Anomalously Rapid Hydration Water Diffusion Dynamics Near DNA Surfaces

The emerging Overhauser effect dynamic
nuclear polarization (ODNP)
technique measures the translational mobility of water within the
vicinity (5–15 Å) of preselected sites. The work presented
here expands the capabilities of the ODNP technique and illuminates
an important, previously unseen, property of the translational diffusion
dynamics of water at the surface of DNA duplexes. We attach nitroxide
radicals (i.e., spin labels) to multiple phosphate backbone positions
of DNA duplexes, allowing ODNP to measure the hydration dynamics at
select positions along the DNA surface. With a novel approach to ODNP
analysis, we isolate the contributions of water molecules at these
sites that undergo free translational diffusion from water molecules
that either loosely bind to or exchange protons with the DNA. The
results reveal that a significant population of water in a localized
volume adjacent to the DNA surface exhibits fast, bulk-like characteristics
and moves unusually rapidly compared to water found in similar probe
volumes near protein and membrane surfaces. Control studies show that
the observation of these characteristics are upheld even when the
DNA duplex is tethered to streptavidin or the mobility of the nitroxides
is altered. This implies that, as compared to protein or lipid surfaces,
it is an intrinsic feature of the DNA duplex surface that it interacts
only weakly with a significant fraction of the surface hydration water
network. The displacement of this translationally mobile water is
energetically less costly than that of more strongly bound water by
up to several kBT and
thus can lower the activation barrier for interactions involving the
DNA surface.