Coexistence of vitreous and crystalline phases of H2O at ambient temperature

Formation of vitreous ice during rapid compression of water at room temperature is important for biology and the study of biological systems. Here, we show that Raman spectra of rapidly compressed water at greater than 1 GPa at room temperature exhibits the signature of high-density amorphous ice, whereas the X-ray diffraction (XRD) pattern is dominated by crystalline ice VI. To resolve this apparent contradiction, we used molecular dynamics simulations to calculate full vibrational spectra and diffraction patterns of mixtures of vitreous ice and ice VI, including embedded interfaces between the two phases. We show quantitatively that Raman spectra, which probe the local polarizability with respect to atomic displacements, are dominated by the vitreous phase, whereas a small amount of the crystalline component is readily apparent by XRD. The results of our combined experimental and theoretical studies have implications for detecting vitreous phases of water, survival of biological systems under extreme conditions, and biological imaging. The results provide additional insight into the stable and metastable phases of H₂O as a function of pressure and temperature, as well as of other materials undergoing pressure-induced amorphization and other metastable transitions.

Life as we know it on Earth depends on water. However, water also poses a critical challenge to life when it freezes at atmospheric pressure and low temperatures. The crystallization of H₂O to form hexagonal ice (ice Ih) under these conditions is accompanied by its well-known expansion, which has a dramatic impact on the structure and function of living cells. This crystallization of H₂O disrupts biological membranes and intracellular organization in living organisms and also displaces and concentrates salts and nutrients in the space between crystals (1). Like many liquids, however, rapid cooling of H₂O at ambient pressure to below its glass-transition temperature results in the formation of an amorphous phase known as low-density amorphous ice. Amorphous solid H₂O provides a chance for biological functions to survive where life otherwise cannot exist. Low-density amorphous ice is not the only amorphous form of H₂O. Ice I_h transforms to high-density amorphous (HDA) ice by application of ∼1 GPa of pressure at temperatures below 130 K (2, 3). In addition, a distinct, very-high-density amorphous state (vHDA) can form by isobaric heating and cooling of the HDA (4). low-density amorphous, high-density amorphous, and very-high-density amorphous state ice thus represent the three dominant, solid amorphous forms of H₂O at low temperatures.Solid amorphous phases of H₂O are broadly important in biology and biological applications. That amorphous H₂O which can exist over a broad range of temperatures, from cryogenic conditions to room temperature, is particularly interesting in the context of biological systems. Managing ice crystals is vital for extremophiles to survive damaging effects of H₂O crystallization. These organisms inhibit the growth of ice crystals and regulate the size and shape of the crystals using special antifreeze proteins (5, 6). Additionally, amorphous phases of H₂O are important in preserving biological samples in cryotomography applications. In cryotomography, the amorphous H₂O at low temperature is utilized routinely for sample preparation (7, 8), and significant efforts have been devoted to increase information obtained from cryotomography techniques. The low-temperature regime of amorphous H₂O routinely accessed in cryotomography creates challenges for light microscopy due to freezing of index-matching medium and objectives, which result in lowering the resolution of light microscopy in these applications. Room-temperature amorphous phases of H₂O are, therefore, advantageous for light microscopy applications and further development of techniques such as correlative light and electron microscopy (9–11).While formation of amorphous phases of H₂O below 200 K has been reported in many studies (2, 3, 12–16), a particularly interesting result is the observation of the Raman signature of HDA ice during fast compression of water at room temperature and moderate pressures (17). On the other hand, independent X-ray diffraction (XRD) measurements of H₂O on fast compression could not verify the formation of amorphous H₂O above 200 K (18). Here, we report high-resolution micro-Raman and synchrotron XRD measurements conducted in parallel in rapidly compressed samples of water in diamond anvil cells (DACs). Our findings, that are supported by molecular dynamics simulations, shed light on the nature of the HDA ice at room temperature and reconciled conflicting previous reports.