Hydration modulates protein structures and dynamics, and thus is fundamental to protein functions. Nonetheless, probing water molecules in hydration shells is still challenging largely because of overwhelming background generated from bulk water. We use phase-resolved chiral sum frequency generation (SFG) spectroscopy in combination with computational modeling to probe water structures around an antiparallel β-sheet protein. Both simulated and experimental spectra show that the phase of chiral SFG response of the water O-H stretching modes reverses with the absolute chirality of the enantiomeric (L-) and (D-) antiparallel β-sheet proteins. This observation reveals that a protein secondary structures can imprint their intrinsic chirality onto water molecules and organize them into chiral supramolecular assemblies. Further analyses of the molecular dynamics trajectories that are used to simulate the chiral SFG spectra in comparison with experimental results identify water molecules that give rise to the water O-H stretches at distinct frequencies. These water molecules assemble into chiral supramolecules through hydrogen-bonding interactions in various strengths and orientation with the protein backbone and side chains, capturing molecular details of the chiral supramolecular assemblies. These results support phase-resolved chiral SFG spectroscopy as a highly selective method for probing molecular details of protein hydration. This work demonstrates that a pair of enantiomeric biomacromolecules can induce hydration structures of opposite chirality, providing fundamental insights into elucidating chiral selectivity of biomacromolecular interactions and potentially the molecular origin of biological homochirality.

Chiral sum frequency generation spectroscopy shows mirror-image β-sheet proteins organize water molecules into supermolecular structures of opposite chirality

ACS Fall 2021

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