Mechanisms of Desiccation Tolerance: Themes and Variations in Brine Shrimp, Roundworms, and Tardigrades

Abstract

Water is critical for the survival of most cells and organisms. Remarkably, a small number of multicellular animals are able to survive nearly complete drying. The phenomenon of anhydrobiosis, or life without water, has been of interest to researchers for over 300 years. In this review we discuss advances in our understanding of protectants and mechanisms of desiccation tolerance that have emerged from research in three anhydrobiotic invertebrates: brine shrimp (Artemia), roundworms (nematodes), and tardigrades (water bears). Discovery of molecular protectants that allow each of these three animals to survive drying diversifies our understanding of desiccation tolerance, and convergent themes suggest mechanisms that may offer a general model for engineering desiccation tolerance in other contexts.

Keywords: Artemia; C. elegans; LEA proteins; anhydrobiosis; desiccation tolerance; nematode; tardigrade; trehalose.

FIGURE 1

Examples of Artemia, Caenorhabditis elegans, and a tardigrade. (A) A transmission electron micrograph of an encysted embryo of Artemia franciscana. This image is reproduced with permission from Clegg et al., 1999. (B) A nauplius larva of Artemia hatches. Photo credit: Patrick Sorgeloos. (C) A desiccated dauer larva of C. elegans in the typical curled form. Scale bar = 50 μm. Photo credit: J. Hibshman. (D) A reproductive C. elegans adult. Photo credit: B. Goldstein. (E) A tardigrade (Hypsibius exemplaris) in the anhydrobiotic tun state. Scale bar = 50 μm. Photo credit: J. Hibshman. (F) An active tardigrade (Hypsibius exemplaris). Photo credit: Sinclair Stammers.

FIGURE 2

An illustration of molecular components and mechanisms implicated in desiccation tolerance. Common molecules that contribute to desiccation tolerance are depicted in subcellular compartments where they have been shown or are suggested to function. Some components like small heat shock proteins can occupy multiple subcellular compartments, as evidenced by p26 from Artemia. Desiccation can lead to protein misfolding and aggregation. During times of desiccation, proteins like sHSPs and LEAs may limit aggregation, and during recovery Hsp70 may refold these proteins to restore proteostasis. During gradual drying, metabolic preparations occur like upregulation of the glyoxylate shunt and production of trehalose. Three common models of protection during desiccation are depicted as well. Although highlighted in three separate insets, these mechanisms likely have a large degree of overlap. Note that components are not to scale. LEA, late embryogenesis abundant; CAHS, cytosolic abundant heat soluble; MAHS, mitochondrial abundant heat soluble; SAHS, secretory abundant heat soluble; Hsp40, 40 kilodalton heat shock protein; Hsp70, 70 kilodalton heat shock protein; Hsf1, heat shock factor 1.