Four kinetically trapped substates of a molten globule-like artificial protein were formed by metal-directed trimerization of an amphiphilic peptide modified with a bipyridine ligand. Although the helical contents of the trapped states range from 50% to 95%, their thermodynamic stabilities are within 0.3 kcal/mol of one another. Each metalloprotein incorporates a different diastereomer of the iron(II) tris(bipyridine-peptide) core; as the diastereomers isomerize at room temperature, the four protein states interconvert, with half-lives on the order of 5 h. With the aid of a model compound, Fe(Ala-bipy)(3), the effects of interhelix interactions were disentangled from the effects of metal complexation, and barriers on the protein’s potential energy surface were determined. The energetic barriers range from 0.5 to 1.7 kcal/mol, significantly smaller than the 2.3 kcal/mol required to unfold the metalloprotein; since the activation energy of denaturation cannot be smaller than Delta G degrees of denaturation, the protein does not unfold completely in the transitions from one molten globule state to another. Tertiary structure in de novo designed proteins is discussed in light of these results.