Aspartate and glutamate side chains are unique among the 20 amino acids, in regard to possessing carboxylate groups that can bind the metal cation either monodentately (via one of the carboxylate O atoms) or bidentately (via both carboxylate O atoms). In this work, we elucidate the physical principles that determine the carboxylate-binding mode in metalloproteins by surveying the Protein Data Bank (PDB) and performing density functional and continuum dielectric calculations. The metal and its first-shell ligands are explicitly modeled and treated quantum mechanically, whereas the second-shell effects and the metal-binding site environment are implicitly taken into account. We systematically investigate the effect on the carboxylate denticity of (i) its immediate surroundings, (ii) the metal type and coordination number, (iii) the total charge of the metal complex, and (iv) the relative solvent exposure of the metal-binding site. The results suggest that the carboxylate-binding mode is determined by competition between the metal cation, on one hand, and nonacidic neighboring ligands from the metal inner or outer coordination sphere, on the other, for the second O atom of the COO- moiety. When the positive charge of the metal is reduced by coordination to negatively charged ligands, first- or second-shell ligand-carboxylate (as opposed to direct metal - carboxylate) interactions dictate the carboxylate-binding mode. In such cases, water molecules have a crucial role in stabilizing the monodentate carboxylate-binding mode of water-rich Mg complexes, whereas the peptide backbone has a role in destabilizing the monodentate carboxylate-binding mode of the "drier" and bulkier Ca complexes. Thus, by fine-tuning the respective interactions, the protein can adopt an appropriate binding-site configuration.