Skip to main content

Environmental Adaptations: Cryobiosis

Part of the Zoological Monographs book series (ZM,volume 2)

Abstract

Tardigrades are well known to withstand very low temperatures in the anhydrobiotic state. However, they even tolerate such low temperatures like −196 °C in the fully hydrated state which is then described with the term cryobiosis. Although this extreme subzero temperature tolerance got quite a lot of attention, there is little knowledge regarding their physiological and biochemical adaptations connected to ecological representative subzero temperatures. General studies on cold tolerance have highlighted some strategies including freeze avoidance, rapid cold hardening and freeze tolerance. Although studies on survival rates, cooling rates and ice formation in tardigrades show high interspecific variations in subzero temperature survival, the water bears seem to tolerate ice formation within their bodies and therefore belong to freeze-tolerant organisms. Calorimetric studies also provide evidence for homogenous ice nucleation, indicating that ice formation is not largely affected by ice-nucleating agents. Ability to tolerate low temperatures and freezing even in embryonic developmental stages further increases the adaptive benefit of tardigrades to cope with low-temperature events.

This is a preview of subscription content, access via your institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • DOI: 10.1007/978-3-319-95702-9_11
  • Chapter length: 16 pages
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
eBook
USD   149.00
Price excludes VAT (USA)
  • ISBN: 978-3-319-95702-9
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
Hardcover Book
USD   199.99
Price excludes VAT (USA)
Fig. 11.1
Fig. 11.2
Fig. 11.3
Fig. 11.4

References

  • Bale JS (1996) Insect cold hardiness: a matter of life and death. Eur J Entomol 93:369–382

    Google Scholar 

  • Block W (1991) To freeze or not to freeze - invertebrate survival of subzero temperatures. Funct Ecol 5:284–290

    CrossRef  Google Scholar 

  • Clark MS, Worland MR (2008) How insects survive the cold: molecular mechanisms - a review. J Comp Physiol B Biochem Syst Environ Physiol 178:917–933

    CAS  CrossRef  Google Scholar 

  • Convey P (2000) How does cold constrain life cycles of terrestrial plants and animals. CryoLetters 21:73–82

    CAS  PubMed  Google Scholar 

  • Crowe JH, Folkert A, Hoekstra I, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599

    CAS  CrossRef  Google Scholar 

  • Danks HV, Kukal O, Ring RA (1994) Insect cold-hardiness – insights from the Arctic. Arctic 47:391–404

    CrossRef  Google Scholar 

  • DeVries AL (1971) Glycoproteins as biological antifreeze agents in Antarctic fishes. Science 172:1152

    CAS  CrossRef  Google Scholar 

  • DeVries AL (1986) Antifreeze glycopeptides and peptides: interactions with ice and water. Methods Enzymol 127:293–303

    CAS  CrossRef  Google Scholar 

  • Doucet D, Walker VK, Qin W (2009) The bugs that came in from the cold: molecular adaptations to low temperatures in insects. Cell Mol Life Sci 66:1404–1418

    CAS  CrossRef  Google Scholar 

  • Duman JG (2001) Antifreeze and ice nucleator proteins in terrestrial arthropods. Annu Rev Physiol 63:327–357

    CAS  CrossRef  Google Scholar 

  • Elnitsky MA, Hayward SAL, Rinehart JP, Denlinger DL, Lee RE (2008) Cryoprotective dehydration and the resistance to inoculative freezing in the Antarctic midge, Belgica antarctica. J Exp Biol 211:524–530

    CrossRef  Google Scholar 

  • Franks F (1985) Biophysics and biochemistry at low temperatures. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Grewal PS, Bornstein-Forest S, Burnell AM, Glazer I, Jagdale GB (2006) Physiological, genetic, and molecular mechanisms of chemoreception, thermobiosis, and anhydrobiosis in entomopathogenic nematodes. Biol Control 38:54–65

    CAS  CrossRef  Google Scholar 

  • Halberg KA, Persson D, Ramløv H, Westh P, Møbjerg-Kristensen R, Møbjerg N (2009) Cyclomorphosis in Tardigrada: adaptation to environmental constraints. J Exp Biol 212:2803–2811

    CrossRef  Google Scholar 

  • Hengherr S, Brümmer F, Schill RO (2008a) Anhydrobiosis in tardigrades and ist effects on longevity traits. J Zool (Lond) 275:216–220

    CrossRef  Google Scholar 

  • Hengherr S, Heyer AG, Köhler HR, Schill RO (2008b) Trehalose and anhydrobiosis in tardigrades-evidence for divergence in responses to dehydration. FEBS J 275:281–288

    CAS  CrossRef  Google Scholar 

  • Hengherr S, Worland MR, Reuner A, Brümmer F, Schill RO (2009) Freeze tolerance, supercooling points and ice formation: comparative studies on the subzero temperature survival of limno-terrestrial tardigrades. J Exp Biol 212:802–807

    CAS  CrossRef  Google Scholar 

  • Hengherr S, Reuner A, Brümmer F, Schill RO (2010) Ice crystallization and freeze tolerance in embryonic stages of the tardigrade Milnesium tardigradum. Comp Biochem Physiol A 156:151–155

    CAS  CrossRef  Google Scholar 

  • Horikawa DD, Sakashita T, Katagiri C, Watanabe M, Kikawada T, Nakahara Y, Hamada N, Wada S, Funayama T, Higashi S (2006) Radiation tolerance in the tardigrade Milnesium tardigradum. Int J Radiat Biol 82:843–848

    CAS  CrossRef  Google Scholar 

  • Jönsson KI, Schill RO (2007) Induction of Hsp70 by desiccation, ionising radiation and heat-shock in the eutardigrade Richtersius coronifer. Comp Biochem Physiol B Biochem Mol Biol 146:456–460

    CrossRef  Google Scholar 

  • Kagoshima H, Kito T, Aizu T, Shin-I H, Kanda S, Kobayashi A, Toyoda A, Fujiyama Y, Kohara P, Convey P, Niki H (2012) Multi-decadal survival of an antarctic nematode, Plectus murrayi, in a -20°C stored moss sample. CryoLetters 33:280–288

    CAS  PubMed  Google Scholar 

  • Kelty JD, Lee RE (1999) Induction of rapid cold hardening by cooling at ecologically relevant rates in Drosophila melanogaster. J Insect Physiol 45:719–726

    CAS  CrossRef  Google Scholar 

  • Kikawada T, Nakahara Y, Kanamori Y, Iwata KI, Watanabe M, McGee B, Tunnacliffe A, Okuda T (2006) Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid. Biochem Biophys Res 348:56–61

    CAS  CrossRef  Google Scholar 

  • Knight CA, Duman JG (1986) Inhibition of recrystallization of ice by insect thermal hysteresis proteins: a possible cryoprotective role. Cryobiology 23:256–262

    CAS  CrossRef  Google Scholar 

  • Lalouette L, Kostal V, Colinet H, Gagneul D, Renault D (2007) Cold exposure and associated metabolic changes in adult tropical beetles exposed to fluctuating thermal regimes. FEBS J 274:1759–1767

    CAS  CrossRef  Google Scholar 

  • Lee RE, Costanzo JP (1998) Biological ice nucleation and ice distribution in cold-hardy ectothermic animals. Annu Rev Physiol 60:55–72

    CAS  CrossRef  Google Scholar 

  • Lee YJ, Chung TJ, Park CW, Hahn Y, Chung JH, Lee BL, Han DM, Jung YH, Kim S, Lee Y (1996) Structure and expression of the tenecin 3 gene in Tenebrio molitor. Biochem Biophys Res Commun 218:6–11

    CAS  CrossRef  Google Scholar 

  • Mackenzie AP, Derbyshire W, Reid DS (1977) Nonequilibrium freezing behaviour of aqueous systems. Philos Trans R Soc Lond Ser B Biol Sci 278:167–189

    CAS  CrossRef  Google Scholar 

  • Newsham KK, Maslen NR, Mcinnes S (2006) Survival of Antarctic soil metazoans at -80°C for six years. CryoLetters 27:269–280

    Google Scholar 

  • Overgaard J, Tomcala A, Sørensen JG, Holmstrup M, Krogh PH, Simek P, Kost lV (2008) Effects of acclimation temperature on thermal tolerance and membrane phospholipid composition in the fruit fly Drosophila melanogaster. J Insect Physiol 54:619–629

    CAS  CrossRef  Google Scholar 

  • Ramazzotti G, Maucci W (1983) The phylum tardigrada. Mem Ist Ital Idrob 41:1–1012

    Google Scholar 

  • Ramløv H (2000) Aspects of natural cold tolerance in ectothermic animals. Hum Reprod 15:26–46

    CrossRef  Google Scholar 

  • Ramløv H, Westh P (1992) Survival of the cyptobiotic Eutardigrade Adorybiotus coronifer during cooling to -196°C: effect of cooling rate, trehalose level, and short-term acclimation. Cryobiology 29:125–130

    CrossRef  Google Scholar 

  • Ramløv H, Westh P (2001) Cryptobiosis in the eutardigrade Adorybiotus (Richtersius) coronifer: tolerance to alcohols, temperature and de novo protein synthesis. Zool Anz 240:517–523

    CrossRef  Google Scholar 

  • Raymond JA, DeVries AL (1977) Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proc Natl Acad Sci U S A 74:2589–2593

    CAS  CrossRef  Google Scholar 

  • Ring RA, Danks HV (1994) Desiccation and cryoprotection—overlapping adaptations. CryoLetters 15:181–190

    Google Scholar 

  • Sakurai M, Furuki T, Akao K, 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 U S A 105:5093–5098

    CAS  CrossRef  Google Scholar 

  • Salvucci ME, Strecher DS, Henneberry TJ (2000) Heat shock proteins in whiteflies, an insect that accumulates sorbitol in response to heat stress. J Thermal Biol 25:363–371

    CAS  CrossRef  Google Scholar 

  • Schill RO, Fritz GB (2008) Desiccation tolerance in embryonic stages of the tardigrade Milnesium tardigradum. J Zool (Lond) 276:103–107

    CrossRef  Google Scholar 

  • Seki K, Toyoshima M (1998) Preserving tardigrades under pressure. Nature 395:853–854

    CAS  CrossRef  Google Scholar 

  • Sinclair BJ (2001) Field ecology of freeze tolerance: interannual variation in cooling rates, freeze-thaw and thermal stress in the microhabitat of the alpine cockroach Celatoblatta quinquemaculata. Oikos 93:286–293

    CrossRef  Google Scholar 

  • Sinclair BJ, Vernon P, Klok CJ, Chown SL (2003) Insects at low temperatures: an ecological perspective. Trends Ecol Evol 18:257–262

    CrossRef  Google Scholar 

  • Smith T, Wharton DA, Marshall CJ (2008) Cold tolerance of an Antarctic nematode that survives intracellular freezing: comparisons with other nematode species. J Comp Physiol B Biochem Syst Environ Physiol 178:93–100

    CAS  CrossRef  Google Scholar 

  • Sømme L, Meier T (1995) Cold tolerance in Tardigrada from Dronning Maud Land, Antarctica. Polar Biol 15:221–224

    CrossRef  Google Scholar 

  • Storey KB, Storey JM (1996) Natural freezing survival in animals. Annu Rev Ecol Syst 27:365–386

    CrossRef  Google Scholar 

  • Storey KB, Baust JG, Buescher P (1981) Determination of water “bound” by soluble subcellular components during low-temperature acclimation in the gall fly larva, Eurosta solidagensis. Cryobiology 18:315–321

    CAS  CrossRef  Google Scholar 

  • Sträßer M (1998) Klimadiagramm-Atlas der Erde, Bd. 1. Dortmunder Vertrieb für Bau und Planungsliteratur. Dortmund, Germany

    Google Scholar 

  • Suzuki AC (2003) Life history of Milnesium tardigradum Doyère (Tardigrada) under a rearing environment. Zool Sci (Tokyo) 20:40–57

    Google Scholar 

  • Tsujimoto M, Satoschi I, Hiroshi K (2016) Recovery and reproduction of an Antarctic tardigrade retrieved from a moss sample frozen for over 30 years. Cryobiology 72:78–81

    CrossRef  Google Scholar 

  • Watanabe M, Tanaka K (1998) Adult diapause and cold hardiness in Aulacophora nigripennis (Coleoptera: Chrysomelidae). J Insect Physiol 44:1103–1110

    CAS  CrossRef  Google Scholar 

  • Westh P, Kristensen RM (1992) Ice formation in the freeze-tolerant eutardigrades Adorybiotus coronifer and Amphibolus nebulosus studied by differential scanning calorimetry. Polar Biol 12:693–699

    CrossRef  Google Scholar 

  • Westh P, Kristiansen J, Hvidt A (1991) Ice-nucleating activity in the freeze-tolerant tardigrade Adorybiotus coronifer. Comp Biochem Physiol A Mol Physiol 99:401–404

    CrossRef  Google Scholar 

  • Wharton DA (2003) The environmental physiology of Antarctic terrestrial nematodes: a review. J Comp Physiol B 173:621–628

    CAS  CrossRef  Google Scholar 

  • Wharton DA, Goodall G, Marshall CJ (2003) Freezing survival and cryoprotective dehydration as cold tolerance mechanisms in the antarctic nematode Panagrolaimus davidi. J Exp Biol 206:215–221

    CrossRef  Google Scholar 

  • Wharton DA, Downes MF, Goodall G, Marshall CJ (2005) Freezing and cryoprotective dehydration in an antarctic nematode (Panagrolaimus davidi) visualised using a freeze substitution technique. Cryobiology 50:21–28

    CAS  CrossRef  Google Scholar 

  • Wilson PW, Heneghan AF, Haymet ADJ (2003) Ice nucleation in nature: supercooling point (SCP) measurements and the role of heterogeneous nucleation. Cryobiology 46:88–98

    CAS  CrossRef  Google Scholar 

  • Worland MR, Block W (2003) Desiccation stress at sub-zero temperatures in polar terrestrial arthropods. J Insect Physiol 49:193–203

    CAS  CrossRef  Google Scholar 

  • Worland MR, Convey P (2008) The significance of the moult cycle to cold tolerance in the Antarctic collembolan Cryptopygus antarcticus. J Insect Physiol 54:1281–1285

    CAS  CrossRef  Google Scholar 

  • Worland MR, Grubor-Lajsic G, Montiel PO (1998) Partial desiccation induced by sub-zero temperatures as a component of the survival strategy of the Arctic collembolan Onychiurus arcticus (Tullberg). J Insect Physiol 44:211–219

    CAS  CrossRef  Google Scholar 

  • Worland MR, Leinaas HP, Chown SL (2006) Supercooling point frequency distributions in Collembola are affected by moulting. Funct Ecol 20:323–329

    CrossRef  Google Scholar 

  • Wright JC (2001) Cryptobiosis 300 years on from van Leuwenhoek: what have we learned about tardigrades? Zool Anz 240:563–582

    CrossRef  Google Scholar 

  • Yoder JA, Benoit JB, Denlinger DL, Rivers DB (2006) Stress-induced accumulation of glycerol in the flesh fly, Sarcophaga bullata: evidence indicating anti-desiccant and cryoprotectant functions of this polyol and a role for the brain in coordinating the response. J Insect Physiol 52:202–214

    CAS  CrossRef  Google Scholar 

  • Zachariassen KE (1985) Physiology of cold tolerance in insects. Physiol Rev 65:799–832

    CAS  CrossRef  Google Scholar 

  • Zachariassen KE (1991) The water relations of overwintering insects. In: Lee RE, Denlinger DL (eds) Insects at low temperature. Chapman and Hall, London, pp 47–63

    CrossRef  Google Scholar 

  • Zachariassen KE, Kristiansen E, Pedersen SA, Hammel HT (2004) Ice nucleation in solutions and freeze-avoiding insects - homogeneous or heterogeneous? Cryobiology 48:309–321

    CrossRef  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Steffen Hengherr .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and Permissions

Copyright information

© 2018 Springer Nature Switzerland AG

About this chapter

Verify currency and authenticity via CrossMark

Cite this chapter

Hengherr, S., Schill, R.O. (2018). Environmental Adaptations: Cryobiosis. In: Schill, R. (eds) Water Bears: The Biology of Tardigrades. Zoological Monographs, vol 2. Springer, Cham. https://doi.org/10.1007/978-3-319-95702-9_11

Download citation