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Review

The role of water, ice nucleators, and inoculation in insect cold survival

Pages 21-30 | Published online: 13 Aug 2015

References

  • Lee RE Jr. Insect cold-hardiness: to freeze or not to freeze. BioSci. 1989;39(5):308–313.
  • Block W. To freeze or not to freeze? Invertebrate survival of sub-zero temperatures. Funct Ecol. 1991;5(2):284–290.
  • Hawes TC, Bale JS. Plasticity in arthropod cryotypes. J Exp Biol. 2007;210(15):2585–2592.
  • Zachariassen EK. Physiology of cold tolerance in insects. Physiol Rev. 1985;65(4):799–832.
  • Wilson PW, Heneghan AF, Haymet ADJ. Ice nucleation in nature: supercooling point (SCP) measurements and the role of heterogeneous nucleation. Cryobiology. 2003;46(1):88–98.
  • Danks HV. Dehydration in dormant insects. J Insect Physiol. 2000;46(6):837–852.
  • Ramløv H. Aspects of natural cold tolerance in ectothermic animals. Hum Reprod. 2000;15(5):26–46.
  • Holmstrup M, Westh P. Dehydration of earthworm cocoons exposed to cold: a novel cold hardiness mechanism. J Comp Physiol B. 1994;164(4):312–315.
  • Holmstrup M, Sømme L. Dehydration and cold hardiness in the Antarctic collembolan Onychiurus arcticus Tullberg 1876. J Comp Physiol B. 1998;168:197–203.
  • Holmstrup M, Bayley M, Ramløv H. Supercool or dehydrate? An experimental analysis of overwintering strategies in small permeable arctic invertebrates. Proc Natl Acad Sci U S A. 2002;99(8):5716–5720.
  • Elnitsky MA, Hayward SAL, Rinehart JP, Denlinger DL, Lee RE Jr. Cryoprotective dehydration and the resistance to inoculative freezing in the Antarctic midge, Belgica antarctica. J Exp Biol. 2008;211(4):524–530.
  • Sørensen JG, Holmstrup M. Cryoprotective dehydration is widespread in Arctic springtails. J Insect Physiol. 2011;57(8):1147–1153.
  • Watanabe M. Anhydrobiosis in invertebrates. Appl Entomol Zool. 2006;41(1):15–31.
  • Watanabe M, Kikawada T, Minagawa N, Yukuhiro F, Okuda T. Mechanism allowing an insect to survive complete dehydration and extreme temperatures. J Exp Biol. 2002;205(18):2799–2802.
  • Crowe JH, Oliver AE, Tablin F. Is there a single biochemical adaptation to anhydrobiosis? Integr Comp Biol. 2002;42(3):497–503.
  • Wasylyk JM, Tice AR, Baust JG. Partial glass formation: a novel mechanism of insect cryoprotection. Cryobiology. 1988;25(5):451–458.
  • Storey JM, Storey KB.. Cold hardiness and freeze tolerance. In: Storey KB, editor. Functional Metabolism: Regulation and Adaptation. Hoboken: John Wiley and Sons Inc.; 2005:473–504.
  • Lundheim R. Physiological and ecological significance of biological ice nucleators. Philos Trans R Soc Lond B Biol Sci. 2002;357(1423):937–943.
  • Layne JR Jr, Lee RE Jr, Huang JL. Inoculation triggers freezing at high subzero temperatures in a freeze-tolerant frog (Rana sylvatica) and insect (Eurosta solidaginis). Can J Zool. 1990;68(3):506–510.
  • Kawarasaki Y, Teets NM, Denlinger DL, Lee RE Jr. Wet hibernacula promote inoculative freezing and limit the potential for cryoprotective dehydration in the Antarctic midge, Belgica antarctica. Polar Biol. 2014;37(6):753–761.
  • Shimada K, Riihamaa A. Cold acclimation, inoculative freezing and slow cooling: essential factors contributing to the freezing tolerance in diapausing larvae of Chymomyza costata (Diptea: Drosophilidae). CryoLetters. 1988;9:5–10.
  • Constanzo JP, Bayuk JM, Lee RE Jr. Inoculative freezing by environmental ice nuclei in the freeze-tolerant wood frog, Rana sylvatica. J Exp Zool. 1999;284(1):7–14.
  • Baker PJ, Costanzo JP, Herlands R, Wood RC, Lee RE Jr. Inoculative freezing promotes winter survival in hatchling diamondback terrapin, Malaclemys terrapin. Can J Zool. 2006;84(1):116–124.
  • Franks F. Unfrozen water: yes; unfreezable water: hardly; bound water: certainly not. An editorial note. Cryoletters. 1986;7:207.
  • Wiggins PM. Role of water in some biological processes. Microbiol Rev. 1990;54(4):432–449.
  • Wolfe J, Bryant G, Koster KL. What is “unfreezable water”, how unfreezable it is and how much is there? Cryoletters. 2002;23(3):157–166.
  • Disalvo EA, Lairion F, Martini F, et al. Structural and functional properties of hydration and confined water in membrane interfaces. BBA Biomembranes. 2008;1778(12):2655–2670.
  • Ball P. Water as an active constituent in cell biology. Chem Rev. 2008;108(1):74–108.
  • Hong MK, Erramilli S. A dynamic role for water in biological systems. J Biol Phys. 2012;38(1):1–2.
  • Brovchenko I, Oleinikova A. Which properties of spanning network of hydration water enable biological functions? ChemPhysChem. 2008;9(18):2695–2702.
  • Block W. Water or ice? – the challenge for invertebrate cold survival. Sci Prog. 2003;86(1–2):77–101.
  • Prestrelski SJ, Tedeschi N, Arakawa T, Carpenter JF. Dehydration-induced conformational transitions in proteins and their inhibition by stabilizers. Biophys J. 1993;65(2):661–671.
  • Hoaglund-Hyzer CS, Counterman AE, Clemme DE. Anhydrous protein ions. Chem Rev. 1999;99(10):3037–3079.
  • Jarrold MF. Peptides and proteins in vapor phase. Annu Rev Phys Chem. 2000;51:179–207.
  • Klibanov AM. Improving enzymes by using them in organic solvents. Nature. 2001;409(6817):241–246.
  • Dolman M, Halling PJ, Moore BD, Waldron S. How dry are anhydrous enzymes? Measurement of residual and buried 18O-labeled water molecules using mass spectrometry. Biopolymers. 1997;41(3):313–321.
  • Kirk GL, Gruner SM, Stein DL. A thermodynamic model of the lamellar to inverse hexagonal phase transition of lipid membrane-water systems. Biochemistry. 1984;23(6):1093–1102.
  • Irwin JT, Lee RE Jr. Energy and water conservation in frozen vs supercooled larvae of the goldenrod gall fly, Eurosta solidaginis (Fitch) (Diptera: Tephritidae). J Exp Zool. 2002;292(4):345–350.
  • Storey KB, Storey JM. Freeze tolerance in animals. Physiol Rev. 1988;68(1):27–84.
  • Voituron Y, Mouquet N, de Mazancourt C, Clobert J. To freeze of not to freeze? An evolutionary perspective on the cold-hardiness strategies of overwintering ectotherms. Am Nat. 2002;160(2):255–270.
  • Elbein AD, Pan YT, Pastuszak I, Carroll D. New insights on trehalose: a multifunctional molecule. Glycobiology. 2003;13(4):17R–27R.
  • Scott P. Resurrection plants and the secrets of eternal leaf. Ann Bot. 2000;85(2):159–166.
  • Clegg JS, Seitz P, Seitz W, Hazlewood CF. Cellular responses to extreme water loss: the water-replacement hypothesis. Cryobiology. 1982;19(3):306–316.
  • Crowe LM, Crowe JH, Rudolph A, Womersley C, Appel L. Preservation of freeze-dried liposomes by trehalose. Arch Biochem Biophys. 1985;242(1):240–247.
  • Jain NK, Roy I. Effect of trehalose on protein structure. Protein Sci. 2009;18(1):24–36.
  • Crowe JH, Crowe LM, Chapman D. Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science. 1984;223(4637):701–703.
  • Grasmeijer N, Stankovic M, de Waard H, Frijlink HW, Hinrichs WLJ. Unraveling protein stabilization mechanisms: vitrification and water replacement in a glass transition temperature controlled system. Biochim Biophys Acta. 2013;1834(4):763–769.
  • Sakurai M, Furuki T, Akao K, et al. Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplanki. Proc Natl Acad Sci U S A. 2008;105(13):5093–5098.
  • Hare PD, Cress WA. Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul. 1997;21(2):79–102.
  • Morgan TD, Chippendale GM. Free amino acids of the hemolymph of the southwestern corn borer and the European corn borer in relation to their diapause. J Insect Physiol. 1983;29(10):735–740.
  • Fields PG, Fleurat-Lessard F, Lavenseau L, Febvay G, Peypelut L, Bonnot G. The effect of cold acclimation and deacclimation on cold tolerance, trehalose and free amino acid levels in Sitophilus granaries and Cryptolestes ferrugineus (Coleoptera). J Insect Physiol. 1998;44(10):955–965.
  • Timasheff SN. Protein-solvent preferential interactions, protein hydration, and the modulation of biochemical reactions by solvent components. Proc Natl Acad Sci U S A. 2002;99(15):9721–9726.
  • Shimizu S, Smith DJ. Preferential hydration and the exclusion of cosolvents from protein surfaces. J Chem Phys. 2004;121(2):1148–1154.
  • Gadd GM, Chalmers K, Reed RH. The role of trehalose in dehydration resistance of Sacharomyces cerevisiae. FEMS Microbiol Lett. 1987;48(1–2):249–254.
  • Zayed G, Roos YH. Influence of trehalose and moisture content on survival of Lactobacilus salivarius subjected to freezedrying and storage. Process Biochem. 2004;39(9):1081–1086.
  • Rothschild LJ, Mancinelli RL. Life in extreme environments. Nature. 2001;409(6823):1092–1101.
  • Jaenicke R, Böhm G. The stability of proteins in extreme environments. Cur Opin Struct Biol. 1998;8(6):738–748.
  • Konings WN, Albers SV, Koning S, Driessen AJM. The cell membrane plays a crucial role in survival of bacteria and archaea in extreme environments. Antonie van Leeuwenhoek. 2002;81(1–4):61–72.
  • Clegg JS. Cryptobiosis – a peculiar state of biological organization. Comp Biochem Physiol B Biochem Mol Biol. 2001;128(4):613–624.
  • Matsumoto M, Saito S, Ohmine I. Molecular dynamics simulation of the ice nucleation and growth process leading to water freezing. Nature. 2002;416(6879):409–413.
  • Lee RE Jr, Constanzo JP. Biological ice nucleation and ice distribution in cold-hardy ectothermic animals. Annu Rev Physiol. 1998;60:55–72.
  • Lee RE Jr. Principles of insect low temperature tolerance. In: Lee RE Jr, Denlinger DL, editors. Insects at Low Temperature. New York: Chapman and Hall; 1991:17–46.
  • Clausse D, Bouabdillah D, Cochet N, Luquet MP, Pulvin S. Ice crystallization induced by silver iodide and bacteria in microsize droplets dispersed within emulsions. Pure Appl Chem. 1991;63(10):1491–1494.
  • Duman JG, Morris JP, Castellino FJ. Purification and composition of an ice nucleating protein from queens of the hornet, Vespula maculata. J Comp Physiol B. 1984;154(1):79–83.
  • Neven LG, Duman JG, Low MG, Sehl LC, Castellino FJ. Purification and characterization of an insect hemolymph lipoprotein ice nucleator: evidence for the importance of phosphatidylinositol and apolipoprotein in the ice nucleator activity. J Comp Physiol B. 1989;159(1):71–82.
  • Gurian-Sherman D, Lindow SE. Bacterial ice nucleation: significance and molecular basis. FASEB J. 1993;7(14):1338–1343.
  • Bale JS. Insect cold hardiness: a matter of life and death. Eur J Entomol. 1996;93(3):369–382.
  • Warren G, Corotto L, Wolber P. Conserved repeats in diverged ice nucleation structural genes from two species of Pseudomonas. Nucleic Acids Res. 1986;14(20):8047–8060.
  • Kajava AV, Lindow SE. A model of the three-dimensional structure of ice nucleation proteins. J Mol Biol. 1993;232(3):709–717.
  • Sømme L. The physiology of cold hardiness in terrestrial arthropods. Eur J Entomol. 1999;96(1):1–10
  • Zachariassen KE, Kristiansen E, Pedersen SA, Hammel HT. Ice nucleation in solutions and freeze-avoiding insects – homogeneous or heterogeneous? Cryobiology. 2004;48(3):309–321.
  • Cantrell W, Heymsfield A. Production of ice in tropospheric clouds: a review. Bull Amer Meteor Soc. 2005;86(6):795–807.
  • Murray BJ, O’Sullivan D, Atkinson JD, Webb ME. Ice nucleation by particles immersed in supercooled cloud droplets. Chem Soc Rev. 2012;41(19):6519–6554.
  • Zimmermann F, Weinbruch S, Schütz L, et al. Ice nucleation properties of the most abundant mineral dust phases. J Geophys Res. 2008;113:D23204.
  • Fornea AP, Brooks SD, Dooley JB, Saha A. Heterogeneous freezing of ice on atmospheric aerosols containing ash, soot, and soil. J Geophys Res. 2009;114:D13201.
  • Marcolli C, Gedamke S, Peter T, Zobrist B. Efficiency of immersion mode ice nucleation on surrogates of mineral dust. Atmos Chem Phys. 2007;7:5081–5091.
  • Mugnano JA, Lee RE Jr, Taylor RT. Fat body cells and calcium phosphate spherules induce ice nucleation in the freeze-tolerant larvae of the gall fly Eurosta solidaginis (Diptera, Tephritidae). J Exp Biol. 1996;199(2):465–471.
  • Lee RE Jr, Strong-Gunderson JM, Lee MR, Grove KS, Riga TJ. Isolation of ice nucleating active bacteria from insects. J Exp Zool. 1991;257(1):124–127.
  • Worland MR, Block W. Ice-Nucleating bacteria from the guts of two Sub-Antarctic beetles, Hydromedion sparsutum and Perimylops antarcticus (Perimylopidae). Cryobiology. 1999;38(1):60–67.
  • Dillon RJ, Dillon VM. The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol. 2004;49:71–92.
  • Sømme L, Block W. Cold hardiness of Collembola at Signy Island, maritime Antarctic. Oikos. 1982;38(2):168–176.
  • Worland MR, Leinaas HP, Chown SL. Supercooling point frequency distributions in Collembola are affected by moulting. Funct Ecol. 2006;20(2):323–329.
  • Hiiesaar K, Williams I, Luik A, et al. Factors affecting cold hardiness in the small striped flea beetle, Phyllotreta undulata. Entomol Exp Appl. 2009;131(3):278–285.
  • Duman JG. Antifreeze and ice nucleator proteins in terrestrial arthropods. Annu Rev Physiol. 2001;63:327–357.
  • Barrett J. Thermal hysteresis proteins. Int J Biochem Cell Biol. 2001;33(2):105–117.
  • Clark MS, Worland MR. How insects survive the cold: molecular mechanisms – a review. J Comp Physiol B. 2008;178(8):917–933.
  • Davies PL, Baardsnes J, Kuiper MJ, Walker VK. Structure and function of antifreeze proteins. Phil Trans R Soc Lond B. 2002;357(1423):927–935.
  • Tursman D, Duman JD, Knight CA. Freeze tolerance adaptations in the centipede, Lithobius forficatus. J Exp Zool. 1994;268(5):347–353.
  • Gehrken U, Southon TE. Supercooling in a freeze-tolerant larva, Tipula sp. J Insect Physiol. 1992;38(2):131–137.
  • Layne JR Jr, Edgar CL, Medwith RE. Cold hardiness of the Wooly Bear caterpillar (Pyrrharctica isabella Lepidoptera: Arctiidae). Am Midl Nat. 1999;141(2):293–304.
  • Olsen TM, Sass SJ, Li N, Duman JG. Factors contributing to seasonal increases in inoculative freezing resistance in overwintering fire-colored beetle larvae Dendroides canadensis (Pyrochroidae). J Exp Biol. 1998;201(10):1585–1594.
  • Gehrken U. Inoculative freezing and thermal hysteresis in the adult beetles Ips acuminatus and Rhagium inquisitor. J Insect Physiol. 1992;38(7):519–524.
  • Danks HV. The roles of insect cocoons in cold conditions. Eur J Entomol. 2004;101(3):433–437.
  • Fields PG, McNeil JN. Possible dual cold-hardiness strategies in Cisseps fulvicollis Lepidoptera Arctiidae. Can Ent. 1986;118(12):1309–1311.
  • Gehrken U, Strømme A, Lundheim R, Zachariassen KE. Inoculative freezing in overwintering tenebrionid beetle, Bolitophagus reticulatus Panz. J Insect Physiol. 1991;37(9):683–687.
  • Koštál V, Havelka J. Diapausing larvae of the midge Aphidoletes aphidimyza (Diptera: Cecidomyiidae) survive at subzero temperatures in a supercooled state but tolerate freezing if inoculated by external ice. Eur J Entomol. 2000;97(3):433–436.
  • Rozsypal J, Koštál V, Zahradnícková H, Šimek P. Overwintering strategy and mechanisms of cold tolerance in the codling moth (Cydia pomonella). PLoS ONE. 2013;8(4):e61745.
  • Enomoto O. Larval diapause in Chymomyza costata (Diptera: Drosophilidae) II. Frost avoidance. Low Temp Sci B. 1981;39:31–39.
  • Moon I, Fujikawa S, Shimada K. Cryopreservation of Chymomyza larvae (Diptera: Drosophilidae) at −196°C with extracellular freezing. CryoLetters. 1996;17:105–110.
  • Shimada K, Riihamaa A. Cold-induced freezing tolerance in diapausing and non-diapausing larvae of Chymomyza costata (Diptera: Drosophilidae) with accumulation of trehalose and proline. CryoLetters. 1990;11:243–250.
  • Koštál V, Zahradníčková H, Šimek P. Hyperprolinemic larvae of the drosophilid fly, Chymomyza costata, survive cryopreservation in liquid nitrogen. Proc Natl Acad Sci U S A. 2011;108(32):13041–13046.
  • Koštál V, Šimek P, Zahradníčková H, Cimlová J, Štětina T. Conversion of the chill susceptible fruit fly larva (Drosophila melanogaster) to a freeze tolerant organism. Proc Natl Acad Sci U S A. 2012;109(9):3270–3274.