Increasing intracellular trehalose is sufficient to confer desiccation tolerance to Saccharomyces cerevisiae.
Diverse organisms capable of surviving desiccation, termed anhydrobiotes, include species from bacteria, yeast, plants, and invertebrates. However, most organisms are sensitive to desiccation, likely due to an assortment of different stresses such as protein misfolding and aggregation, hyperosmotic stress, membrane fracturing, and changes in cell volume and shape leading to an overcrowded cytoplasm and metabolic arrest. The exact stress(es) that cause lethality in desiccation-sensitive organisms and how the lethal stresses are mitigated in desiccation-tolerant organisms remain poorly understood. The presence of trehalose in anhydrobiotes has been strongly correlated with desiccation tolerance. In the yeast Saccharomyces cerevisiae, trehalose is essential for survival after long-term desiccation. Here, we establish that the elevation of intracellular trehalose in dividing yeast by its import from the media converts yeast from extreme desiccation sensitivity to a high level of desiccation tolerance. This trehalose-induced tolerance is independent of utilization of trehalose as an energy source, de novo synthesis of other stress effectors, or the metabolic effects of trehalose biosynthetic intermediates, indicating that a chemical property of trehalose is directly responsible for desiccation tolerance. Finally, we demonstrate that elevated intracellular maltose can also make dividing yeast tolerant to short-term desiccation, indicating that other disaccharides have stress effector activity. However, trehalose is much more effective than maltose at conferring tolerance to long-term desiccation. The effectiveness and sufficiency of trehalose as an antagonizer of desiccation-induced damage in yeast emphasizes its potential to confer desiccation tolerance to otherwise sensitive organisms.
Department of Molecular and Cell Biology.
Hugo
H
Tapia
Department of Molecular and Cell Biology.
Lindsey
L
Young
Department of Chemistry, and.
Douglas
D
Fox
Department of Molecular and Cell Biology, Department of Chemistry, and Howard Hughes Medical Institute, University of California, Berkeley, CA 94705.
Carolyn R
CR
Bertozzi
Department of Molecular and Cell Biology, koshland@berkeley.edu.
Douglas
D
Koshland
D003593:Cytoplasm / Q000378:metabolism; D003890:Desiccation; D004187:Disaccharides / Q000378:metabolism; D024581:Glyceraldehyde-3-Phosphate Dehydrogenase (Phosphorylating) / Q000378:metabolism; D008320:Maltose / Q000378:metabolism; D009004:Monosaccharide Transport Proteins / Q000378:metabolism; D011401:Promoter Regions, Genetic; D012441:Saccharomyces cerevisiae / Q000502:physiology*; D029701:Saccharomyces cerevisiae Proteins / Q000378:metabolism; D013312:Stress, Physiological; D027981:Symporters / Q000378:metabolism; D014199:Trehalose / Q000378:metabolism*; D014867:Water / Q000502:physiology
D004187:Disaccharides; D009004:Monosaccharide Transport Proteins; D029701:Saccharomyces cerevisiae Proteins; D027981:Symporters; C067575:maltose transport system, S cerevisiae; D014867:Water; D008320:Maltose; D014199:Trehalose; D024581:Glyceraldehyde-3-Phosphate Dehydrogenase (Phosphorylating); C465226:TDH3 protein, S cerevisiae
anhydrobiosis; desiccation; stress; trehalose; yeast