Biomolecular hydration is fundamental to biological functions. Using phase-resolved chiral sum-frequency generation spectroscopy (SFG), we probe molecular architectures and interactions of water molecules around a self-assembling antiparallel β-sheet protein. We find that the phase of the chiroptical response from the O-H stretching vibrational modes of water flips with the absolute chirality of the (
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l -) or (d -) antiparallel β-sheet. Therefore, we can conclude that the (d -) antiparallel β-sheet organizes water solvent into a chiral supermolecular structure with opposite handedness relative to that of the (l -) antiparallel β-sheet. We use molecular dynamics to characterize the chiral water superstructure at atomic resolution. The results show that the macroscopic chirality of antiparallel β-sheets breaks the symmetry of assemblies of surrounding water molecules. We also calculate the chiral SFG response of water surrounding (l -) and (d -) LK7β to confirm the presence of chiral water structures. Our results offer a different perspective as well as introduce experimental and computational methodologies for elucidating hydration of biomacromolecules. The findings imply potentially important but largely unexplored roles of water solvent in chiral selectivity of biomolecular interactions and the molecular origins of homochirality in the biological world. -
Konstantinovsky, Daniel ; Perets, Ethan A. ; Santiago, Ty ; Velarde, Luis ; Hammes-Schiffer, Sharon ; Yan, Elsa C. Y. ( , ACS Central Science)