Modulation of Electrostatic Interactions as a Mechanism of Cryptic Adaptation of Colwellia to High Hydrostatic Pressure

The role of various interactions in determining the pressure adaptation of the proteome in piezophilic organisms remains to be established. It is clear that the adaptation is not limited to one or two proteins, but has a more general evolution of the characteristics of the entire proteome, the so-called cryptic evolution. Using the synergy between bioinformatics, computer simulations, and some experimental evidence, we probed the physico-chemical mechanisms of cryptic evolution of the proteome of psychrophilic strains of model organism, Colwellia, to adapt to life at various pressures, from the surface of the Arctic ice to the depth of the Mariana Trench. From the bioinformatics analysis of proteomes of several strains of Colwellia, we have identified the modulation of interactions between charged residues as a possible driver of evolutionary adaptation to high hydrostatic pressure. The computational modeling suggests that these interactions have different roles in modulating the function-stability relationship for different protein families. For several classes of proteins, the modulation of interactions between charges evolved to lead to an increase in stability with pressure, while for others, just the opposite is observed. The latter trend appears to benefit enzyme activity by countering structural rigidification due to the high pressure.