Slower reorientation of hydration water surrounding trehalose compared to maltose and sucrose

Abstract

Trehalose, in the presence of water, exhibits the strongest bioprotective effects among disaccharides across a wide temperature range. To elucidate the molecular origin of trehalose’s superiority, it is important to compare the hydration state of different disaccharides under dilute conditions, which selectively reflects the interactions between water and single solute molecules without interferences from other disaccharide molecules, in terms of the following hydration properties: hydration number, reorientational cooperativity, and reorientational relaxation time. Specifically, the solute dependence of those hydration properties at different concentrations and different temperatures is worth investigating although such comprehensive understandings are yet to be achieved. In this study, we performed dielectric spectroscopy (from 80 MHz to 1 THz) on 0.5%–5% aqueous solutions of maltose, sucrose, and trehalose at 283, 298, and 313 K. The concentration-dependent analysis at 298 K revealed an almost identical hydration number (∼25 hydration water per solute molecule) and reorientational cooperativity (∼1.2 times greater than bulk water) for all the disaccharides. However, hydration water surrounding trehalose, with ∼three times slower reorientation than bulk water, exhibited the longest reorientational relaxation time among the three disaccharides, by up to 10%. The temperature-dependent analysis also showed that trehalose significantly differs only in reorientational relaxation time even at 283 and 313 K. These results demonstrate that, compared to maltose and sucrose, the hydration water surrounding trehalose is characterized only by its slowest reorientation and not by the hydration number or reorientational cooperativity. Our findings offer a possible mechanism of the superior bioprotective effects of trehalose to other disaccharides.