title: Tardigrades Use Intrinsically Disordered Proteins to Survive Desiccation.
abstract: Tardigrades are microscopic animals that survive a remarkable array of stresses, including desiccation. How tardigrades survive desiccation has remained a mystery for more than 250 years. 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. Here we show that tardigrade-specific intrinsically disordered proteins (TDPs) are essential for desiccation tolerance. TDP genes are constitutively expressed at high levels or induced during desiccation in multiple tardigrade species. TDPs are required for tardigrade desiccation tolerance, and these genes are sufficient to increase desiccation tolerance when expressed in heterologous systems. TDPs form non-crystalline amorphous solids (vitrify) upon desiccation, and this vitrified state mirrors their protective capabilities. 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.
authors.affiliation: Department of Chemistry, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA; Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA. Electronic address: tboothby@gmail.com.
authors.forename: Thomas C
authors.initials: TC
authors.lastname: Boothby
authors.affiliation: Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA.
authors.forename: Hugo
authors.initials: H
authors.lastname: Tapia
authors.affiliation: Department of Chemical and Biomolecular Engineering, North Carolina State University, Raleigh, NC 27695, USA.
authors.forename: Alexandra H
authors.initials: AH
authors.lastname: Brozena
authors.affiliation: Department of Chemistry, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
authors.forename: Samantha
authors.initials: S
authors.lastname: Piszkiewicz
authors.affiliation: Department of Chemistry, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
authors.forename: Austin E
authors.initials: AE
authors.lastname: Smith
authors.affiliation: Department of Life Sciences, University of Modena and Reggio Emilia, Modena 41125, Italy.
authors.forename: Ilaria
authors.initials: I
authors.lastname: Giovannini
authors.affiliation: Department of Life Sciences, University of Modena and Reggio Emilia, Modena 41125, Italy.
authors.forename: Lorena
authors.initials: L
authors.lastname: Rebecchi
authors.affiliation: Department of Chemistry, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
authors.forename: Gary J
authors.initials: GJ
authors.lastname: Pielak
authors.affiliation: Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA.
authors.forename: Doug
authors.initials: D
authors.lastname: Koshland
authors.affiliation: Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
authors.forename: Bob
authors.initials: B
authors.lastname: Goldstein
mesh_terms: D000064:Acclimatization; D000818:Animals; D003681:Dehydration / Q000201:enzymology* / Q000235:genetics; D003890:Desiccation; D004795:Enzyme Stability; D004798:Enzymes / Q000378:metabolism*; D004926:Escherichia coli / Q000201:enzymology / Q000235:genetics; D064267:Intrinsically Disordered Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D011487:Protein Conformation; D034622:RNA Interference; D012441:Saccharomyces cerevisiae / Q000201:enzymology / Q000235:genetics; D058467:Tardigrada / Q000201:enzymology* / Q000235:genetics; D015854:Up-Regulation; D058989:Vitrification
chemical_list: D004798:Enzymes; D064267:Intrinsically Disordered Proteins
keywords: CAHS proteins; anhydrobiosis; cryptobiosis; desiccation tolerance; freeze tolerance; intrinsically disordered proteins; tardigrades; trehalose; vitrification; water bear