The dynamics of a hyperthermophilic protein fragment in a water environment, as studied by performing molecular dynamics (MD) simulations at various temperatures, is compared to the dynamical behavior of a homologous mesophilic protein simulated under identical conditions. The effects on the stability of the spatial arrangement and mobility of the charged residues in solution were quantified by calculating free energy changes upon salt bridge formation in these proteins. Electrostatic free energy terms derived from a thermodynamic cycle were obtained by solving the linearized Poisson-Boltzmann equation for a series of protein conformations generated by MD simulations and placed subsequently in a continuum solvent medium. Our results show that the ion pairs are electrostatically stabilizing in most of the cases, but their individual contributions vary significantly. The greater contribution of the charged residues to the stability of the hyperthermophilic protein as compared with the mesophilic counterpart was evidenced only by the calculations that included conformations sampled at 343 and 373 K. The "dynamic" structure of the hyperthermophilic protein fragment simulated at elevated temperatures reveals an optimum placement of the ionizable residues within the protein structure as well as the role of their cooperative interactions in promoting thermal stability. The thermodynamic properties such as electrostatic free energy differences, configurational entropies, and specific heat capacities calculated in the dynamic context of the protein structure provided new insight into the mechanism of protein thermostabilization.