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A thermal hysteresis-producing xylomannan glycolipid antifreeze associated with cold tolerance is found in diverse taxa

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Abstract

The presence of large-molecular-mass, thermal hysteresis (TH)-producing antifreezes (e.g., antifreeze proteins) has been reported in numerous and diverse taxa, including representative species of fish, arthropods, plants, fungi, and bacteria. However, relatively few of these antifreeze molecules have been chemically characterized. We screened diverse species by subjecting their homogenates to ice-affinity purification and discovered the presence of a newly identified class of antifreeze, a xylomannan-based TH-producing glycolipid that was previously reported in one species of freeze-tolerant Alaskan beetle. We isolated xylomannan-based antifreeze glycolipids from one plant species, six insect species, and the first frog species to be shown to produce a large-molecular-mass antifreeze. 1H NMR spectra of the ice-purified molecules isolated from these diverse freeze-tolerant and freeze-avoiding organisms were nearly identical, indicating that the chemical structures of the glycolipids were highly similar. Although the exact functions remain uncertain, it appears that antifreeze glycolipids play a role in cold tolerance.

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Abbreviations

TH:

Thermal hysteresis

AF(G)Ps:

Antifreeze (glyco)proteins

AFGLs:

Antifreeze glycolipids

References

  • Alberts B, Bray D, Hopkin K, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2004) Essential cell biology: an introduction to the molecular biology of the cell. Taylor & Francis, New York

    Google Scholar 

  • Bennett VA, Sformo T, Walters K, Toien O, Jeannet K, Hochstrasser R, Pan Q, Serianni AS, Barnes BM, Duman JG (2005) Comparative overwintering physiology of Alaska and Indiana populations of the beetle Cucujus clavipes (Fabricius): roles of antifreeze proteins, polyols, dehydration and diapause. J Exp Biol 208:4467–4477

    Article  PubMed  CAS  Google Scholar 

  • Block W (1990) Cold tolerance of insects and other arthropods. Phil Trans R Soc Lond B 326:613–633

    Article  Google Scholar 

  • Brown CL, Bale JS, Walters KFA (2004) Freezing induces a loss of freeze tolerance in an overwintering insect. Proc R Soc Lond B 271:1507–1511

    Article  CAS  Google Scholar 

  • Curatolo W (1987) Glycolipid function. Biochim Biophys Acta 906:137–160

    PubMed  CAS  Google Scholar 

  • Denlinger DL, Lee RE (2010) Low temperature biology of insects. Cambridge University Press, New York

    Book  Google Scholar 

  • DeVries AL (1971) Glycoproteins as biological antifreeze agents in antarctic fishes. Science 172:1152–1155

    Article  PubMed  CAS  Google Scholar 

  • DeVries AL (1988) The role of antifreeze glycopeptides and peptides in the freezing avoidance of Antarctic fishes. Comp Biochem and Physiol B 90:611–621

    Article  Google Scholar 

  • DeVries AL (2004) Ice, antifreeze proteins, and antifreeze genes in polar fishes. In: Barnes BM, Carey HV (eds) Life in the cold: evolution, mechanisms, adaptation and application. University of Alaska Press, Fairbanks, pp 307–328

    Google Scholar 

  • DeVries AL, Cheng CHC (2005) Antifreeze proteins and organismal freezing avoidance in polar fishes. Fish Physiol 22:155–201

    Article  Google Scholar 

  • Duman JG (1984) Change in overwintering mechanism of the Cucujid beetle, Cucujus clavipes. J Insect Physiol 30:235–239

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Duman JG, Olsen TM (1993) Thermal hysteresis protein activity in bacteria, fungi, and phylogenetically diverse plants. Cryobiology 30:322–328

    Article  Google Scholar 

  • Duman JG, Bennett V, Sformo T, Hochstrasser R, Barnes BM (2004) Antifreeze proteins in Alaskan insects and spiders. J Insect Physiol 50:259–266

    Article  PubMed  CAS  Google Scholar 

  • Duman JG, Walters KR, Sformo T, Carrasco MA, Nickell PK, Lin X, Barnes BM (2010) Antifreeze and ice-nucleator proteins. In: Denlinger DL, Lee RE (eds) Low temperature biology of insects. Cambridge University Press, New York, pp 59–90

  • Graether SP, Sykes BD (2004) Cold survival of freeze intolerant insects: the structure and function of beta-helical antifreeze proteins. Eur J Biochem 271:3285–3296

    Article  PubMed  CAS  Google Scholar 

  • Graether SP, Kuiper MJ, Gagne SM, Walker VK, Jia Z, Sykes BD, Davies PL (2000) Beta-helix structure of a hyperactive antifreeze protein from an insect. Nature 406:325–328

    Article  PubMed  CAS  Google Scholar 

  • Griffith M, Yaish MW (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9:399–405

    Article  PubMed  CAS  Google Scholar 

  • Hays LM, Feeney RE, Crowe LM, Crowe JH, Oliver AE (1996) Antifreeze glycoproteins inhibit leakage from liposomes during thermotropic phase transitions. Proc Natl Acad Sci USA 93:6835–6840

    Article  PubMed  CAS  Google Scholar 

  • Horwath KL, Duman JG (1984) Yearly variations in the overwintering mechanisms of the cold-hardy beetle Dendroides canadensis. Physiol Zool 57:40–45

    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

    Article  CAS  Google Scholar 

  • Knight CA, Wen D, Laursen RA (1995) Nonequilibrium antifreeze peptides and the recrystallization of ice. Cryobiology 32:23–34

    Article  PubMed  CAS  Google Scholar 

  • Kuiper MJ, Lankin C, Gauthier SY, Walker VK, Davies PL (2003) Purification of antifreeze proteins by adsorption to ice. Biochem Biophys Res Commun 300:645–648

    Article  PubMed  CAS  Google Scholar 

  • Neven LG, Duman JG, Beals JM, Castellino FJ (1986) Overwintering adaptations of the stag beetle, Ceruchus piceus: removal of ice nucleators in winter to promote supercooling. J Comp Physiol B 156:707–716

    Article  CAS  Google Scholar 

  • Olsen TM, Duman JG (1996) Maintenance of the supercooled state in overwintering pyrochroid beetle larvae, Dendroides canadensis: role of hemolymph ice nucleators and antifreeze proteins. J Comp Physiol B 167:105–113

    Article  Google Scholar 

  • Olsen T, Sass S, Li N, Duman J (1998) Factors contributing to seasonal increases in inoculative freezing resistance in overwintering fire-colored beetle larvae Dendroides canadensis. J Exp Biol 20:1585–1594

    Google Scholar 

  • Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151:341–353

    Article  CAS  Google Scholar 

  • Rubinsky B, Arav A, Mattioli M, DeVries AL (1990) The effect of antifreeze glycopeptides on membrane potential changes at hypothermic temperatures. Biochem Biophys Res Commun 173:1369–1374

    Article  PubMed  CAS  Google Scholar 

  • Sformo T, Kohl F, McIntyre J, Kerr P, Duman JG, Barnes BM (2009) Simultaneous freeze tolerance and avoidance in individual fungus gnats, Exechia nugatoria. J Comp Physiol B 179:897–902

    Article  PubMed  Google Scholar 

  • Sformo T, Walters KR, Jeannet K, Wowk B, Fahy G, Barnes BM, Duman JG (2010) Deep supercooling, vitrification, and limited survival to −100°C in the Alaskan beetle larvae Cucujus clavipes puniceus (Coleoptera:Cucujuidae). J Exp Biol 213:502–509

    Article  PubMed  CAS  Google Scholar 

  • Steponkus PL, Lynch DV, Uemura M (1990) Influence of cold acclimation on the lipid composition and cryobehaviour of the plasma membrane of isolated rye protoplasts. Phil Trans R Soc Lond B 326:571–583

    Article  CAS  Google Scholar 

  • Storey KB (1990) Life in a frozen state: adaptive strategies for natural freeze tolerance in amphibians and reptiles. Am J Physiol Regul Integr Comp Physiol 258:R559–R568

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  PubMed  CAS  Google Scholar 

  • Tomčala A, Tollarová M, Overgaard J, Šimek P, Koštál V (2006) Seasonal acquisition of chill-tolerance and restructuring of membrane glycerophospholipids in an overwintering insect: triggering by low temperature, desiccation and diapauses progression. J Exp Biol 209:4102–4114

    Article  PubMed  Google Scholar 

  • Tomczak MM, Crowe JH (2002) The interaction of antifreeze proteins with model membranes and cells. In: Ewart K, Hew C (eds) Fish antifreeze proteins. World Scientific, New Jersey, pp 187–212

    Chapter  Google Scholar 

  • Tursman D, Duman JG (1995) Cryoprotective effects of thermal hysteresis protein on survivorship of frozen gut cells from the freeze-tolerant centipede Lithobius forficatus. J Exp Zool 272:249–257

    Article  CAS  Google Scholar 

  • Tursman D, Duman JG, Knight CA (1994) Freeze tolerance adaptations in the centipede, Lithobius forficatus. J Exp Zool 268:347–353

    Article  Google Scholar 

  • Voituron Y, Joly P, Eugène M, Barré H (2005) Freezing tolerance of the European water frogs: the good, the bad, and the ugly. Am J Physiol Regul Integr Comp Physiol 288:R1563–R1570

    Article  PubMed  CAS  Google Scholar 

  • Walters KR, Sformo T, Barnes BM, Duman JG (2009a) Freeze tolerance in the Arctic Alaska stonefly, Nemoura arctica. J Exp Biol 212:305–312

    Article  PubMed  Google Scholar 

  • Walters KR, Serianni AS, Sformo T, Barnes BM, Duman JG (2009b) A non-protein thermal hysteresis-producing xylomannan antifreeze in the freeze-tolerant Alaskan beetle, Upis ceramboides. Proc Natl Acad Sci USA 106:210–215

    Article  Google Scholar 

  • Wilson SL, Kelley DL, Walker VK (2006) Ice-active characteristics of soil bacteria selected by ice-affinity. Environ Microbiol 8:1816–1824

    Article  PubMed  CAS  Google Scholar 

  • Zacchariassen KE, Kristiansen E (2000) Ice nucleation and antinucleation in nature. Cryobiology 41:257–259

    Article  Google Scholar 

  • Zachariassen KE, Hammel HT (1976) Nucleating agents in the haemolymph of insects tolerant to freezing. Nature 262:285–287

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by National Science Foundation grants OPP-0117104 and IOS-0618342 to JD and BB.

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Correspondence to Kent R. Walters Jr..

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Communicated by H.V. Carey.

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Walters, K.R., Serianni, A.S., Voituron, Y. et al. A thermal hysteresis-producing xylomannan glycolipid antifreeze associated with cold tolerance is found in diverse taxa. J Comp Physiol B 181, 631–640 (2011). https://doi.org/10.1007/s00360-011-0552-8

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  • DOI: https://doi.org/10.1007/s00360-011-0552-8

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