![]() Colored circles indicate CAHS (red), SAHS (blue), and MAHS (green) genes encoding tardigrade-specific IDPs. dujardini genes under hydrated and dry conditions. (C) MA plot showing enrichment (log 2 fold change) versus abundance (log 2 CPM ) of expressed H. dujardini after slow drying (95% relative humidity), quick drying (70% RH), and slow followed by quick drying. Animals desiccated at lower relative humidity experience increased rates of drying compared with those desiccated at higher relative humidity. ![]() (A) Published data on the survival versus relative humidity for Hypsibius dujardini (red), Paramacrobiotus richtersi (green), and Milnesium tardigradum (black). Tardigrades Upregulate Genes Encoding Tardigrade-Specific IDPs as They Dry This trend suggests that tardigrades need time to produce protectants, a theory supported by the recent evidence that de novo transcription and translation are required for the tardigrade Hypsibius dujardini to robustly survive desiccation ( Kondo et al., 2015). However, the role of IDPs in tardigrade desiccation tolerance remains untested.Īlthough no molecular mediators of desiccation tolerance have been identified in tardigrades, one clue as to how these animals survive desiccation comes from the observation ( Figure 1A) that different tardigrade species survive drying at different rates, but all species tested die if dried too quickly ( Wright, 1989). In the past two decades, myriad cellular roles for IDPs have emerged, including roles in transcription, post-translational modification, development, cellular organization, and abiotic stress tolerance ( Chakrabortee et al., 2012 Garay-Arroyo et al., 2000 Hincha and Thalhammer, 2012 Iakoucheva et al., 2004 Nott et al., 2015 Xie et al., 2007 Zhang et al., 2015). This latter class of proteins is enigmatic, in that unlike typical globular proteins, they lack persistent tertiary structure. In addition to trehalose and other sugars, a number of protein families and classes have been implicated in mediating desiccation tolerance in other systems, including heat-shock proteins, antioxidant enzymes, and some intrinsically disordered protein (IDP) families ( Hincha and Thalhammer, 2012 Hoekstra et al., 2001). Currently, the use and presence of trehalose in tardigrades are unclear some studies report low levels of this sugar, while others failed to identify trehalose at all in the same species ( Guidetti et al., 2011 Hengherr et al., 2008 Jönsson and Persson, 2010 Westh and Ramløv, 1991). However, some desiccation-tolerant animals do not require or even appear to make this sugar ( Lapinski and Tunnacliffe, 2003). Trehalose is essential for some organisms to survive desiccation and is thought to protect organisms by vitrifying their cellular contents ( Erkut et al., 2011 Sakurai et al., 2008 Tapia and Koshland, 2014). The disaccharide trehalose has been proposed and often assumed to play a role in mediating desiccation tolerance in tardigrades ( Hengherr et al., 2008 Jönsson and Persson, 2010 Westh and Ramløv, 1991). Although they have fascinated scientists for more than 250 years, little is known about how tardigrades survive such extreme environmental stresses, and no molecular mediators of tardigrade desiccation tolerance have been experimentally confirmed. Tardigrades (water bears) comprise a phylum of microscopic animals renowned for their ability to survive a vast array of environmental extremes, including essentially complete desiccation for up to a decade ( Goldstein and Blaxter, 2002). Our study identifies TDPs as functional mediators of tardigrade desiccation tolerance, expanding our knowledge of the roles and diversity of disordered proteins involved in stress tolerance. TDPs form non-crystalline amorphous solids (vitrify) upon desiccation, and this vitrified state mirrors their protective capabilities. TDPs are required for tardigrade desiccation tolerance, and these genes are sufficient to increase desiccation tolerance when expressed in heterologous systems. TDP genes are constitutively expressed at high levels or induced during desiccation in multiple tardigrade species. Here we show that tardigrade-specific intrinsically disordered proteins (TDPs) are essential for desiccation tolerance. Trehalose, a disaccharide essential for several organisms to survive drying, is detected at low levels or not at all in some tardigrade species, indicating that tardigrades possess potentially novel mechanisms for surviving desiccation. How tardigrades survive desiccation has remained a mystery for more than 250 years. Tardigrades are microscopic animals that survive a remarkable array of stresses, including desiccation.
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