Antifreeze proteins: An unusual tale of structural evolution, hydration and function

Abstract

Organisms living in extreme cold conditions find a unique solution for cold adaptation. They produce a group of proteins, called antifreeze proteins (AFPs) which cause depression of freezing point in a non-colligative manner. AFPs are unusual in every sense, i.e., their evolution, hydration and function. Evolutionary analysis reveals that AFPs do not emerge from a common ancestor; rather their evolution is independent and closely correlated to the Antarctic glaciation events. AFPs exert antifreeze activity by adsorption-inhibition mechanism. According to the model, ice can grow in the region between two bound AFPs, which results in the generation of a curved growing ice front. As a result, the radius of curvature decreases with further growth of the ice front and ultimately halts at the limit of critical radius. Main assumption of the model is that AFPs irreversibly bind to the ice surface, which is also validated by recent microfluidic experiments. Initially hydrogen bond mediated ice binding has been proposed, but experimental mutation data invalidated the hypothesis. A surface complementarity driven ice adsorption mechanism has been lately proposed, however, it is inadequate to explain the irreversible binding. Mechanism of ice recognition by AFP still remains elusive. Recently, AFPs have been shown to induce water ordering and we have proposed that the ordered hydration water adopts clathrate-like structure, which effectively adsorbs AFP on ice. Hydrophobic hydration induces clathrate formation around the ice binding surface. The model is highly promising and qualitatively explains mutational data and binding plane specificity data from ice-etching experiments.