Specific Ion–Protein Interactions Influence Bacterial Ice Nucleation

Abstract

Ice nucleation-active bacteria are the most efficient ice nucleators known, enabling the crystallization of water at temperatures close to 0 °C, thereby overcoming the kinetically hindered phase transition process at these conditions. Using highly specialized ice-nucleating proteins (INPs), they can cause frost damage to plants and influence the formation of clouds and precipitation in the atmosphere. In nature, the bacteria are usually found in aqueous environments containing ions. The impact of ions on bacterial ice nucleation efficiency, however, has remained elusive. Here, we demonstrate that ions can profoundly influence the efficiency of bacterial ice nucleators in a manner that follows the Hofmeister series. Weakly hydrated ions inhibit bacterial ice nucleation whereas strongly hydrated ions apparently facilitate ice nucleation. Surface-specific sum-frequency generation spectroscopy and molecular dynamics simulations reveal that the different effects are due to specific interactions of the ions with the INPs on the surface of the bacteria. Our results demonstrate that heterogeneous ice nucleation facilitated by bacteria strongly depends upon the nature of the ions, and specific ion–protein interactions are essential for the complete description of heterogeneous ice nucleation by bacteria.