We have combined spectroscopy, chromatography, calorimetry, and small-angle X-ray scattering (SAXS) to provide a comprehensive structural and stoichiometric description of the sodium dodecyl sulfate (SDS)-induced denaturation of the 86-residue α-helical bovine acyl-coenzyme-A-binding protein (ACBP). Denaturation is a multistep process. Initial weak binding of 1-3 SDS molecules per protein molecule below 1.3 mM does not perturb the tertiary structure. Subsequent binding of 13 SDS molecules per ACBP molecule leads to the formation of SDS aggregates on the protein and changes in both tertiary and secondary structures. SAXS data show that, at this stage, a decorated micelle links two ACBP molecules together, leaving about half of the polypeptide chain as a disordered region protruding into the solvent. Further titration with SDS leads to the additional uptake of 26 SDS molecules, which, according to SAXS, forms a larger decorated micelle bound to a single ACBP molecule. At the critical micelle concentration, we conclude from reduced mobility and increased fluorescence anisotropy that each ACBP molecule becomes associated with more than one micelle. At this point, 56-60 SDS molecules are bound per ACBP molecule. Our data provide key structural insights into decorated micelle complexes with proteins, revealing a remarkable diversity in the different conformations they can stabilize. The data highlight that a minimum decorated micelle size, which may be a key driving force for intermolecular protein association, exists. This may also provide a structural basis for the known ability of submicellar surfactant concentrations to induce protein aggregation and fibrillation.