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.

Mitochondrial alternative oxidase contributes to successful tardigrade anhydrobiosis

“…Accordingly, LEA proteins and heat shock proteins have been shown to be important for these animals’ successful anhydrobiosis while other mechanisms are more prominent in some of these animals than others. For example Artemia shrimps and nematodes produce significant levels of trehalose to replace water as cells dehydrate, while some species of tardigrades produce none at all [ 2 , 9 , 17 , 18 ]. On the other hand, three families of intrinsically disordered proteins were identified only in tardigrades, namely the Cytoplasmic-, Secreted-, and Mitochondrial- Abundant Heat Soluble (CAHS, SAHS, and MAHS, respectively) proteins, collectively termed Tardigrade Disordered Proteins (TDPs).…”

“…These proteins are highly expressed constitutively or significantly enriched in response to desiccation (e.g. [ 18 , 19 ],) but seem to be missing in some tardigrades, suggesting that anhydrobiosis in tardigrades cannot be attributed solely to TDPs [ 20 , 21 ]. However, available data appear to support a common and important role of proper mitochondria function in anhydrobiosis.…”

Mitochondrial Alternative Oxidase Contributes to Successful Tardigrade Anhydrobiosis

“…On the other hand, three families of intrinsically disordered proteins were identi ed only in tardigrades, namely the Cytoplasmic-, Secreted-, and Mitochondrial-Abundant Heat Soluble (CAHS, SAHS, and MAHS, respectively) proteins, collectively termed Tardigrade Disordered Proteins (TDPs). These proteins are highly expressed constitutively or signi cantly enriched in response to desiccation [e.g., [18][19]] but seem to be missing in some tardigrades, suggesting that anhydrobiosis in tardigrades cannot be attributed solely to TDPs [20][21].…”

A distinct molecular signature on anhydrobiotic cyanobacterial metallothioneins

“…Anhydrobiosis (life without water) is a reversible ametabolic state of suspended animation, in which some (anhydrobiotic) organisms enter when exposed to extreme desiccation and can withstand osmotic imbalances for decades (Hibshman et al, 2020). In addition, desiccated anhydrobiotic organisms display tolerance to several physical stresses, such as extreme temperatures, high hydrostatic pressures and ionizing radiation (Hibshman et al, 2020).…”

“…Anhydrobiosis (life without water) is a reversible ametabolic state of suspended animation, in which some (anhydrobiotic) organisms enter when exposed to extreme desiccation and can withstand osmotic imbalances for decades (Hibshman et al, 2020). In addition, desiccated anhydrobiotic organisms display tolerance to several physical stresses, such as extreme temperatures, high hydrostatic pressures and ionizing radiation (Hibshman et al, 2020). To ensure the maintenance of dry cells under these harsh conditions, anhydrobiosis-associated genes entails protective molecular adaptations that include the synthesis of non-reducing disaccharides, accumulation of late embryogenesis abundant (LEA) proteins, the activities of chaperones and repair enzymes (after rehydration), among other elements (Schill et al, 2009).…”