When Phased without Water: Biophysics of Cellular Desiccation, from Biomolecules to Condensates

Abstract

The molecular machinery that enables life has evolved in water, yet many of the organisms around us are able to survive even extreme desiccation. Especially remarkable are single-cell and sedentary organisms that rely on specialized biomolecular machinery to survive in environments that are routinely subjected to a near-complete lack of water. In this review, we zoom in on the molecular level of what is happening in the cellular environment under water stress. We cover the various mechanisms by which biochemical components of the cell can dysfunction in dehydrated cells and detail the different strategies that organisms have evolved to eliminate or cope with these desiccation-induced perturbations. We specifically focus on two survival strategies: (1) the use of disordered proteins to protect the cellular environment before, during, and in the recovery from desiccation, and (2) the use of biomolecular condensates as a self-assembly mechanism that can sequester or protect specific cellular machinery in times of water stress. We provide a summary of experimental work describing the critical contributions of disordered proteins and biomolecular condensates to the cellular response to water loss and highlight their role in desiccation tolerance. Desiccation biology is an exciting area of cell biology, still far from being completely explored. Understanding it on the molecular level is bound to give us critical new insights in how life adapted/can adapt to the loss of water, spanning from the early colonization of land to how we can deal with climate change in our future.

Helicity of a tardigrade disordered protein contributes to its protective function during desiccation

“…An emerging paradigm in the anhydrobiosis field is the prevalent enrichment of IDPs that help to mediate protection during drying (Hand et al, 2011; Hesgrove & Boothby, 2020; Romero‐Perez et al, 2023). Transient helicity, and the acquisition of increased helical content during desolvation, has been reported in many desiccation‐related IDPs spanning diverse families (Bremer et al, 2017; Shimizu et al, 2010; Tunnacliffe et al, 2010; Yamaguchi et al, 2012).…”

“…An emerging paradigm in the anhydrobiosis field is the involvement of intrinsically disordered proteins (IDPs) in mediating desiccation tolerance (Boothby et al, 2017; Boothby & Pielak, 2017; Romero‐Perez et al, 2023; Tunnacliffe et al, 2010; Yamaguchi et al, 2012). Some of the first IDPs implicated in anhydrobiosis were late embryogenesis abundant (LEA) proteins, which were first identified in cotton seeds (Dure et al, 1981), but have subsequently been found in a number of diverse organisms (Battista et al, 2001; Browne et al, 2002; Dure et al, 1981; Hand et al, 2011; Kikawada et al, 2006; Schokraie et al, 2010; Tunnacliffe et al, 2005).…”

Protecting Proteins from Desiccation Stress Using Molecular Glasses and Gels

“…Under dehydrating conditions, water molecules evaporate, and solute concentrations increase, challenging protein stability. , The contact of proteins with the air–water interface also increases. Proteins tend to adsorb and denature at the interface, to an extent comparable to their accumulation at water–oil interfaces (Figure ).…”

“…Glassy matrices also protect DNA and lipids, and similar strategies are employed in protection from other types of stress, including freezing. These aspects are not covered here, but excellent reviews are available. ,,,− …”

“…In the plant and fungi realm, desiccation tolerance is primarily, though not exclusively, observed in seeds, pollen, and spores. The ability of these reproductive elements to undergo reversible anhydrobiosis facilitates their efficient distribution, even under challenging environmental conditions, and their reactivation only when and where conditions are favorable …”