Anoxia pp 205-217 | Cite as

Survival of Tardigrades in Extreme Environments: A Model Animal for Astrobiology

  • Daiki D. HorikawaEmail author
Part of the Cellular Origin, Life in Extreme Habitats and Astrobiology book series (COLE, volume 21)


Tardigrades, which are tiny invertebrate animals, have been considered as an appropriate model for astrobiological studies based on their high survival ability under various types of environmental stresses. So far, researches have shown that tardigrades have high tolerance to ionizing radiation, wide ranges of temperatures, vacuum, and high pressures in anhydrobiosis, a state that organisms lack free water in the body, and they resume activity when water is added. In addition, recently, a short-term flight experiment demonstrated that tardigrades in an anhydrobiotic state survived open space environments at low Earth orbit. Results from those exposure experiments indicate that tardigrades are well tolerant of extremely low temperatures, vacuum, and high pressures. On the other hand, ionizing radiation, UV radiation, and high temperatures could be the critical factors to limit habitable environments for tardigrades. Future astrobiological research on tardigrades, such as long-term exposure experiments, might provide important insight into the possibilities of existence of animal-like life forms or interplanetary transfer of multicellular organisms in an anhydrobiotic state.


Hydrated State Late Embryogenesis Abundant High Hydrostatic Pressure Flight Experiment Space Vacuum 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



I thank Lynn J. Rothschild and John Cumbers from NASA Ames Research Center for providing research advice on my studies. I also thank the NASA Astrobiology Institute Postdoctoral Program for supporting my research project at NASA Ames Research Center.


  1. Abe F, Kato C, Horikoshi K (1999) Pressure-regulated metabolism in microorganisms. Trends Microbiol 7:447–453PubMedCrossRefGoogle Scholar
  2. Alpert P (2006) Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? J Exp Biol 209:1575–1584PubMedCrossRefGoogle Scholar
  3. Altiero T, Rebecchi L (2001) Rearing tardigrades: results and problems. Zool Anz 240:217–221CrossRefGoogle Scholar
  4. Becquerel P (1950) La suspension de la vie au dessous de 1/20 K absolu par demagnetization adiabatique de l’alun de fer dans le vide les plus eléve. C R hebd Séances Acad Sci Paris 231:261–263Google Scholar
  5. Bertolani R (1970) Mitosi somatische e constanza cellulare numerica nei Tardigradi. Atti Accad Naz Lincei Rend Ser 8a:739–742Google Scholar
  6. 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 3:966–975PubMedCrossRefGoogle Scholar
  7. Cavicchioli R (2002) Extremophiles and the search for extraterrestrial life. Astrobiology 2:281–292PubMedCrossRefGoogle Scholar
  8. Clegg JS (1962) Free glycerol in dormant cysts of the brine shrimp, Artemia salina, and its disappearance during development. Biol Bull 122:295–301CrossRefGoogle Scholar
  9. Crowe JH (1972) Evaporative water loss by tardigrades under controlled relative humidities. Biol Bull 142:407–416CrossRefGoogle Scholar
  10. Crowe JH, Crowe LM, Carpenter JF, Wistrom CA (1987) Stabilization of dry phospholipid bilayers and proteins by sugars. Biochem J 242:1–10PubMedGoogle Scholar
  11. Daly MJ, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Leapman RD, Lai B, Ravel B, Li SM, Kemner KM, Fredrickson JK (2007) Protein oxidation implicated as the primary determinant of bacterial radioresistance. PLoS Biol 5:769–779CrossRefGoogle Scholar
  12. Denekamp NY, Thorne MA, Kube M, Reinhardt R, Lubzens E (2009) Discovering genes associated with dormancy in the monogonont rotifer Brachionus plicatilis. BMC Genomics 10:108PubMedCrossRefGoogle Scholar
  13. Diaz B, Schulze-Makuch D (2006) Microbial survival rates of Escherichia coli and Deinococcus radiodurans under low temperature, low pressure, and UV–irradiation conditions, and their relevance to possible martian life. Astrobiology 6:332–347PubMedCrossRefGoogle Scholar
  14. Doyère PLN (1842) Memories sur les tardigrades. Sur le facilité que possedent les tardigrades, les rotifers, les anguillules des toits et quelques autres of animalcules, de revenir à la vie après été completement déssechées. Ann Sci Nat (Ser 2) 18:5Google Scholar
  15. Ducoff HS (1972) Causes of death in irradiated adult insects. Biol Rev 47:211–240PubMedCrossRefGoogle Scholar
  16. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sørensen MV, Haddock SHD, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749PubMedCrossRefGoogle Scholar
  17. Franks F, Hatley RHM, Mathias SF (1991) Materials science and the production of shelf stable biologicals. Pharm Technol Int 3:24–34Google Scholar
  18. Gabriel WN, McNuff R, Patel SK, Gregory TR, Jeck WR, Jones CD, Goldstein B (2007) The tardigrade Hypsibius dujardini, a new model for studying the evolution of development. Dev Biol 312:545–559PubMedCrossRefGoogle Scholar
  19. Guidetti R, Jönsson KI (2002) Long-term anhydrobiotic survival in semi-terrestrial micrometazoans. J Zool 257:181–187CrossRefGoogle Scholar
  20. Hand SC, Jones D, Menze MA, Witt TL (2007) Life without water: expression of plant LEA genes by an anhydrobiotic arthropod. J Exp Zool 307A:62–66CrossRefGoogle Scholar
  21. Hengherr S, Heyer AG, Köhler HR, Schill RO (2008) Trehalose and anhydrobiosis in tardigrades–evidence for divergence in responses to dehydration. FEBS J 275:281–288PubMedCrossRefGoogle Scholar
  22. Horikawa DD, Higashi S (2004) Desiccation tolerance of the tardigrade Milnesium tardigradum collected in Sapporo, Japan, and Bogor. Indonesia Zool Sci 21:813–816Google Scholar
  23. Horikawa DD, Sakashita T, Katagiri C, Watanabe M, Kikawada T, Nakahara Y, Hamada N, Wada S, Funayama T, Higashi S, Kobayashi Y, Okuda T, Kuwabara M (2006) Radiation tolerance in the tardigrade Milnesium tardigradum. Int J Radiat Biol 82:843–848PubMedCrossRefGoogle Scholar
  24. Horikawa DD, Kunieda T, Abe W, Watanabe M, Nakahara Y, Sakashita T, Hamada N, Wada S, Funayama T, Kobayashi Y, Katagiri C, Higashi S, Okuda T (2008) Establishment of a rearing system of the extremotolerant tardigrade Ramazzottius varieornatus: a new model animal for astrobiology. Astrobiology 8:549–556PubMedCrossRefGoogle Scholar
  25. Horikawa DD, Iwata K, Kawai K, Koseki S, Okuda T, Yamamoto K (2009) High hydrostatic pressure tolerance of four different anhydrobiotic animal species. Zool Sci 26:238–242PubMedCrossRefGoogle Scholar
  26. Horneck G (1999) Astrobiology studies of microbes in simulated interplanetary space. In: Ehrenfreund P, Krafft C, Kochan H, Pirronello V (eds) Laboratory astrophysics and space research. Springer, Berlin, pp 667–686CrossRefGoogle Scholar
  27. Horneck G (2003) Could life travel across interplanetary space? Panspermia revisited. In: Rothschild LJ, Lister AM (eds) Evolution of planet earth. Academic, Amsterdam, pp 109–127CrossRefGoogle Scholar
  28. Iwasaki T (1964) Sensitivity of Artemia eggs to the gamma-irradiation. III. The sensitivity and the duration of hydration. J Radiat Res 5:91–96CrossRefGoogle Scholar
  29. Johnson AP, Pratt LM, Vishnivetskaya T, Pfiffner S, Bryan RA, Dadachova E, White L, Radtke K, Chan E, Tronnick S, Borgonie G, Mancinelli R, Rotshchild L, Rogoff D, Horikawa DD, Onstott TC (2011) Extended survival of several microorganisms and relevant amino acid and biomarkers under simulated Martian surface conditions as a function of burial depth. Icarus 211:1162–1178CrossRefGoogle Scholar
  30. Jönsson KI (2007) Tardigrades as a potential model organism in space research. Astrobiology 7:757–766PubMedCrossRefGoogle Scholar
  31. Jönsson KI, Harms-Ringdahl M, Torudd J (2005) Radiation tolerance in the eutardigrade Richtersius coronifer. Int J Radiat Biol 81:649–656PubMedCrossRefGoogle Scholar
  32. Jönsson KI, Rabbow E, Schill RO, Harms-Ringdahl M, Rettberg P (2008) Tardigrades survive exposure to space in low Earth orbit. Curr Biol 18:R729–R731PubMedCrossRefGoogle Scholar
  33. Keilin D (1959) The problem of anabiosis or latent life: history and current concept. Proc R Soc Lond B 150:149–191PubMedCrossRefGoogle Scholar
  34. Kikawada T, Nakahara Y, Kanamori Y, Iwata K, Watanabe M, McGee B, Tunnacliffe A, Okuda T (2006) Dehydration-induced expression of late-embryogenesis abundant proteins in an anhydrobiotic chironomid. Biochem Biophys Res Commun 348:56–61PubMedCrossRefGoogle Scholar
  35. Krisko A, Radman M (2010) Protein damage and death by radiation in Escherichia coli and Deinococcus radiodurans. PNAS 107:14373–14377PubMedCrossRefGoogle Scholar
  36. Lapinski J, Tunnacliffe A (2003) Anhydrobiosis without trehalose in bdelloid rotifers. FEBS Lett 553:387–390PubMedCrossRefGoogle Scholar
  37. Madin KAC, Crowe JH (1975) Anhydrobiosis in nematodes: carbohydrate and lipid metabolism during dehydration. J Exp Zool 193:335–342CrossRefGoogle Scholar
  38. Mattimore V, Battista JR (1996) Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J Bacteriol 178:633–637PubMedGoogle Scholar
  39. May RM, Maria M, Guimard J (1964) Action différentielle des rayons x et ultraviolets sur le tardigrade Macrobiotus areolatus, a l’état actif et desséché. Bull Biol Fr Belg 98:349–367Google Scholar
  40. Neumann S, Reuner A, Brümmer F, Schill RO (2009) DNA damage in storage cells of anhydrobiotic tardigrades. Comp Biochem Physiol A 153:425–429CrossRefGoogle Scholar
  41. Ono F, Saigusa M, Uozumi T, Matsushima Y, Ikeda H, Saini NL, Yamashita M (2008) Effect of high hydrostatic pressure on a life of a tiny animal tardigrade. J Phys Chem Solids 69:2297–2300CrossRefGoogle Scholar
  42. Pigon A, Weglarska B (1955) Rate of metabolism in tardigrades during active life and anabiosis. Nature 176:121–122PubMedCrossRefGoogle Scholar
  43. Rahm PG (1921) Biologische und physiologische Beiträge zur Kenntnis de Moosfauna. Z allgem Physiol 20:1–35Google Scholar
  44. Ramløv H, Westh P (1992) Survival of the cryptobiotic eutardigrade Adorybiotus coronifer during cooling to −196°C: effect of cooling rate, trehalose level, and short-term acclimation. Cryobiology 29:125–130CrossRefGoogle Scholar
  45. Ramløv H, Westh P (2001) Cryptobiosis in the eutardigrade Adorybiotus coronifer: tolerance to alcohols, temperature and de novo protein synthesis. Zool Anz 240:517–523CrossRefGoogle Scholar
  46. Rebecchi L, Altiero T, Guidetti R, Cesari M, Bertolani R, Negroni M, Rizzo AM (2009a) Tardigrade resistance to space effects: first results of experiments on the LIFE-TARSE mission on FOTON-M3 (September 2007). Astrobiology 9:581–591PubMedCrossRefGoogle Scholar
  47. Rebecchi L, Cesari M, Altiero T, Frigieri A, Guidetti R (2009b) Survival and DNA degradation in anhydrobiotic tardigrades. J Exp Biol 212:4033–4039PubMedCrossRefGoogle Scholar
  48. Rothschild LJ, Mancinelli RL (2001) Life in extreme environments. Nature 409:1092–1101PubMedCrossRefGoogle Scholar
  49. Sakurai M, Furuki T, Akao K-i, Tanaka D, Nakara Y, Kikawada T, Watanabe M, Okuda T (2008) Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplanki. PNAS 105:5093–5098PubMedCrossRefGoogle Scholar
  50. Schokraie E, Hotz-Wagenblatt A, Warnken U, Mail B, Förster 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:e9502PubMedCrossRefGoogle Scholar
  51. Seki K, Toyoshima M (1998) Preserving tardigrades under pressure. Nature 395:853–854CrossRefGoogle Scholar
  52. Suzuki AC (2003) Life history of Milnesium tardigradum Doyère (Tardigrada) under a rearing environment. Zool Sci 20:49–57PubMedCrossRefGoogle Scholar
  53. Watanabe M (2006) Anhydrobiosis in invertebrates. Appl Entomol Zool 41:15–31CrossRefGoogle Scholar
  54. Watanabe M, Kikawada T, Yukuhiro F, Okuda T (2002) Mechanism allowing an insect to survive complete dehydration and extreme temperatures. J Exp Biol 205:2799–2802PubMedGoogle Scholar
  55. Watanabe M, Kikawada T, Okuda T (2003) Increase of internal ion concentration triggers trehalose synthesis associated with cryptobiosis in larvae of Polypedilum vanderplanki. J Exp Biol 206:2281–2286PubMedCrossRefGoogle Scholar
  56. Watanabe M, Sakashita T, Fujita A, Kikawada T, Horikawa DD, Nakahara Y, Wada S, Funayama T, Hamada N, Kobayashi Y, Okuda T (2006) Biological effects of anhydrobiosis in an African chironomid, Polypedilum vanderplanki on radiation tolerance. Int J Radiat Biol 82:587–592PubMedCrossRefGoogle Scholar
  57. Westh P, Ramløv H (1991) Trehalose accumulation in the tardigrade Adorybiotus coronifer during anhydrobiosis. J Exp Zool 258:303–311CrossRefGoogle Scholar
  58. Wise MJ, Tunnacliffe A (2004) POPP the question: what do LEA proteins do? Trends Plant Sci 9:13–17PubMedCrossRefGoogle Scholar
  59. Wright JC (1989) Desiccation tolerance and water-retentive mechanisms in tardigrades. J Exp Biol 142:267–292Google Scholar
  60. Yoshinaga K, Yoshioka H, Kurosaki H, Hirasawa K, Uritani M, Hasegawa M (1997) Protection by trehalose of DNA from radiation damage. Biosci Biotechnol Biochem 61:160–161PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V.  2012

Authors and Affiliations

  1. 1.Universety PAris Descartes-site NeckerParis Cedex 15France
  2. 2.Mediterranean Institute for Life SciencesSplitCroatia

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