Preordering of water is not needed for ice recognition by hyperactive antifreeze proteins

Abstract

Antifreeze proteins (AFPs) inhibit ice growth in organisms living in cold environments. Hyperactive insect AFPs are particularly effective, binding ice through "anchored clathrate" motifs. It has been hypothesized that the binding of hyperactive AFPs to ice is facilitated by preordering of water at the ice-binding site (IBS) of the protein in solution. The antifreeze protein AFP displays the best matching of its binding site to ice, making it the optimal candidate to develop ice-like order in solution. Here we use multiresolution simulations to unravel the mechanism by whichAFP recognizes and binds ice. We find that water at the IBS of the antifreeze protein in solution does not acquire ice-like or anchored clathrate-like order. Ice recognition occurs by slow diffusion of the protein to achieve the proper orientation with respect to the ice surface, followed by fast collective organization of the hydration water at the IBS to form an anchored clathrate motif that latches the protein to the ice surface. The simulations suggest that anchored clathrate order could develop on the large ice-binding surfaces of aggregates of ice-nucleating proteins (INP). We compute the infrared and Raman spectra of water in the anchored clathrate motif. The signatures of the OH stretch of water in the anchored clathrate motif can be distinguished from those of bulk liquid in the Raman spectra, but not in the infrared spectra. We thus suggest that Raman spectroscopy may be used to probe the anchored clathrate order at the ice-binding surface of INP aggregates.

Mimicking the Ice Recrystallization Activity of Biological Antifreezes. When is a New Polymer “Active”?

“…Figure B shows a simulation of spruce budworm AFP and its hypothesized binding to the prism plane via coordinated water molecules providing a match . Whilst the molecular binding details are still under investigation, there is overwhelming evidence for AFPs binding to ice faces and strong evidence of molecular level interactions have been determined . However, for the facially amphipathic molecules, with no evidence for ice binding, an alternative molecular level mechanism which can give rise to IRI is required.…”

Combined molecular dynamics and neural network method for predicting protein antifreeze activity

“…This layer can then be easily incorporated into the growing ice crystal, binding the protein to the solid-liquid interface (12). Recent work by Hudait et al (13) has shown that water near the IBS is not truly ice like, since its structural order is much lower than ice, but simulations do show that water near the IBS displays exceptionally slower hydrogen bond reorientation dynamics compared with other protein surfaces (14). The presence of slow hydrogen bond dynamics near the IBS was also confirmed experimentally by Meister et al (15).…”

Hydrogen polarity of interfacial water regulates heterogeneous ice nucleation

“…Water freezing on various material surfaces is of importance in wide-ranging fields [1][2][3][4][5] such as cloud seeding in climate, frost heaving, and cell preserving. So far, the microscopic mechanisms of the key process of freezing on substrates, the heterogeneous ice nucleation, still remains elusive [6][7][8][9] .…”