Unusual Properties of Water at Heterogeneous Biological Interfaces

Abstract

Water is an essential constituent of life, which acts as a solvent for biomolecular reactions and a transporter of biomolecules. It also plays a crucial role in determining structures and assemblies of complex biological molecules such as proteins and long DNA strands. Water is involved in processes of bioenergy transformation and utilization such as photosynthesis and respiration through redox reactions of water molecules. Water is considered inert and relatively stable; however, it becomes catalytically and electrochemically active when bulk water is formed into microdroplets. We found biomolecular reactions such as protein unfolding, protein-ligand interactions, and demetallation of chlorophylls are markedly accelerated by the factor of a thousand or more in water microdroplets compared to bulk water (Lee et al., PNAS, 2015; Lee et al., Q Rev Phys, 2015 and 2017). Thermodynamically unfavored reactions in bulk water such as phosphorylation and the formation of ribonucleosides can proceed in water microdroplets (Nam et al., PNAS, 2017). We also found that metal ions are spontaneously reduced to form nanostructures (Lee et al., Nat Commun, 2018) and biomolecules involved in citric acid cycles including pyruvate, fumarate, and oxaloacetate are spontaneously reduced in water microdroplets without any added reducing agents (Lee et al., JACS, 2019). This spontaneous reduction is paired and caused by the spontaneous oxidation of water molecules or ions in microdroplets to form reactive oxygen species including hydroxyl radicals and hydrogen peroxides (Lee et al., PNAS, 2019). One of primary mechanisms responsible for these unusual properties of water is a strong intrinsic electric field formed at the interface of water microdroplets (Kathmann et al., JACS, 2009). These findings suggest that water molecules strongly influence biomolecular reactions and consequently, cellular regulations in cells which is in the form of a micron-sized reactor containing various heterogeneous interfaces.