Heterogeneous nucleation of ice induced by organic materials is of fundamental importance for climate, biology, and industry. Among organic ice-nucleating surfaces, monolayers of long chain alcohols are particularly effective, while monolayers of fatty acids are significantly less so. As these monolayers expose to water hydroxyl groups with an order that resembles the one in the basal plane of ice, it was proposed that lattice matching between ice and the surface controls their ice-nucleating efficiency. Organic monolayers are soft materials and display significant fluctuations. It has been conjectured that these fluctuations assist in the nucleation of ice. Here we use molecular dynamic simulations and laboratory experiments to investigate the relationship between the structure and fluctuations of hydroxylated organic surfaces and the temperature at which they nucleate ice. We find that these surfaces order interfacial water to form domains with ice-like order that are the birthplace of ice. Both mismatch and fluctuations decrease the size of the preordered domains and monotonously decrease the ice freezing temperature. The simulations indicate that fluctuations depress the freezing efficiency of monolayers of alcohols or acids to half the value predicted from lattice mismatch alone. The model captures the experimental trend in freezing efficiencies as a function of chain length and predicts that alcohols have higher freezing efficiency than acids of the same chain length. These trends are mostly controlled by the modulation of the structural mismatch to ice. We use classical nucleation theory to show that the freezing efficiencies of the monolayers are directly related to their free energy of binding to ice. This study provides a general framework to relate the equilibrium thermodynamics of ice binding to a surface and the nonequilibrium ice freezing temperature and suggests that these could be predicted from the structure of interfacial water.

Ice nucleation in the atmosphere influences cloud properties, altering precipitation and the radiative balance, ultimately regulating Earth’s climate. An accepted ice nucleation pathway, known as deposition nucleation, assumes a direct transition of water from the vapor to the ice phase, without an intermediate liquid phase. However, studies have shown that nucleation occurs through a liquid phase in porous particles with narrow cracks or surface imperfections where the condensation of liquid below water saturation can occur, questioning the validity of deposition nucleation. We show that deposition nucleation cannot explain the strongly enhanced ice nucleation efficiency of porous compared with nonporous particles at temperatures below −40 °C and the absence of ice nucleation below water saturation at −35 °C. Using classical nucleation theory (CNT) and molecular dynamics simulations (MDS), we show that a network of closely spaced pores is necessary to overcome the barrier for macroscopic ice-crystal growth from narrow cylindrical pores. In the absence of pores, CNT predicts that the nucleation barrier is insurmountable, consistent with the absence of ice formation in MDS. Our results confirm that pore condensation and freezing (PCF), i.e., a mechanism of ice formation that proceeds via liquid water condensation in pores, is a dominant pathway for atmospheric ice nucleation below water saturation. We conclude that the ice nucleation activity of particles in the cirrus regime is determined by the porosity and wettability of pores. PCF represents a mechanism by which porous particles like dust could impact cloud radiative forcing and, thus, the climate via ice cloud formation.

Cold-adapted organisms produce antifreeze and ice-nucleating proteins to prevent and promote ice formation. The crystal structure of hyperactive bacterial antifreeze protein (AFP) MpAFP suggests that this protein binds ice through an anchored clathrate motif. It is not known whether other hyperactive AFPs and ice-nucleating proteins (INPs) use the same motif to recognize or nucleate ice. Here we use molecular simulations to elucidate the ice-binding motifs of hyperactive insect AFPs and a model INP of Pseudomonas syringae. We find that insect AFPs recognize ice through anchored clathrate motifs distinct from that of MpAFP. By performing simulations of ice nucleation by PsINP, we identify two distinct ice-binding sites on opposite sides of the β-helix. The ice-nucleating sequences identified in the simulations agree with those previously proposed for the closely related INP of Pseudomonas borealis based on the structure of the protein. The simulations indicate that these sites have comparable ice-nucleating efficiency, but distinct binding motifs, controlled by the amino acid sequence: one is an anchored clathrate and the other ice-like. We conclude that anchored clathrate and ice-like motifs can be equally effective for binding proteins to ice and promoting ice nucleation.

Organisms that thrive at cold temperatures produce ice-binding proteins to manage the nucleation and growth of ice. Bacterial ice-nucleating proteins (INP) are typically large and form aggregates in the cell membrane, while insect hyperactive antifreeze proteins (AFP) are soluble and generally small. Experiments indicate that larger ice-binding proteins and their aggregates nucleate ice at warmer temperatures. Nevertheless, a quantitative understanding of how do size and aggregation of ice-binding proteins determine the temperature Thet at which proteins nucleate ice is still lacking. Here we address this question using molecular simulations and nucleation theory. The simulations indicate that the 2.5 nm long antifreeze protein TmAFP nucleates ice at 2±1 °C above the homogeneous nucleation temperature, in good agreement with recent experiments. We predict that the addition of ice-binding loops to TmAFP increases Thet until the length of the binding-site becomes ~4 times its width, beyond which Thet plateaus. We implement an accurate procedure to determine Thet of surfaces of finite size using classical nucleation theory and, after validating the theory against Thet of the proteins in molecular simulations, we use it to predict Thet of the INP of Ps. syringae as a function of the length and number of proteins in the aggregates. We conclude that assemblies with at most 34 INP already reach the Thet = -2 °C characteristic of this bacterium. Interestingly, we find that Thet is a strongly varying non-monotonic function of the distance between proteins in the aggregates. This indicates that to achieve maximum freezing efficiency, bacteria must exert exquisite, sub-angstrom control of the distance between INP in their membrane.

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.