Survival of Tardigrades in Extreme Environments: A Model Animal for Astrobiology
- 10 Citations
- 150 Mentions
- 2.1k Downloads
Abstract
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.
Keywords
Hydrated State Late Embryogenesis Abundant High Hydrostatic Pressure Flight Experiment Space VacuumNotes
Acknowledgments
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.
References
- Abe F, Kato C, Horikoshi K (1999) Pressure-regulated metabolism in microorganisms. Trends Microbiol 7:447–453PubMedCrossRefGoogle Scholar
- Alpert P (2006) Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? J Exp Biol 209:1575–1584PubMedCrossRefGoogle Scholar
- Altiero T, Rebecchi L (2001) Rearing tardigrades: results and problems. Zool Anz 240:217–221CrossRefGoogle Scholar
- 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
- Bertolani R (1970) Mitosi somatische e constanza cellulare numerica nei Tardigradi. Atti Accad Naz Lincei Rend Ser 8a:739–742Google 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 3:966–975PubMedCrossRefGoogle Scholar
- Cavicchioli R (2002) Extremophiles and the search for extraterrestrial life. Astrobiology 2:281–292PubMedCrossRefGoogle Scholar
- 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
- Crowe JH (1972) Evaporative water loss by tardigrades under controlled relative humidities. Biol Bull 142:407–416CrossRefGoogle Scholar
- Crowe JH, Crowe LM, Carpenter JF, Wistrom CA (1987) Stabilization of dry phospholipid bilayers and proteins by sugars. Biochem J 242:1–10PubMedGoogle Scholar
- 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
- 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
- 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
- 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
- Ducoff HS (1972) Causes of death in irradiated adult insects. Biol Rev 47:211–240PubMedCrossRefGoogle Scholar
- 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
- Franks F, Hatley RHM, Mathias SF (1991) Materials science and the production of shelf stable biologicals. Pharm Technol Int 3:24–34Google Scholar
- 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
- Guidetti R, Jönsson KI (2002) Long-term anhydrobiotic survival in semi-terrestrial micrometazoans. J Zool 257:181–187CrossRefGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Jönsson KI (2007) Tardigrades as a potential model organism in space research. Astrobiology 7:757–766PubMedCrossRefGoogle Scholar
- Jönsson KI, Harms-Ringdahl M, Torudd J (2005) Radiation tolerance in the eutardigrade Richtersius coronifer. Int J Radiat Biol 81:649–656PubMedCrossRefGoogle Scholar
- 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
- Keilin D (1959) The problem of anabiosis or latent life: history and current concept. Proc R Soc Lond B 150:149–191PubMedCrossRefGoogle Scholar
- 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
- Krisko A, Radman M (2010) Protein damage and death by radiation in Escherichia coli and Deinococcus radiodurans. PNAS 107:14373–14377PubMedCrossRefGoogle Scholar
- Lapinski J, Tunnacliffe A (2003) Anhydrobiosis without trehalose in bdelloid rotifers. FEBS Lett 553:387–390PubMedCrossRefGoogle Scholar
- Madin KAC, Crowe JH (1975) Anhydrobiosis in nematodes: carbohydrate and lipid metabolism during dehydration. J Exp Zool 193:335–342CrossRefGoogle 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 178:633–637PubMedGoogle Scholar
- 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
- 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
- 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
- Pigon A, Weglarska B (1955) Rate of metabolism in tardigrades during active life and anabiosis. Nature 176:121–122PubMedCrossRefGoogle Scholar
- Rahm PG (1921) Biologische und physiologische Beiträge zur Kenntnis de Moosfauna. Z allgem Physiol 20:1–35Google Scholar
- 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
- 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
- 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
- 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
- Rothschild LJ, Mancinelli RL (2001) Life in extreme environments. Nature 409:1092–1101PubMedCrossRefGoogle Scholar
- 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
- 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
- Seki K, Toyoshima M (1998) Preserving tardigrades under pressure. Nature 395:853–854CrossRefGoogle Scholar
- Suzuki AC (2003) Life history of Milnesium tardigradum Doyère (Tardigrada) under a rearing environment. Zool Sci 20:49–57PubMedCrossRefGoogle Scholar
- Watanabe M (2006) Anhydrobiosis in invertebrates. Appl Entomol Zool 41:15–31CrossRefGoogle Scholar
- 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
- 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
- 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
- Westh P, Ramløv H (1991) Trehalose accumulation in the tardigrade Adorybiotus coronifer during anhydrobiosis. J Exp Zool 258:303–311CrossRefGoogle Scholar
- Wise MJ, Tunnacliffe A (2004) POPP the question: what do LEA proteins do? Trends Plant Sci 9:13–17PubMedCrossRefGoogle Scholar
- Wright JC (1989) Desiccation tolerance and water-retentive mechanisms in tardigrades. J Exp Biol 142:267–292Google Scholar
- 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