A two-dimensional adsorption kinetic model for thermal hysteresis activity in antifreeze proteins

Abstract

Antifreeze proteins ͑AFPs͒ and antifreeze glycoproteins ͑AFGPs͒, collectively abbreviated as AF͑G͒Ps, are synthesized by various organisms to enable their cells to survive in subzero environments. Although the AF͑G͒Ps are markedly diverse in structure, they all function by adsorbing to the surface of embryonic ice crystals to inhibit their growth. This adsorption results in a freezing temperature depression without an appreciable change in the melting temperature. The difference between the melting and freezing temperatures, termed thermal hysteresis ͑TH͒, is used to detect and quantify the antifreeze activity. Insights from crystallographic structures of a number of AFPs have led to a good understanding of the ice-protein interaction features. Computational studies have focused either on verifying a specific model of AFP-ice interaction or on understanding the protein-induced changes in the ice crystal morphology. In order to explain the origin of TH, we propose a novel two-dimensional adsorption kinetic model between AFPs and ice crystal surfaces. The validity of the model has been demonstrated by reproducing the TH curve on two different ␤-helical AFPs upon increasing the protein concentration. In particular, this model is able to accommodate the change in the TH behavior observed experimentally when the size of the AFPs is increased systematically. Our results suggest that in addition to the specificity of the AFPs for the ice, the coverage of the AFPs on the ice surface is an equally necessary condition for their TH activity.

Microfluidic experiments reveal that antifreeze proteins bound to ice crystals suffice to prevent their growth

“…Several theoretical studies explained the experimentally observed concentration dependence of the FH activity by assuming that the adsorption of AFPs is reversible (11,(15)(16)(17). To investigate the binding kinetics at the ice-water interface and the dependence of FH on AFP concentration, it is important to understand the respective roles of AFPs in solution and AFPs bound to the ice surface.…”

“…This theory has been criticized for assuming that the ice-water interface is sharp, contrary to the experimental evidence that the transitions from an ordered solid phase to a liquid phase at the ice-water interfaces are gradual and occur over several layers of water molecules (9-12). Perhaps the hardest criticism to answer is related to the experimentally observed dependence of FH activity on AFP concentration, which strongly suggests a dynamic exchange between adsorbed AFPs and free AFPs in the surrounding solution (11,(13)(14)(15)(16)(17)(18).…”

“…This theory has been criticized for assuming that the ice-water interface is sharp, contrary to the experimental evidence that the transitions from an ordered solid phase to a liquid phase at the ice-water interfaces are gradual and occur over several layers of water molecules (9-12). Perhaps the hardest criticism to answer is related to the experimentally observed dependence of FH activity on AFP concentration, which strongly suggests a dynamic exchange between adsorbed AFPs and free AFPs in the surrounding solution (11,(13)(14)(15)(16)(17)(18).A few theories relating the kinetics of adsorption of AFP molecules to the ice surface with the observed FH activity have been suggested (19,20). Several experimental studies have examined the kinetics of AFP binding to ice, but the questions of reversibility of the AFP binding and of the contribution of AFP molecules in solution to the inhibition of ice growth have not been resolved.…”

Interaction of ice binding proteins with ice, water and ions

“…86,103,104 An insightful study by Kristiansen and Zachariassen builds upon the original adsorption-inhibition model, but argues that it is a pressure build-up due to convex ice growth that underlies the Gibbs-Thomson effect. 71 Alternative models consider the anisotropic surface energy of ice, 106 reversible adsorption, [107][108][109][110][111] the polymeric nature of IBPs, 112,113 and lowering of the interfacial tension or step energy. 114,115 …”

Interactions of β-Helical Antifreeze Protein Mutants with Ice

“…Furthermore, a transition layer about a nanometer thick 14 in which the molecular order gradually increases between bulk liquid water and ice precludes, according to some researchers, the possibility for a simple, direct attachment of protein to ice. 15 Some of these issues have been attended to in kinetic models based either on reversible 16 or irreversible 12 adsorption of AFP molecules to ice, or even a combination of the two. 17 A large number of biochemical, biophysical, and structural studies have been conducted to elucidate the mechanism by which AFPs bind to specific planes of ice.…”