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Organization and mobility of water in amorphous and crystalline trehalose

Nature Materials volume 5, pages 632–635 (2006)Cite this article

Abstract

The disaccharide trehalose is accumulated by microorganisms, such as yeasts, and multicellular organisms, such as tardigrades1,2, when conditions of extreme drought occur. In this way these organisms can withstand dehydration through the formation of an intracellular carbohydrate glass, which, with its high viscosity and hydrogen-bonding interactions3,4, stabilizes and protects the integrity of complex biological structures and molecules. This property of trehalose can also be harnessed in the stabilization of liposomes5, proteins6 and in the preservation of red blood cells7, but the underlying mechanism of bioprotection is not yet fully understood. Here we use positron annihilation lifetime spectroscopy to probe the free volume of trehalose matrices; specifically, we develop a molecular picture of the organization and mobility of water in both amorphous and crystalline states. Whereas in amorphous matrices, water increases the average intermolecular hole size, in the crystalline dihydrate it is organized as a confined one-dimensional fluid in channels of fixed diameter that allow activated diffusion of water in and out of the crystallites. We present direct real-time evidence of water molecules unloading reversibly from these channels, thereby acting as both a sink and a source of water in low-moisture systems. We postulate that this behaviour may provide the overall stability required to keep organisms viable through dehydration conditions.

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Figure 1: Mean radius of holes in amorphous trehalose as a function of the water content at 25∘C.
Figure 2: Transitions in trehalose dihydrate heated in open cell under vacuum.
Figure 3: Isothermal dehydration of trehalose dihydrate under vacuum.

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Acknowledgements

We thank M.-I. Alonso and J.-P. Marquet for technical assistance. This research was sponsored by a postdoctoral grant from Nestec Ltd to the University of Bristol (D.K.).

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Authors and Affiliations

  1. H.H. Wills Physics Laboratory, University of Bristol, Tyndall Avenue, Bristol, BS8 1TL, UK

    Duncan Kilburn, Sam Townrow, Robert Richardson & Ashraf Alam

  2. Nestlé Research Center, Vers-chez-les-Blanc, CH-1000, Lausanne, 26, Switzerland

    Vincent Meunier & Job Ubbink

Authors
  1. Duncan Kilburn
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Correspondence to Job Ubbink.

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Kilburn, D., Townrow, S., Meunier, V. et al. Organization and mobility of water in amorphous and crystalline trehalose. Nature Mater 5, 632–635 (2006). https://doi.org/10.1038/nmat1681

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