Spontaneous Reduction of Biomolecules on the Surface of Water Droplets

Abstract

Reduction and oxidation reactions are a family of reactions that involves the transfer of electrons between species. Redox reactions play a crucial role in living organism as they are involved in photosynthesis, respiration, and metabolism. Chemical reactions in confined environments behave differently than the same ones in bulk solution. We have found that chemical reactions are significantly accelerated in micron-sized aqueous droplets (microdroplets) by the factor over 105 for various reactions including protein unfolding, protein-ligand binding, chlorophyll demetallation, and hydrogen-deuterium exchange (PNAS 2015, Q Rev Biophys 2016 and 2017). We also found that the reactions with a high thermodynamic barrier can spontaneously occur in microdroplets by lowering the entropy change at the water surface (PNAS, in press). Here we present spontaneous reduction of biomolecules including pyruvate, cystine, lipoic acid, and fumarate with up to ∼ 95 % reduction efficiency within hundreds of microseconds at the water-air interface on microdroplets without an added reducing agent. The reduction efficiency decreased as the concentration of pyruvate increased above 10 nM, suggesting the capacity of the reducing power of water microdroplet is limited to around tens of nanomoles per liter. The increase of surface-to-volume ratio of the microdroplets by generating smaller microdroplets led to increased reduction efficiency, indicating the reduction occurs at or very near the surface of microdroplets. The increase of O2 composition in the surrounding gas reduced reduction efficiency, suggesting that the oxidation of OH- due to a strong electric field at the water surface is a probable mechanism of the reduction. This discovery of spontaneous reduction at the water-air interface may provide a new biophysical mechanism of altering metabolomic balance without the participation of charge carriers or reducing agents/enzymes as well as elucidating the reduction of biomolecules in the prebiotic era.