Retardation of Bulk Water Dynamics by Disaccharide Osmolytes.

The bioprotective nature of disaccharides is hypothesized to derive from the modification of the hydrogen bonding network of water which protects biomolecules through lowered water activity at the protein interface. Using ultrafast fluorescence spectroscopy, we measured the relaxation of bulk water dynamics around the induced dipole moment of two fluorescent probes (Lucifer Yellow Ethylenediamine and Tryptophan). Our results indicate a reduction in bulk water reorganization rate of approximately 30%. We observe this retardation in the low concentration regime measured at 0.1 and 0.25 M, far below the onset of glassy dynamics. This reduction in water activity could be significant in crowded biological systems, contributing to global change in protein energy landscape, resulting in a significant enhancement of protein stability under environmental stress. We observed similar dynamic reduction for two disaccharide osmolytes, sucrose and trehalose, with trehalose being the more effective in reducing solvation dynamics.

[1]  B. Halle,et al.  Hydration and mobility of trehalose in aqueous solution. , 2012, The journal of physical chemistry. B.

[2]  C. Behm.  The role of trehalose in the physiology of nematodes. , 1997, International journal for parasitology.

[3]  Jonathan C. Wright.  Cryptobiosis 300 years on from van Leuwenhoek : what have we learned about tardigrades? , 2001 .

[4]  Samir Kumar Pal,et al.  Dynamics of water in biological recognition. , 2004, Chemical reviews.

[5]  J. Brady,et al.  Reversible dehydration of trehalose and anhydrobiosis: from solution state to an exotic crystal? , 2001, Carbohydrate research.

[6]  C. Colaco,et al.  The role of trehalose and other carbohydrates in biopreservation. , 1993, Biotechnology & genetic engineering reviews.

[7]  J. Lee,et al.  The stabilization of proteins by sucrose. , 1981, The Journal of biological chemistry.

[8]  M. Maroncelli,et al.  Subpicosecond Measurements of Polar Solvation Dynamics: Coumarin 153 Revisited , 1995 .

[9]  J. Brady,et al.  Reversible dehydration of trehalose and anhydrobiosis: from solution state to an exotic crystal? , 2001 .

[10]  E. Taylor,et al.  Sucralose Destabilization of Protein Structure. , 2015, The journal of physical chemistry letters.

[11]  M. Maroncelli,et al.  Computer simulation of the dynamics of aqueous solvation , 1988 .

[12]  P. Bordat,et al.  Influence of homologous disaccharides on the hydrogen-bond network of water: complementary Raman scattering experiments and molecular dynamics simulations. , 2005, Carbohydrate research.

[13]  R. Campen,et al.  Disaccharide topology induces slowdown in local water dynamics. , 2011, The journal of physical chemistry. B.

[14]  B. Halle,et al.  Protein hydration dynamics in solution: a critical survey. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[15]  U. Landman,et al.  Relaxation dynamics following transition of solvated electrons , 1989 .

[16]  J. Knutson,et al.  Chapter 8 Ultrafast Fluorescence Spectroscopy via Upconversion , 2008 .

[17]  M. Sola-Penna,et al.  Stabilization against thermal inactivation promoted by sugars on enzyme structure and function: why is trehalose more effective than other sugars? , 1998, Archives of biochemistry and biophysics.

[18]  Graham R. Fleming,et al.  Femtosecond solvation dynamics of water , 1994, Nature.

[19]  Milo M. Lin,et al.  Solvation in protein (un)folding of melittin tetramer–monomer transition , 2009, Proceedings of the National Academy of Sciences.

[20]  D. Fioretto,et al.  Rotational dynamics of trehalose in aqueous solutions studied by depolarized light scattering. , 2010, The Journal of chemical physics.

[21]  A. Tortschanoff,et al.  Relaxation dynamics of tryptophan in water: A UV fluorescence up-conversion and molecular dynamics study. , 2010, The journal of physical chemistry. A.

[22]  E. Vauthey,et al.  Ultrafast excited-state dynamics of oxazole yellow DNA intercalators. , 2007, The journal of physical chemistry. B.

[23]  Jianhua Xu,et al.  Ultrafast fluorescence spectroscopy via upconversion applications to biophysics. , 2008, Methods in enzymology.

[24]  T. Uchida,et al.  Trehalose solution viscosity at low temperatures measured by dynamic light scattering method : Trehalose depresses molecular transportation for ice crystal growth , 2009 .

[25]  N Sasaki,et al.  Thermostabilization and thermoactivation of thermolabile enzymes by trehalose and its application for the synthesis of full length cDNA. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[26]  R. Bhat,et al.  Why Is Trehalose an Exceptional Protein Stabilizer? , 2003, Journal of Biological Chemistry.

[27]  M. Maroncelli,et al.  Picosecond solvation dynamics of coumarin 153: The importance of molecular aspects of solvation , 1987 .

[28]  N. Ernsting,et al.  Observing the Hydration Layer of Trehalose with a Linked Molecular Terahertz Probe. , 2014, The journal of physical chemistry letters.

[29]  P. Yancey.  Water Stress, Osmolytes and Proteins1 , 2001 .

[30]  L. Ingram,et al.  Enhanced Trehalose Production Improves Growth of Escherichia coli under Osmotic Stress , 2005, Applied and Environmental Microbiology.

[31]  S. N. Timasheff,et al.  On the role of surface tension in the stabilization of globular proteins , 1996, Protein science : a publication of the Protein Society.

[32]  P. Belton,et al.  The trehalose coating effect on the internal protein dynamics. , 2012, Physical chemistry chemical physics : PCCP.

[33]  J. Thevelein,et al.  Role of trehalose in survival of Saccharomyces cerevisiae under osmotic stress. , 1998, Microbiology.

[34]  H. Stanley,et al.  Microscopic mechanism of protein cryopreservation in an aqueous solution with trehalose , 2013, Scientific Reports.

[35]  J. Crowe,et al.  Anhydrobiosis in nematodes: Carbohydrate and lipid metabolism during dehydration , 1975 .

[36]  Seunho Jung,et al.  Molecular dynamics simulations of trehalose as a 'dynamic reducer' for solvent water molecules in the hydration shell. , 2006, Carbohydrate research.

[37]  A. Zewail,et al.  Hydration dynamics at fluorinated protein surfaces , 2010, Proceedings of the National Academy of Sciences.

[38]  P. Karplus,et al.  Molecular Dynamics Studies of the Hydration of α,α-Trehalose , 1997 .

[39]  O. Kel,et al.  Site-dependent excited-state dynamics of a fluorescent probe bound to avidin and streptavidin. , 2009, Chemphyschem : a European journal of chemical physics and physical chemistry.

[40]  J. Smith,et al.  Solvent dependence of dynamic transitions in protein solutions. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[41]  J. Carpenter,et al.  The role of vitrification in anhydrobiosis. , 1998, Annual review of physiology.

[42]  S. N. Timasheff,et al.  The thermodynamic mechanism of protein stabilization by trehalose. , 1997, Biophysical chemistry.

[43]  P. Bordat,et al.  Low-frequency vibrational properties of lysozyme in sugar aqueous solutions: a Raman scattering and molecular dynamics simulation study. , 2009, The Journal of chemical physics.

[44]  L. Sømme.  Anhydrobiosis and cold tolerance in tardigrades , 2013 .

[45]  Awanish Kumar,et al.  Trehalose protects urea-induced unfolding of α-chymotrypsin. , 2010, International journal of biological macromolecules.

[46]  I. Roy,et al.  Effect of trehalose on protein structure , 2008, Protein science : a publication of the Protein Society.

[47]  K. Storey,et al.  Frozen and alive. , 1990, Scientific American.

[48]  A. Tortschanoff,et al.  Femtosecond fluorescence upconversion setup with broadband detection in the ultraviolet. , 2007, Optics letters.

[49]  E. Vauthey,et al.  Ultrafast solvation dynamics of coumarin 153 in imidazolium-based ionic liquids. , 2006, The journal of physical chemistry. A.

[50]  E. Vauthey,et al.  Excited-state dynamics of the fluorescent probe Lucifer Yellow in liquid solutions and in heterogeneous media , 2005, Photochemical and Photobiological Sciences.

[51]  S. Magazù,et al.  Alpha,alpha-trehalose-water solutions. VIII. Study of the diffusive dynamics of water by high-resolution quasi elastic neutron scattering. , 2006, The journal of physical chemistry. B.