In the nacre layer of the mollusk, proteins play an important role in regulating the morphology and lattice structure of calcium carbonate minerals. However, this process remains elusive due to the fact that we do not understand how protein sequences control the structure and morphology of biominerals. To take us a step further in this direction, we report the molecular structure of a 30 AA N-terminal mineral interactive sequence (n16N) of the aragonite-promoting protein, n16, and contrast these findings to those previously reported for two "calcite-blocker" nacre-associated sequences, AP7N and AP24N. We find that n16N is conformationally labile and adopts a random-coil conformation that possesses short, dispersed extended beta-strand segments that are located at the A1-Y2, K5-Y9, Y11-114, and D21-N25 sequence blocks. Like AP7N and AP24N, Ca(II) ion interactions with n16N alter chain dynamics and local structure, and n16N is adsorbed onto calcite crystals and cannot easily be displaced via differential washing techniques. Furthermore, all three sequences have planar surface regions that could serve as putative sites for mineral interactions or ion cluster formation. However, what sets n16N apart from AP7N and AP24N are different folding propensities as well as unique molecular surface features and amino acid composition. n16N has a more condensed structure that, in the presence of TFE, folds into a beta-strand. This contrasts with the more open structures of AP7N and AP24N that are induced by TFE to fold into alpha-helices. Mapping of the n16N molecular surface reveals significant cationic regions and diffuse anionic charge, which contrasts with the small anionic "pocket" regions of AP7N/AP24N. Finally, n16N has 50% fewer sites for mineral surface- or ion cluster-associated water interactions compared to AP7N and AP24N. Overall, the structure of n16N is "tuned" to a different function within the in vitro mineralization scheme. The different features found in AP7N, AP24N, and n16N could be exploited for engineering polypeptides that recognize and bind to different surface features of inorganic crystalline solids.