Cooperative Rotational Motion Triggered by a Water Switch: Dehydration and Rehydration of Cytosine Monohydrate

Abstract

Monohydrate and anhydrate crystalline forms of the DNA nucleobase cytosine interconvert via a topotactic solid-state mechanism where water functions as a molecular switch. The solid-state dehydration mechanism and kinetics were elucidated using complementary time-resolved synchrotron powder X-ray diffraction and thermogravimetric methods. Results indicate the reaction initiates from the crystal surface, involves no other crystalline intermediates, and proceeds at rates that depend on the monohydrate processing. A molecular-level model, based on least-motion arguments and consistent with the totality of the experimental data, is proposed to account for the high degree of structure transfer associated with the transformation. Water loss on the monohydrate crystal surface activates the rotation of one-dimensional cytosine ribbons, which in turn alters the local environment of the neighboring unit cell, facilitating the release of additional water molecules and ribbon rotation. As the dehydration front progresses into the solid, this cooperative mechanism effectively converts two-dimensional layers of antiparallel π-offset stacked ribbons into orthogonal two-dimensional layers of parallel π-face–face stacked ribbons. Moisture sorption experiments performed under high-humidity conditions confirm the anhydrate product can be reversibly rehydrated back to the monohydrate and that repeated dehydration–rehydration cycles proceed at consistent rates. The ability to track both the structural and compositional changes in the sample throughout the course of the reaction makes this a powerful combination of techniques for characterizing cooperative rotational motions triggered by water loss and/or uptake from crystalline materials.

Enhancement of Hydrate Stability through Substitutional Defects

“…Importantly, we previously showed that the DSC dehydration endotherms of as-grown (unground), hand-ground, and ball-milled CM had indistinguishable T max values . This confirmed that by DSC, CM dehydration temperatures determined were independent of particle size.…”

“…As expected, dehydration is faster as the isothermal temperature is increased. Previous work indicated that the CM dehydration kinetics varied depending on how the sample was processed (unground, manually-ground, or milled) . Samples shown in Figure were prepared by the same experimentalist using a similar grinding rigor.…”

“…For the dye-doped materials, the average E a = 108.6 ± 7.8 kJ/mol (CM-EB 100 ), E a = 131.3 ± 3.9 kJ/mol (CM-CR 200 ), and E a = 104.3 ± 10.6 kJ/mol (CM-AG 200 ). In comparison, the same model-free methods yielded an E a = 96.4 ± 1.7 kJ/mol for CM …”

Cytosine monohydrate under mechanical stress

“…The deformation patterns observed in CM are consistent with the activation of motion in the π-stacking direction that was previously proposed in the dehydration of CM to its anhydrate, Cd. 14 In that work, dehydration via concerted water loss and ribbon rotation were rationalized in terms of least-motion principles even though the reaction has a large associated 18.3% volume change. While there is no evidence to suggest that indentation at these forces results in water loss, the current nanoindentation studies provide additional support for the proposed ribbon–rotation model.…”

“…CM is stable under ambient conditions, though it dehydrates when subjected to elevated temperatures or low humidity environments. 8–13 In previous work, 14 we demonstrated through a combination of time-resolved synchrotron powder X-ray diffraction and TGA kinetic experiments that the hydrate to anhydrate solid state reaction is a reversible one-step process that does not appear to involve other crystalline intermediates. A molecular-level model based on water loss simultaneous with the cooperative rotation of 1-dimensional hydrogen bonded ribbons was proposed to account for the high degree of structure-transfer associated with the solid state reaction.…”