Trehalose renders dauer larva of Caenorhabditis elegans resistant to extreme desiccation

Water is essential for life on Earth. In the absence of it, however, some organisms are able to interrupt their life cycle and enter an ametabolic state, known as anhydrobiosis [1, 2]. Upon reappearance of water, anhydrobiotes can resume life activities. How can an organism cope with depletion of water? What are the molecular principles of anhydrobiosis? It is assumed that sugars (in particular trehalose) are instrumental for survival under anhydrobiotic conditions and for the preservation of cellular structure [3, 4]. However, the role of trehalose remained obscure since the corresponding evidence was purely correlative and based mostly on in vitro studies. So far, genetic manipulations on trehalose metabolism of anhydrobiotic animals with the aim to study desiccation tolerance have not been reported. In order to study molecular mechanisms of anhydrobiosis, we decided to make use of one of the best genetic models, Caenorhabditis elegans. In this study we show that C. elegans dauer larva is a true anhydrobiote: Under defined conditions it can survive extreme desiccation and lose up to 98% of its body water. This ability is correlated with a several fold increase in the amount of trehalose. To study the role of trehalose, we produced a strain that cannot synthesize it and show that mutant larvae do not survive even mild dehydration. This strain allowed us dissecting the function of trehalose on the cellular and molecular levels. Light and electron microscopy show that one of the major functions of trehalose on the cellular level is the preservation of membrane organization. Fourier-transform infrared spectroscopy of whole worms suggests that this is achieved by preserving homogeneous and compact packing of lipid acyl chains. The damage in the absence of trehalose occurs already during desiccation and spectroscopy allows distinguishing a “dry, yet alive” larva from a “dry and dead” one.