation processes that form inorganic solids. However, very little is known regarding the structure of these interesting polypeptides and how their structure contributes to functionality. To address this deficiency, we report structural investigations of an artificial protein, p288, that self-assembles and controls the nucleation of simple salts and organic compounds into dendrite-like crystals. Under aqueous conditions at low pH and in the presence of high salt, p288 is conformationally labile and exists primarily as a random coil conformer in equilibrium with other undefined secondary structures, including polyproline type II and beta turn. We note that p288 can fold into either a partial beta strand (at neutral pH) or a predominantly alpha helical (in the presence of TFE) conformation. Solid-state C-13-N-15 NMR experiments also reveal that p288 in the lyophilized, hydrated state possesses some degree of nonrandom coil structure. These results indicate that p288 is conformationally labile but can undergo conformational transitions to a more stable structure when water solvent loss/displacement occurs and protein concentrations increase. We believe that conformational instability and the ability to adopt different structures as a function of different environmental conditions represent important molecular features that impact p288 supramolecular assembly and crystal nucleation processes.