Water Bears: The Biology of Tardigrades pp 273-293 | Cite as
Environmental Adaptations: Desiccation Tolerance
Abstract
Survival in microhabitats that experience extreme fluctuations in water availability and temperature requires extreme adaptations. Antonie van Leeuwenhoek was the first who describe the phenomenon of the resurrection of a desiccated rotifer in 1702. As with some rotifers and other small organisms, tardigrades enter a desiccated state known as anhydrobiosis to withstand such environmental conditions. This allows them to cope with the temporal variation of available water and to extend their lifespan in an anhydrobiotic state by up to 20 years without biological aging, according to the Sleeping Beauty hypothesis. Heat shock proteins serve as molecular chaperones to preserve or restore protein integrity, and tardigrade-specific intrinsically disordered proteins (TDPs) as well as metabolite help prevent the formation of damaging cellular compartments aggregates during water stress.
References
- Albertson NH, Nyström T, Kjelleberg S (1990) Functional mRNA half-lives in the marine Vibrio sp. S14 during starvation and recovery. J Gen Microbiol 136:2195–2199CrossRefGoogle Scholar
- Alpert P (2000) The discovery, scope, and puzzle of desiccation tolerance in plants. Plant Ecol 151:5–17CrossRefGoogle Scholar
- Altiero T, Rebecchi L, Bertolani R (2006) Phenotypic variations in the life history of two clones of Macrobiotus richtersi (Eutardigrada, Macrobiotidae). Hydrobiologia 558:33–40CrossRefGoogle Scholar
- Arakawa K (2018) The complete mitochondrial genome of Echiniscus testudo (Heterotardigrada: Echiniscidae). Mitochondrial DNA Part B 3:810–811CrossRefGoogle Scholar
- Arakawa K, Yoshida Y, Tomita M (2016) Genome sequencing of a single tardigrade Hypsibius dujardini individual. Sci Data 3:16006CrossRefGoogle Scholar
- Arrigo A-P, Müller WEG (2002) Small stress proteins. Springer, Berlin, I–XV, 1–270 ppGoogle Scholar
- Bahrndorff S, Tunnacliffe A, Wise MJ, McGee B, Holmstrup M, Loeschcke V (2008) Bioinformatics and protein expression analyses implicate LEA proteins in the drought response of Collembola. J Insect Physiol 55:210–217CrossRefGoogle Scholar
- Battista JR, Park MJ, McLemore AE (2001) Inactivation of two homologues of proteins presumed to be involved in the desiccation tolerance of plants sensitizes Deinococcus radiodurans R1 to desiccation. Cryobiology 43:133–139PubMedCrossRefGoogle Scholar
- Baumann H (1927) Anabiosis of tardigrades. Zool Anz 72:175–179Google Scholar
- Beisser D, Grohme M, Kopka J, Frohme M, Schill RO, Hengherr S, Dandekar T, Klau GW, Dittrich M, Müller T (2012) Integrated pathway modules using time-course metabolic profiles and EST data from Milnesium tardigradum. BMC Syst Biol 6:72PubMedPubMedCentralCrossRefGoogle Scholar
- Bell LN, Hageman MJ (1996) Glass transition explanation for the effect of polyhydroxy compounds on protein denaturation in dehydrated solids. J Food Sci Technol 61:372–378Google Scholar
- Bemm F, Weiss CL, Schultz J, Förster F (2016) Genome of a tardigrade: horizontal gene transfer or bacterial contamination? Proc Natl Acad Sci U S A 113:E3054–E3056PubMedPubMedCentralCrossRefGoogle Scholar
- Benítez L, Gutiérrez JC (1997) Encystment – specific mRNA is accumulated in the resting cysts of the ciliate Colpoda inflata. Biochem Mol Biol Int 41:1137–1141PubMedGoogle Scholar
- Bertolani R, Guidetti R, Jönsson KI, Altiero T, Boschini D, Rebecchi L (2004) Experiences with dormancy in tardigrades. J Limnol 63:16–25CrossRefGoogle Scholar
- Bianchi G, Gamba A, Limiroli R, Pzzi N, Ester R, Salamini F, Bartels D (1993) The unusual sugar composition in leaves of the resurrection plant Myrothamnus flabellifolia. Physiol Plant 87:223–226CrossRefGoogle Scholar
- Billi D (2009) Subcellular integrities in Chroococcidiopsis sp. CCMEE 029 survivors after prolonged desiccation revealed by molecular probes and genome stability assays. Extremophiles 13:49–57PubMedCrossRefGoogle Scholar
- Blasius M, Hubscher U, Sommer S (2008) Deinococcus radiodurans: what belongs to the survival kit? Crit Rev Biochem Mol Biol 43:221–238PubMedCrossRefGoogle Scholar
- Boothby TC, Tapia H, Brozena AH, Piszkiewicz S, Smith AE, Giovannini I, Rebecchi L, Pielak GJ, Koshland D, Goldstein B (2017) Tardigrades use intrinsically disordered proteins to survive desiccation. Mol Cell 65(975–984):e975CrossRefGoogle Scholar
- Boothby TC, Tenlen JR, Smith FW, Wang JR, Patanella KA, Nishimura EO, Tintori SC, Li Q, Jones CD, Yandell M, Messina DN, Glasscock J, Goldstein B (2015) Evidence for extensive horizontal gene transfer from the draft genome of a tardigrade. Proc Natl Acad Sci U S A 112:15976–15981PubMedPubMedCentralCrossRefGoogle Scholar
- Borner J, Rehm P, Schill RO, Ebersberger I, Burmester T (2014) A transcriptome approach to ecdysozoan phylogeny. Mol Phylogenet Evol 80:79–87PubMedCrossRefPubMedCentralGoogle Scholar
- Bose S, Weikl T, Bugl H, Buchner J (1996) Chaperone function of Hsp90-associated proteins. Science 274:1715–1717PubMedCrossRefGoogle Scholar
- Browne J, Tunnacliffe A, Burnell A (2002) Anhydrobiosis – plant desiccation gene found in a nematode. Nature 416:38PubMedCrossRefGoogle Scholar
- Browne JA, Dolan KM, Tyson T, Goyal K, Tunnacliffe A, Burnell AM (2004) Dehydration-specific induction of hydrophilic protein genes in the anhydrobiotic nematode Aphelenchus avenae. Eukaryot Cell 3:966–975PubMedPubMedCentralCrossRefGoogle Scholar
- Buitink J, Leprince O (2004) Glass formation in plant anhydrobiotes: survival in the dry state. Cryobiology 48:215–228PubMedCrossRefGoogle Scholar
- Byers TJ, Kim BG, King LE, Hugo ER (1991) Molecular aspects of the cell cycle and encystment of Acanthamoeba. Rev Infect Dis 5:373–384CrossRefGoogle Scholar
- Camonis J, Julien J, Ayala J, Jaequet M (1982) Polyadenylated RNA population present in dormant spores of Dictyostelium discoideum. Cell Differ (1):55–61CrossRefGoogle Scholar
- Carpenter JF, Crowe LM, Crowe JH (1987) Stabilization of phosphofructokinase with sugars during freeze-drying characterization of enhanced protection in the presence of divalent cations. Biochim Biophys Acta 923:109–115PubMedCrossRefGoogle Scholar
- Chandler J, Bartels D (1999) Plant desiccation. In: Lerner HR (ed) Plant responses to environmental stresses: from phytohormones to genome reorganization. Marcel Dekker, New York, pp 575–590Google Scholar
- Chen T, Amons R, Clegg JS, Warner AH, MacRae TH (2003) Molecular characterization of artemin and ferritin from Artemia franciscana. Eur J Biochem 270:137–145PubMedCrossRefGoogle Scholar
- Chen T, Villeneuve TS, Garant KA, Amons R, MacRae TH (2007) Functional characterization of artemin, a ferritin homolog synthesized in Artemia embryos during encystment and diapause. FEBS J 274:1093–1101PubMedCrossRefGoogle Scholar
- Clegg JS (1967) Metabolic studies of crytobiosis in encysted embryos of Artemia salina. Comp Biochem Physiol 20:801–809CrossRefGoogle Scholar
- Clegg JS (1986) The physical properties and metabolic status of Artemia cysts at low water contents: the water replacement hypothesis. In: Leopold AC (ed) Membranes, metabolism and dry organisms. Cornell University Press, New York, pp 169–187Google Scholar
- Clegg JS (1997) Embryos of Artemia franciscana survive four years of continuous anoxia: the case for complete metabolic rate depression. J Exp Biol 200:467–475PubMedGoogle Scholar
- Clegg JS (2007) Protein stability in Artemia embryos during prolonged anoxia. Biol Bull 212:74–81PubMedCrossRefGoogle Scholar
- Clegg JS, Conte F (1980) A review of the cellular and developmental biology of Artemia. In: Persoone GP, Sorgeloos P, Roels O, Jaspers E (eds) The brine shrimp, Artemia. Universa Press, Wetteren, pp 11–54Google Scholar
- Clegg JS, Drost-Hansen W (1990) On the biochemistry and cell physiology of water. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes. Elsevier, Amsterdam, pp 1–23Google Scholar
- Clegg JS, Jackson SA, Liang P, MacRae TH (1995) Nuclear-cytoplasmic translocations of protein p26 during aerobic-anoxic transitions in embryos of Artemia franciscana. Exp Cell Res 219:1–7PubMedCrossRefGoogle Scholar
- Clegg JS, Jackson SA, Warner AH (1994) Extensive intracellular translocations of a major protein accompany anoxia in embryos of Artemia franciscana. Exp Cell Res 212:77–83PubMedCrossRefGoogle Scholar
- Clegg JS, Willsie JK, Jackson SA (1999) Adaptive significance of a small heat shock/alpha-crystallin protein (p26) in encysted embryos of the brine shrimp, Artemia franciscana. Am Zool 39:836–847CrossRefGoogle Scholar
- Crowe JH (1971) Anhydrobiosis: an unsolved problem. Am Nat 105:563–573CrossRefGoogle Scholar
- Crowe JH (1975) The physiology of cryptobiosis in tardigrades. Memorie dell’Istituto Italiano di Idrobiologica 32(Suppl):37–59Google Scholar
- Crowe LM (2002) Lessons from nature: the role of sugars in anhydrobiosis. Comp Biochem Physiol A Mol Integr Physiol 131:505–513PubMedCrossRefGoogle Scholar
- Crowe JH, Clegg JS (1973) Anhydrobiosis. Dowden, Hutchinson and Ross, Stroudsburg, p 477Google Scholar
- Crowe JH, Clegg JS (1978) Dry biological systems. Academic Press, New YorkGoogle Scholar
- Crowe JH, Madin KAC (1975) Anhydrobiosis in nematodes: evaporative water loss and survival. J Exp Zool 193:323–333CrossRefGoogle Scholar
- Crowe JH, Crowe LM, Carpenter JF, Wistrom CA (1987) Stabilization of dry phospholipid bilayers and proteins by sugars. Biochem J 242:1–10PubMedPubMedCentralCrossRefGoogle Scholar
- Crowe JH, Crowe LM, Carpenter JF, Rudolph AS, Wistrom CA, Spargo BJ, Anchordoguy TJ (1988) Interactions of sugars with membranes. Biochim Biophys Acta 947:367–384PubMedCrossRefGoogle Scholar
- Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599PubMedCrossRefGoogle Scholar
- Crowe JH, Leslie SB, Crowe LM (1994) Is vitrification sufficient to preserve liposomes during freeze-drying? Cryobiology 31:355–366PubMedCrossRefGoogle Scholar
- Crowe JH, Crowe LM, Petrelski S, Hoekstra FA, Araujo PD, Panek AD (1997) Anhydrobiosis: cellular adaptation to extreme dehydration. In: Dantzler WH (ed) Handbook of physiology. Oxford University Press, New YorkGoogle Scholar
- Crowe JH, Carpenter JF, Crowe LM (1998) The role of vitrification in anhydrobiosis. Annu Rev Physiol 60:73–103PubMedCrossRefGoogle Scholar
- De Graaf J, Amons R, Möller W (1990) The primary structure of artemin from artemia cysts. Eur J Biochem 193:737–750PubMedCrossRefGoogle Scholar
- Doyère PLN (1842) Memoires sur les Tardigrades. Sur le facilité que possedent les Tardigrades, les rotiferes, les anguillules des toits et quelques autres animalcules, de revenir à la vie après été completement desséchées. Ann Sci Nat Zool Biol Anim 2e:5–35Google Scholar
- Drennan P, Smith M, Goldsworthly D, van Staden J (1993) The occurence of trehalose in the leaves of the desiccation-tolerant angiosperm Myrothamnus flabellifolius. J Plant Physiol 142:493–496CrossRefGoogle Scholar
- Ellis RJ (2004) From chloroplasts to chaperones: how one thing led to another. Photosynth Res 80:333–343CrossRefGoogle Scholar
- Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282CrossRefGoogle Scholar
- Fielding MJ (1951) Observations on the length of dormancy in certain plant infecting nematodes. Proc Helminthol Soc Wash 18:110–112Google Scholar
- Förster F, Beisser D, Frohme M, Schill RO, Dandekar T (2011a) Tardigrade bioinformatics: molecular adaptations, DNA j-family and dynamical modeling. J Zool Syst Evol Res 49:120–126CrossRefGoogle Scholar
- Förster F, Beisser D, Grohme M, Liang C, Mali B, Siegl AM, Engelmann JC, Shkumatov AV, Schokraie E, Müller T, Schnölzer M, Schill RO, Frohme M, Dandekar T (2011b) Transcriptome analysis in tardigrade species reveals specific molecular pathways for stress adaptations. Bioinf Biol Insights 6:69–96Google Scholar
- Förster F, Liang C, Shkumatov A, Beisser D, Engelmann JC, Schnölzer M, Frohme M, Müller T, Schill RO, Dandekar T (2009) Tardigrade workbench: comparing stress-related proteins, sequence-similar and functional protein clusters as well as RNA elements in tardigrades. BMC Genomics 10:469–479PubMedPubMedCentralCrossRefGoogle Scholar
- Franceschi T (1948) Anabiosi nei tardigradi. Boll Mus Ist Biot Univ Genova:47–49Google Scholar
- Freeman BC, Morimoto RI (1996) The human cytosolic molecular chaperones hsp90, hsp70 (hsc70) and hdj-1 have distinct roles in recognition of a non-native protein and protein refolding. EMBO J 15:2969–2979PubMedPubMedCentralCrossRefGoogle Scholar
- Galau GA, Hughes DW, Dure L III (1986) Abscisic-acid induction of cloned cotton gossypium-hirsutum late embryogenesis-abundant lea messenger rna species. Plant Mol Biol 7:155–170PubMedCrossRefGoogle Scholar
- Gething M-J, Sambrook J (1992) Protein folding in the cell. Nature 355:33–45PubMedPubMedCentralCrossRefGoogle Scholar
- Goodey T (1923) Quiescence and reviviscence in nematodes, with special reference to Tylenchus tritici and Tylenchus dipsaci. J Helminthol 1:47–52CrossRefGoogle Scholar
- Goyal K, Pinelli C, Maslen SL, Rastogi RK, Stephens E, Tunnacliffe A (2005) Dehydration-regulated processing of late embryogenesis abundant protein in a desiccation-tolerant nematode. FEBS Lett 579:4093–4098PubMedCrossRefPubMedCentralGoogle Scholar
- Goyal K, Tisi L, Basran A, Browne J, Burnell A, Zurdo J, Tunnacliffe A (2003) Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein. J Biol Chem 278:12977–12984PubMedCrossRefPubMedCentralGoogle Scholar
- Gros L, Saparbaev MK, Laval J (2002) Enzymology of the repair of free radicals-induced DNA damage. Oncogene 21:8905–8925PubMedCrossRefPubMedCentralGoogle Scholar
- Grzelezak ZF, Sattalo MH, Hanley-Bowdoin LK, Kennedy TD, Lane BG (1982) Synthesis and turnover of proteins and mRNA in germinating wheat embryos. Can J Biochem Physiol:389–397Google Scholar
- Guidetti R, Jönsson KI (2002) Long-term anhydrobiotic survival in semi-terrestrial micrometazonas. J Zool (Lond) 257:181–187CrossRefGoogle Scholar
- Guzhova I, Krallish I, Khroustalyova G, Margulis B, Rapoport A (2008) Dehydration of yeast: changes in the intracellular content of Hsp70 family proteins. Process Biochem 43:1138–1141CrossRefGoogle Scholar
- Hanafusa H (1969) Rapid transformation of cells by rous sarcoma virus. Proc Natl Acad Sci 63:318–325PubMedCrossRefPubMedCentralGoogle Scholar
- Harrigan PR, Madden TD, Cullis PR (1990) Protection of liposomes during dehydration or freezing. Chem Phys Lipids 52:139–149PubMedCrossRefPubMedCentralGoogle Scholar
- Hengherr S, Heyer AG, Brümmer F, Schill RO (2008) Trehalose as protecting agent in aquatic invertebrates during dormancy induced by desiccation. Comp Biochem Physiol A Comp Physiol 151:S34CrossRefGoogle Scholar
- Hengherr S, Heyer AG, Brümmer F, Schill RO (2011) Trehalose and vitreous states: desiccation tolerance in dormant stages of the crustaceans Triops and Daphnia. Physiol Biochem Zool 84:147–153PubMedCrossRefPubMedCentralGoogle Scholar
- Hengherr S, Schill RO (2011) Dormant stages in freshwater bryozoans – an adaptation to transcend environmental constraints. J Insect Physiol 57:595–601PubMedCrossRefGoogle Scholar
- Hengherr S, Worland MR, Reuner A, Brümmer F, Schill RO (2009) High-temperature tolerance in anhydrobiotic tardigrades is limited by glass transition. Physiol Biochem Zool 82:749–755PubMedCrossRefGoogle Scholar
- Hoekstra FA (1986) Water content in relation to stress in pollen. In: Leopold CA (ed) Membranes, metabolism and dry organisms. Cornell University Press, New YorkGoogle Scholar
- Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403PubMedCrossRefGoogle Scholar
- Jönsson KI, Bertolani R (2001) Facts and fiction about long-term survival in tardigrades. J Zool (Lond) 255:121–123CrossRefGoogle Scholar
- Jørgensen A, Møbjerg N, Kristensen RM (2007) A molecular study of the tardigrade Echiniscus testudo (Echiniscidae) reveals low DNA sequence diversity over a large geographical area. J Limnol 66:77–83CrossRefGoogle Scholar
- Kalichevsky MT, Jaroszkiewicz EM, Ablett S, Blanshard JMV, Lillford PJ (1992) The glass transition of amylopectin measured by DSC, DMTA and NMR. Carbohydr Polym 18:77–88CrossRefGoogle Scholar
- Keilin D (1959) The leeuwenhoek lecture. The problem of anabiosis or latent life: history and current concept. Proc R Soc Lond B Biol Sci 150:149–191PubMedCrossRefPubMedCentralGoogle Scholar
- Kikawada T, Nakahara Y, Kanamori Y, Iwata K-i, Watanabe M, McGee B, Tunnacliffe A, Okuda T (2006) Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid. Biochem Biophys Res Commun 348:56–61PubMedCrossRefPubMedCentralGoogle Scholar
- Kondo K, Kubo T, Kunieda T (2015) Suggested involvement of PP1/PP2A activity and de novo gene expression in anhydrobiotic survival in a tardigrade, Hypsibius dujardini, by chemical genetic approach. PLoS One 10:e0144803PubMedPubMedCentralCrossRefGoogle Scholar
- Koster KL, Leopold AC (1988) Sugars and desiccation tolerance in seeds. Plant Physiol (Rockv) 88:829–832CrossRefGoogle Scholar
- Lapinski J, Tunnacliffe A (2003) Anhydrobiosis without trehalose in bdelloid rotifers. FEBS Lett 553:387–390PubMedCrossRefGoogle Scholar
- Lee DL (1961) Two new species of cryptobiotic (anabiotic) freshwater nematodes, Actinolaimus hintoni sp. nov. and Dorylaimus keilini sp. nov. (Dorylaimidae). Parasitology 51:237–240CrossRefGoogle Scholar
- Liang P, Amons R, Clegg JS, MacRae TH (1997a) Molecular characterization of a small heat shock/alpha-crystallin protein in encysted Artemia embryos. J Biol Chem 272:19051–19058PubMedCrossRefGoogle Scholar
- Liang P, Amons R, MacRae TH, Clegg JS (1997b) Purification, structure and in vitro molecular-chaperone activity of Artemia p26, a small heatshock a-crystallin protein. Eur J Biochem 243:225–232PubMedCrossRefGoogle Scholar
- Liang P, MacRae TH (1999) The synthesis of a small heat shock/alpha-crystallin protein in Artemia and its relationship to stress tolerance during development. Dev Biol 207:445–456PubMedCrossRefGoogle Scholar
- Lindahl T (1993) Instability and decay of the primary structure of DNA. Nature 362:709–715PubMedCrossRefGoogle Scholar
- Madin KAC, Crowe JH (1975) Anhydrobiosis in nematodes: carbohydrate and lipid metabolism during dehydration. J Exp Zool 193:335–342CrossRefGoogle Scholar
- Mali B, Grohme M, Wełnicz W, Dandekar T, Schnölzer M, Reuter D, Schill RO, Frohme M (2008) Genomic analyses of cryptobiotic tardigrades. In: Wissenschaftliche Beiträge 2008. WildauGoogle Scholar
- Martinez-Guitarte JL, Planello R, Morcillo G (2007) Characterization and expression during development and under environmental stress of the genes encoding ribosomal proteins L11 and L13 in Chironomus riparius. Comp Biochem Physiol B Biochem Mol Biol 147:590–596PubMedCrossRefGoogle Scholar
- Mattimore V, Battista JR (1996) Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J Bacteriol 178:633–637PubMedPubMedCentralCrossRefGoogle Scholar
- McGee B, Schill RO, Tunnacliffe A (2004) Hydrophilic proteins in invertebrate anhydrobiosis. Integr Comp Biol 44:679–679Google Scholar
- Morimoto RI (1993) Cells in stress: transcriptional activation of heat shock genes. Science 259:1409–1410PubMedCrossRefGoogle Scholar
- Nathan DF, Vos MH, Lindquist S (1997) In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc Natl Acad Sci U S A 94:12949–12956PubMedPubMedCentralCrossRefGoogle Scholar
- Neumann S, Reuner A, Brümmer F, Schill RO (2009) DNA damage in storage cells of anhydrobiotic tardigrades. Comp Biochem Physiol A Mol Integr Physiol 153:425–429PubMedCrossRefGoogle Scholar
- Örstan A (1995) Desiccation survival of the eggs of the rotifer Adineta vaga (Davis, 1873). Hydrobiologia 313/314:373–375Google Scholar
- Örstan A (1998) Factors affecting long-term survival of dry bdelloid rotifers: a preliminary study. Hydrobiologia 387/388:327–331CrossRefGoogle Scholar
- Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496CrossRefGoogle Scholar
- Picard D, Khursheed B, Garabedian MJ, Fortin MG, Lindquist S, Yamamoto KR (1990) Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature 348:166–168PubMedCrossRefGoogle Scholar
- Potts M (2001) Desiccation tolerance: a simple process? Trends Microbiol 9:553–559PubMedCrossRefGoogle Scholar
- Prestrelski SJ, Tedeschi N, Arakawa T, Carpenter JF (1993) Dehydration-induced conformational transitions in proteins and their inhibition by stabilizers. Biophys J 65:661–671PubMedPubMedCentralCrossRefGoogle Scholar
- Priestley DA (1986) Seed aging. Cornell University Press, New YorkGoogle Scholar
- Rahm PG (1923) Biologische und physiologische Beiträge zur Kenntnis der Moosfauna. Zeitschrift für allgemeine Physiologie 20:1–34Google Scholar
- Ramazzotti G, Maucci W (1983) Il phylum Tardigrada. Memorie dell’Istituto Italiano di ldrobiologia. Istituto Italiano di idrobiologia, Verbana Pallanza, Italien, 1014 ppGoogle Scholar
- Ramløv H, Westh P (2001) Cryptobiosis in the eutardigrade Adorybiotus (Richtersius) coronifer: tolerance to alcohols, temperature and de novo protein synthesis. Zool Anz 240:517–523CrossRefGoogle Scholar
- Rebecchi L, Guidetti R, Borsari S, Altiero T, Bertolani R (2006) Dynamics of long-term anhydrobiotic survival of lichen-dwelling tardigrades. Hydrobiologia 558:23–30CrossRefGoogle Scholar
- Reuner A, Hengherr S, Mali B, Förster F, Arndt D, Reinhardt R, Dandekar T, Frohme M, Brümmer F, Schill RO (2009) Stress-response in tardigrades: differential gene expression of molecular chaperones. Cell Stress Chaperones 15:423–430PubMedPubMedCentralCrossRefGoogle Scholar
- Ricci C (1998) Anhydrobiotic capabilities of bdelloid rotifers. Hydrobiologia 387/388:321–326CrossRefGoogle Scholar
- Ricci C (2001) Dormancy patterns in rotifers. Hydrobiologia 446/447:1–11CrossRefGoogle Scholar
- Ricci C, Pagani M (1997) Desiccation of Panagrolaimus rigidus (nematoda): survival, reproduction and the influence on the internal clock. Hydrobiologia 347:1–13CrossRefGoogle Scholar
- Ricci C, Caprioli M (1998) Stress during dormancy: effect on recovery rates and life-history traits of anhydrobiotic animals. Aquat Ecol 32:353–359CrossRefGoogle Scholar
- Ricci C, Caprioli M (2005) Anhydrobiosis in bdelloid species, populations and individuals. Integr Comp Biol 45:759–763PubMedCrossRefGoogle Scholar
- Ricci C, Covino C (2005) Anhydrobiosis of Adineta ricciae: costs and benefits. Hydrobiologia 546:307–314CrossRefGoogle Scholar
- Ricci C, Vaghi L, Manzini ML (1987) Desiccation of rotifers (Macrotrachela quadricornifera): survival and reproduction. Ecology 68:1488–1494CrossRefGoogle Scholar
- Sakurai M, Furuki T, Akao K-i, Tanaka D, Nakahara Y, Kikawada T, Watanabe M, Okuda T (2008) Vitrification is essential for anhydrobiosis in an african chironomid, Polypedilum vanderplanki. Proc Natl Acad Sci 105:5093–5098PubMedCrossRefGoogle Scholar
- Schill RO, Fritz GB (2008) Desiccation tolerance in embryonic stages of the tardigrade. J Zool (Lond) 276:103–107CrossRefGoogle Scholar
- Schill RO, Steinbrück GHB, Köhler H-R (2004) Stress gene (hsp70) sequences and quantitative expression in Milnesium tardigradum (Tardigrada) during active and cryptobiotic stages. J Exp Biol 207:1607–1613PubMedCrossRefGoogle Scholar
- Schokraie E, Hotz-Wagenblatt A, Warnken U, Mali B, Frohme M, Forster F, Dandekar T, Hengherr S, Schill RO, Schnölzer M (2010) Proteomic analysis of tardigrades: towards a better understanding of molecular mechanisms by anhydrobiotic organisms. PLoS One 5:e9502.9501–e9502.9537CrossRefGoogle Scholar
- Schokraie E, Warnken U, Hotz-Wagenblatt A, Grohme M, Hengherr S, Förster F, Schill RO, Frohme M, Dandekar T, Schnölzer M (2012) Comparative proteome analysis of Milnesium tardigradum in early embryonic state versus adults in active and anhydrobiotic state. PLoS One 7:e45682PubMedPubMedCentralCrossRefGoogle Scholar
- Schöneich C (1999) Reactive oxygen species and biological aging: amechanistical approach. Exp Gerontol 34:19–34PubMedCrossRefPubMedCentralGoogle Scholar
- Schumacher RJ, Hansen WJ, Freeman BC, Alnemri E, Litwack G, Toft DO (1996) Cooperative action of Hsp70, Hsp90, and DnaJ proteins in protein renaturation. Biochemistry 35:14889–14898PubMedCrossRefGoogle Scholar
- Scott P (2000) Resurrection plants and the secrets of eternal leaf. Ann Bot (Lond) 85:159–166CrossRefGoogle Scholar
- Slade L, Levine H (1991) Beyond water activity: recent advances based on an alternative approach to the assessment of food quality and safety. Crit Rev Food Sci Nutr 30:115–360PubMedCrossRefGoogle Scholar
- Steiner G, Albin FE (1946) Resuscitation of the nematode Tylenchus polyhypnus n. sp. after almost 39 years’ dormancy. J Wash Acad Sci 36:97–99PubMedGoogle Scholar
- Sun WQ, Leopold AC (1997) Cytoplasmic vitrification and survival of anhydrobiotic organisms. Comp Biochem Physiol A Physiol 117:327–333CrossRefGoogle Scholar
- Tanaka S, Tanaka J, Miwa Y, Horikawa DD, Katayama T, Arakawa K, Toyoda A, Kubo T, Kunieda T (2015) Novel mitochondria-targeted heat-soluble proteins identified in the anhydrobiotic Tardigrade improve osmotic tolerance of human cells. PLoS One 10:e0118272PubMedPubMedCentralCrossRefGoogle Scholar
- Tissières A, Mitchell HK, Tracy UM (1974) Protein synthesis in the salivary glands of Drosophila melanogaster. J Mol Biol 84:389–398PubMedCrossRefGoogle Scholar
- Tomos D (1992) Life without water. Curr Biol 2:594–596PubMedCrossRefGoogle Scholar
- Tourancheau AB, Morin L, Yang T, Perasso R (1999) Messenger RNA in dormant cells of sterkiella histriomuscorum (oxytrichidae): identification of putative regulatory gene transcripts. Protist 150:137–147PubMedCrossRefGoogle Scholar
- Tunnacliffe A, de Castro AG, Manzanera M (2001) Anhydrobiotic engineering of bacterial and mammalian cells: is intracellular trehalose sufficient? Cryobiology 43:124–132PubMedCrossRefGoogle Scholar
- Tunnacliffe A, Lapinski J (2003) Resurrecting van Leeuwenhoek’s rotifers: a reappraisal of the role of disaccharides in anhydrobiosis. Philos Trans R Soc Lond Ser B Biol Sci 358:1755–1771CrossRefGoogle Scholar
- Tunnacliffe A, Lapinski J, McGee B (2005) A putative LEA protein, but no trehalose, is present in anhydrobiotic bdelloid rotifers. Hydrobiologia 546:315–321CrossRefGoogle Scholar
- Tunnacliffe A, Wise MJ (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften 94:791–812PubMedCrossRefGoogle Scholar
- van Leeuwenhoek A (1702) On certain animalcules found in the sediments in gutters of the roofs of houses. Letter 144. In: The selected works of Anton van Leeuwenhoek. London, pp 207–213Google Scholar
- Vertucci CW, Farrant JM (1995) Acquisition and loss of desiccation. Marcel Dekker, New YorkGoogle Scholar
- Warner AH, Brunet RT, MacRae TH, Clegg JS (2004) Artemin is an RNA-binding protein with high thermal stability and potential RNA chaperone activity. Arch Biochem Biophys 424:189–200PubMedCrossRefGoogle Scholar
- Watanabe M, Kikawada T, Minagawa N, Yukuhiro F, Okuda T (2002) Mechanism allowing an insect to survive complete dehydration and extreme temperatures. J Exp Biol 205:2799–2802PubMedGoogle Scholar
- Webb SJ, Dumasia MD, Bhorjee JS (1965) Bound water, inositol, and the biosynthesis of temperate and virulent bacteriophages by air-dried Escherichia coli. Can J Microbiol 11:141–150PubMedCrossRefGoogle Scholar
- Westh P, Ramlov H (1988) Cryptobiosis in arctic tardigrades with special attention to the appearance of trehalose. In: Petersen GH (eds) Bericht über die Grönland-Exkursion des Instituts für Polarökologie. Universität für Polarökologie, Kiel, pp 227–245Google Scholar
- Westh P, Ramlov H (1991) Trehalose accumulation in the tardigrade Adorybiotus coronifer during anhydrobiosis. J Exp Zool 258:303–311CrossRefGoogle Scholar
- Wharton DA (2003) The environmental physiology of antarctic terrestrial nematodes: a review. J Comp Physiol B Biochem Syst Environ Physiol 173:621–628CrossRefGoogle Scholar
- Wharton DA, Aalders O (1999) Desiccation stress and recovery in the anhydrobiotic nematode Ditylenchus dipsaci (Nematoda : Anguinidae). Eur J Entomol 96:199–203Google Scholar
- Willsie JK, Clegg JS (2002) Small heat shock protein p26 associates with nuclear lamins and HSP70 in nuclei and nuclear matrix fractions from stressed cells. J Cell Biochem 84:601–614PubMedCrossRefGoogle Scholar
- Wolkers WF, McCready S, Brandt WF, Lindsey GG, Hoekstra FA (2001) Isolation and characterization of a D-7 LEA protein from pollen that stabilizes glasses in vitro. Biochim Biophys Acta Protein Struct Mol Enzymol 1544:196–206CrossRefGoogle Scholar
- Wolkers WF, Oldenhof H, Alberda M, Hoekstra FA (1998) A Fourier transform infrared microspectroscopy study of sugar glasses: application to anhydrobiotic higher plant cells. Biochim Biophys Acta 1379:83–96PubMedCrossRefGoogle Scholar
- Wolkers WF, Tetteroo FA, Alberda M, Hoekstra FA (1999) Changed properties of the cytoplasmic matrix associated with desiccation tolerance of dried carrot somatic embryos. An in situ fourier transform infrared spectroscopic study. Plant Physiol 120:153–164PubMedPubMedCentralCrossRefGoogle Scholar
- Womersley CZ (1987) A re-evaluation of strategies employed by nematode anhydrobiotes in relation to their natural environment. In: Veech JA, Dickson DW (eds) Vistas on nematology. Society of Nematologists, Hyattsville, pp 165–173Google Scholar
- Wright JC (1991) The significance of four xeric parameters in the ecology of terrestrial tardigrada. J Zool (Lond) 224:59–77CrossRefGoogle Scholar
- Wright JC (2001) Cryptobiosis 300 years on from van Leuwenhoek: what have we learned about tardigrades? Zool Anz 240:563–582CrossRefGoogle Scholar
- Xu Y, Lindquist S (1993) Heat-shock protein hsp90 governs the activity of pp60v-src kinase. Proc Natl Acad Sci U S A 90:7074–7078PubMedPubMedCentralCrossRefGoogle Scholar
- Yamaguchi A, Tanaka S, Yamaguchi S, Kuwahara H, Takamura C (2012) Two novel heat-soluble protein families abundantly expressed in an anhydrobiotic tardigrade. PLoS One 7:e44209PubMedPubMedCentralCrossRefGoogle Scholar
- Yoshida Y, Koutsovoulos G, Laetsch DR, Stevens L, Kumar S, Horikawa DD, Ishino K, Komine S, Kunieda T, Tomita M, Blaxter M, Arakawa K (2017) Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus. PLoS Biol 15:e2002266PubMedPubMedCentralCrossRefGoogle Scholar