Proteins are macromolecules consisting of myriad intramolecular interactions together with interactions with solvent that determine their conformational ensemble, stability and dynamics. Global constraints such as temperature and solvent composition play an essential role in defining equilibrium properties. Similarly, covalent bonding and other intramolecular interactions such as hydrogen bonds impose local mechanical constraints. Application of graph-rigidity has played an important role in predicting protein flexibility, exploring conformational dynamics through geometrical simulation (GS) and predicting thermodynamic stability via a Distance Constraint Model (DCM) that accounts for non-additivity in conformational entropy. A DCM/GS hybrid method is presented that rapidly explores conformational dynamics guided by changes in free energy by successively solving a free energy functional. A critical part of the free energy functional is modeling the solvation contribution to balance accuracy and speed so as to enable rapid exploration of conformational space that is scalable to a collection of proteins in a multi-component solvent to investigate protein-protein interactions in specific formulations and the cellular environment. Among the many implicit solvation models available in the literature, two approaches are being pursued currently which will be used to generate discussions among the experts.