Increasing intracellular trehalose is sufficient to confer desiccation tolerance to Saccharomyces cerevisiae

Abstract

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.trehalose | desiccation | yeast | anhydrobiosis | stress

Metabolic and stress responses of Acinetobacter oleivorans DR1 during long‐chain alkane degradation

“…Gluconeogenesis occurred during TRI degradation as indicated by high RPKM values of gluconeogenesis‐related genes ( eno , gpm I, fda ), which are associated with SUC metabolism (Table S2). Trehalose is also one of the representative alpha‐linked disaccharides synthesized intracellularly that helps cells to adapt to various stressors such as oxidative, heat, osmotic and desiccation stress (Benaroudj et al ., ; Purvis et al ., ; Doehlemann et al ., ; Tapia et al ., ). Trehalose measurement was performed using wild type and the otsA ‐disrupted strain.…”

Metabolic engineering of Saccharomyces cerevisiae for improvement in stresses tolerance

“…Trehalose functions as a protector for cell membranes and cellular proteins under environmental stresses such as heat, cold, desiccation, dehydration, ethanol, oxidation and anoxia. 22,26,27 In yeast, trehalose level is low under favorable growth condition but is induced by environmental stresses. However, Ratnakumar and Tunnacliffe 28 suggested that there was no consistent relationship between intracellular trehalose concentration and desiccation tolerance in S. cerevisiae.…”

A Tale of Two Sugars: Trehalose 6-Phosphate and Sucrose

“…One way in which trehalose protects cells is by initiating controlled autophagy, thereby avoiding uncontrolled damage that would otherwise trigger programmed cell death (Williams et al, 2015). Trehalose also confers desiccation tolerance on yeast cells (Tapia et al, 2015), in part by protecting them from oxidative damage by reactive oxygen species (Benaroudj et al, 2001). Many of the abiotic (and biotic) stresses faced by plants lead to reactive oxygen species production, and the accumulation of sugars such as trehalose and Suc is one of the mechanisms providing protection from oxidative stress (Romero et al, 2002;Cortina and Culianez-Macia, 2005;Couée et al, 2006;Luo et al, 2008;Chen and Hoehenwarter, 2015).…”