Protein dynamics, folding, and thermodynamics represent a central aspect of biophysical chemistry. pH, temperature, and denaturant perturbations inform our understanding of diverse contributors to stability and rates. In this work, we performed a thermodynamic analysis using a combined experimental and computational approach to gain insights into the role of electrostatics in the folding reaction of a psychrophile frataxin variant from Psychromonas ingrahamii. This folding reaction is strongly modulated by pH with a single, narrow, and well-defined transition state with similar to 80% compactness, similar to 70% electrostatic interactions, and similar to 60% hydration shell compared to the native state (alpha(D) = 0.82, alpha(H) = 0.67, and alpha(Delta Cp) = 0.59). Our results are best explained by a two-proton/two-state model with very different pK(a) values of the native and denatured states (similar to 5.5 and similar to 8.0, respectively). As a consequence, the stability strongly increases from pH 8.0 to 6.0 (vertical bar Delta Delta G degrees vertical bar = 5.2 kcal mol(-1)), mainly because of a decrease in the T Delta S degrees. Variation of Delta H degrees and Delta S degrees at pH below 7.0 is dominated by a change in Delta H-f double dagger and Delta S-f double dagger, while at pH above 7.0, it is governed by Delta H-u double dagger and Delta S-u double dagger. Molecular dynamics simulations showed that these pH modulations could be explained by the fluctuations of two regions, rich in electrostatic contacts, whose dynamics are pH dependent and motions are strongly correlated. Results presented herein contribute to the understanding of the stability and dynamics of this frataxin variant, pointing to an intrinsic feature of the family topology to support different folding mechanisms.