An NMR approach to determining the solution molecular structure of a high-spin ferric hemoprotein, 13 kDa ferricytochrome c’ from Rhodopseudomonas palustris (Rp), has been investigated. In parallel with the use of appropriately tailored 1D and 2D experiments to provide scalar and dipolar correlations for the strongly relaxed and hyperfine-shifted heme cavity residues, we explore an interpretive basis of the large hyperfine shifts for noncoordinated residues which could provide constraints in solution structure determination for high-spin ferric hemoproteins. It is shown that the complete heme can be uniquely assigned in spite of the extreme relaxation properties (T(1)s 1-8 ms). Sufficient scalar connectivities are detected for strongly relaxed protons (T-1, greater than or equal to 4 ms) to uniquely assign residues on both the proximal and distal sides of the heme. The spatial correlations indicate that the structure is homologous to the four-helix bundle observed for other cytochromes c’. The pattern of large hyperfine shifts for noncoordinated residues is shown to be qualitatively reproduced by the dipolar shifts for a structural homolog based on an axial zero-field splitting of similar to 12 cm(-1) It is concluded that, when this approach is combined with more conventional 2D methods for the diamagnetic portion of the protein, a complete structure determination of a five-coordinate ferric hemoprotein should be readily attainable. It is shown that the ferricytochrome c’ unfolds reversibly at high temperature and that there exists at least one equilibrium intermediate in this unfolding that is suggested to involve helix separation from the heme.