The H2O Helix: The Chiral Water Superstructure Surrounding DNA

The double helix structure of DNA comes as close as it gets in science to a household brand. Results reported by Petersen and co-workers uncover a new structure buried just at the surface of DNA: a chiral, helical superstructure of water molecules (Figure 1). The authors applied second-order nonlinear optical spectroscopy to observe the collective orientation of these waters. They propose that DNA shapes weakly bound water molecules into a right-handed helix that follows the contours of the DNA minor groove. The findings represent the first observation of a chiral water superstructure under ambient conditions, marking a new chapter in experimental studies of the DNA hydration shell. In the 1980s, X-ray crystal structures showed that all waters in the hydration shell of DNA do not behave the same, giving the first hint of a non-bulk-like ordering of water around DNA. This study and later NMR experiments revealed a “spine of hydration”: highly ordered water molecules in the minor groove of DNA with residence times of several hundred picoseconds. Nonetheless, the hydrated water molecules had not been observed using optical methods under ambient conditions. The major challenge comes from the background of a much larger population of water molecules in bulk solution. To make the observations, Petersen and co-workers relied on chiral vibrational sum frequency generation (SFG) spectroscopy. Chiral SFG does not require spectroscopic labels that could perturb the sample. While conventional SFG has long been used to probe structures and dynamics at interfaces, chiral SFG has recently emerged as a powerful method in probing chiral biomacromolecules. Under the dipole approximation, the second-order chiral SFG signal originates from an electric dipole response described by a third-rank (3 × 3 × 3) tensor. Hence, this response inherits enough dimensions and does not rely on relatively weak magnetic dipole and/or electric quadrupole to specify structural chirality. Thus, nonlinear chiral SFG provides higher sensitivity than conventional linear chiral optical methods (e.g., circular dichroism and Raman optical activity). This point is key to Petersen’s success in observing DNA’s chiral waters. The ability to observewithout labels or interference from the bulka chiral helix of ordered waters around DNA presents new research potential into the real-time dynamics, structures, and functions of hydrated DNA molecules. When Watson and Crick first proposed the double helix structure in 1953, they already predicted the delicate relationship between DNA structure and aqueous environments. Upon partial dehydration, the iconic “B-form” of DNA (with a minor groove of ∼7.3 Å and a major groove