Skip to main content
SpringerLink
Log in

Antifreeze Proteins in Other Species

  • Chapter
  • First Online:
Antifreeze Proteins Volume 1

  • 733 Accesses

Abstract

Ice-binding proteins (IBPs) are now recognized to include three types of proteins. (1) Antifreeze proteins (AFPs), first discovered in Antarctic fish, protect freeze-avoiding organisms from lethal ice formation of their body fluids by lowering the freezing point of aqueous solutions by a non-colligative mechanism—binding to ice crystals and preventing their growth. This results in a difference between the freezing and melting points termed thermal hysteresis (TH). AFPs prevent inoculative freezing across the body surface by exterior ice and they also promote supercooling by inhibiting potential ice nucleation surfaces. (2) Recrystallization inhibition proteins (RIPs) function primarily to inhibit recrystallization of ice in freeze-tolerant organisms (those able to freeze and survive) although they also generally produce minor TH. Note that true While AFPs inhibit recrystallization of ice, the primary function of recrystallization inhibition proteins (RIPs), although they also produce minor TH, is to inhibit recrystallization in freeze-tolerant organisms (those able to freeze and survive). (3) Adaptive ice-nucleating proteins (INPs) function in freeze-tolerant species to inhibit supercooling and promote freezing at a high subzero temperature where the resulting freezing is more easily controlled. Although INPs are best known in bacteria, AFPs and RIPs traditionally have been most studied in fish, insects, and plants. However, these proteins are also present in numerous other organisms. These “other” TH-producing organisms are the focus of this chapter. They include many types of animals such as noninsect arthropods (spiders, mites, ticks, centipedes, a crustacean, and snow fleas), mollusks, ribbon worms, fish leeches, sponges, nematodes, frogs, perhaps even mammals and birds; several fungi and numerous bacteria, and archaea. Antifreeze glycolipids will also be discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 179.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abraham NM, Liu L, Jutras BL, Yadav AK, Narasimhan S, Gopalakrishnan V, Ansari JM, Jefferson KK, Cava F, Jacobs-Wagner C, Fikrig E (2017) Pathogen-mediated manipulation of arthropod microbiota to promote infection. Proc Natl Acad Sci USA 114:E781–E790

    CAS  PubMed  PubMed Central  Google Scholar 

  • Adhikari BN, Wall DH, Adams BJ (2009) Desiccation survival in an Antarctic nematode: molecular analysis using expressed sequence tags. BMC Genomics 10:69–85

    PubMed  PubMed Central  Google Scholar 

  • Ali F, Wharton DA (2016) Ice-active substances from the infective juveniles of the freeze tolerant entomopathogenic nematode, Steinernema feltiae. PLoS One 11(5):e0156502. https://doi.org/10.1371/journal.pone.0156502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anthony SE, Sinclair BJ (2019) Overwintering red velvet mites are freeze tolerant. Physiol Biochem Zool 92:201–205

    PubMed  Google Scholar 

  • Arrigo KR, Thomas DN (2004) Large scale importance of sea ice biology in the Southern Ocean. Antarct Sci 16:471–486

    Google Scholar 

  • Ashworth EN, Kieth TL (1995) Ice nucleation activity associated with plants and fungi. In: Lee RE, Warren GJ, Gusta LV (eds) Biological ice nucleation and its applications. American Phytological Society Press, St Paul, MN, pp 137–162

    Google Scholar 

  • Banerjee R, Chakraborti P, Bhowmick R, Mukhopadhyay S (2015) Distinct molecular features facilitating ice-binding mechanisms in hyperactive antifreeze proteins closely related to an Antarctic sea ice bacterium. J Biomol Struct Dyn 33:1424–4141

    CAS  PubMed  Google Scholar 

  • Bayer-Giraldi M, Weikusat I, Besir H, Dieckmann G (2011) Characterization of an antifreeze protein from the polar diatom Fragilariopsis cylindrus and its relevance in sea ice. Cryobiology 63(3):210–219

    CAS  PubMed  Google Scholar 

  • Biggar KK, Kolani E, Furusawa T, Storey KB (2013) Expression of freeze-responsive proteins, Fr10 and Li16, from freeze-tolerant frogs enhances freezing survival of BmN insect cells. FASEB J 27:3376–3383

    CAS  PubMed  Google Scholar 

  • Block W (1977) Oxygen consumption of the terrestrial mite Alaskozetes antarcticus (Acari: Cryptostigmata). J Exp Biol 68:69–87

    Google Scholar 

  • Block W (1980) Survival strategies in polar terrestrial arthropods. Biol J Linn Soc 14:29–38

    Google Scholar 

  • Block W (1982) Supercooling points of insects and mites on the Antarctic Peninsula. Ecol Entomol 7:1–8

    Google Scholar 

  • Block W, Duman JG (1989) Presence of thermal hysteresis producing antifreeze proteins in the Antarctic mite, Alaskozetes antarcticus. J Exptl Zool 250:229–231

    CAS  Google Scholar 

  • Block W, Zettel J (1980) Cold hardiness of some alpine Collembola. Ecol Entomol 5:1–9

    Google Scholar 

  • Bryon A, Wybouw N, Dermauw W, Tirry L, Thomas Van Leeuwen T (2013) Genome wide gene-expression analysis of facultative reproductive diapause in the two-spotted spider mite Tetranychus urticae. BMC Genomics 14:815–835

    PubMed  PubMed Central  Google Scholar 

  • Bryon A, Kurlovs AH, Van Leeuwen T, Clark RM (2017) A molecular-genetic understanding of diapause in spider mites: current knowledge and future directions. Physiol Entomol 42(3):211–224

    Google Scholar 

  • Buzzini P, Margesin M (2014) Cold-adapted yeasts: biodiversity, adaptation strategies and biotechnological significance. Heidelberg, Springer, Germany, p 549

    Google Scholar 

  • Cannon RJC, Block W (1988) Cold tolerance of microarthropods. Biol Rev 63:23–77

    Google Scholar 

  • Cao H, Zhao Y, Zhu YB, Xu F, Yu JS, Yuan M (2016) Antifreeze and cryoprotective activities of ice-binding collagen peptides from pig skin. Food Chem 194:1245–1253

    CAS  PubMed  Google Scholar 

  • Carrasco MA, Duman JG (2011) A cross-species compendium of proteins related to cold stress identified by bioinformatic approaches. J Insect Physiol 57:1127–1135

    CAS  PubMed  Google Scholar 

  • Cavicchioli R (2006) Cold-adapted archaea. Nature Rev Microbiol 4:331–343

    CAS  Google Scholar 

  • Chen L, DeVries AL, Cheng CHC (1997) Convergent evolution of antifreeze glycoproteins in Antarctic fish and Arctic cod. Proc Natl Acad Sci USA 94:3817–3822

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng J, Hanada Y, Miura A, Tsuda S, Kondo H (2016) Hydrophobic ice-binding sites confer hyperactivity of an antifreeze protein from a snow mold fungus. Biochem J 473:4011–4026

    CAS  PubMed  Google Scholar 

  • Costanzo (2019) Overwintering adaptations and extreme freeze tolerance in a subarctic population of the wood frog Rana sylvatica. J Comp Physiol B 189:1–5

    PubMed  Google Scholar 

  • Costanzo JP, Lee RE (2013) Avoidance and tolerance of freezing in ectothermic vertebrates. J Exp Biol 216:1961–1967

    PubMed  Google Scholar 

  • Crawford CS, Riddle WA (1974) Cold hardiness in centipedes and scorpions in New Mexico. Oikos 25(1):86

    Google Scholar 

  • Crawford CS, Riddle WA, Pugach S (1975) Overwintering physiology of the centipede Scolopendra polymorpha. Physiol Zool 48(3):290–294

    Google Scholar 

  • Damodaran S (2007) Inhibition of ice crystal growth in ice cream mix by gelatin hydrolysate. J Agric Food Chem 55:10918–10923

    CAS  PubMed  Google Scholar 

  • Danks HV (1981) Arctic arthropods. Entomological Society of Canada, Ottawa, p 608

    Google Scholar 

  • Danks HV (1991) Winter habitats and ecological adaptations for winter survival. In: Lee RE, Denlinger DL (eds) Insects at low temperature. Chapman & Hall, London, pp 231–259

    Google Scholar 

  • Dantel H, Knulle W (1996) The supercooling ability of ticks (Acari, Ixodoidea). J Comp Physiol B 166:517–524

    Google Scholar 

  • Davies PL (2014) Ice-binding proteins: a remarkable diversity of structures for stopping and starting ice growth. Trends Biochem Sci 39:548–555

    CAS  PubMed  Google Scholar 

  • Dayton PK, Robilliard GA, DeVries AL (1969) Anchor ice formation in McMurdo Sound, Antarctica, and its biological effects. Science 163:273–274

    CAS  PubMed  Google Scholar 

  • Denlinger DL, Lee RE (2010) Low temperature biology of insects. Cambridge University Press, Cambridge, p 390

    Google Scholar 

  • DeVries AL, Wohlschlag DE (1969) Freezing resistance in some Antarctic fishes. Science 163(3871):1073–1075

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • DeVries AL, Cheng C-HC (2005) Antifreeze proteins in polar fishes. In: Farrell AP, Steffensen JF (eds) Fish physiology, vol XXII. Academic Press, San Diego, pp 155–201

    Google Scholar 

  • Do H, Lee JH, Lee SG, Hak Jun Kim HJ (2012a) Crystallization and preliminary X-ray crystallographic analysis of an ice-binding protein (FfIBP) from Flavobacterium frigoris PS1. Acta Crystallogr Sect F Struct Biol Cryst Commun F68:806–809

    Google Scholar 

  • Do H, Lee JH, Lee SG, Hak Jun Kim HJ (2012b) Crystallization and preliminary X-ray crystallographic analysis of an ice-binding protein (FfIBP) from Flavobacterium frigoris PS1. Addendum. Acta Crystallogr Sect F Struct Biol Cryst Commun F68:1418–1420

    Google Scholar 

  • Doucet CJ, Byass L, Elias L, Worrall D, Smallwood M, Bowles DJ (2000) Distribution and characterization of recrystallization inhibitor activity in plant and lichen species from the UK and maritime Antarctic. Cryobiology 40:218–227

    CAS  PubMed  Google Scholar 

  • Du L, Betti M (2016) Identification and evaluation of cryoprotective peptides from chicken collagen: ice-growth inhibition activity compared to that of type I antifreeze proteins in sucrose model systems. J Agric Food Chem 64:5232–5240

    CAS  PubMed  Google Scholar 

  • Duman JG (1979) Subzero temperature tolerance in spiders: the role of thermal hysteresis factors. J Comp Physiol 131:347–352

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Duman JG (2015) Animal ice-binding (antifreeze) proteins and glycolipids: an overview with emphasis on physiological function. J Exp Biol 218:1846–1855

    PubMed  Google Scholar 

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

    Google Scholar 

  • Duman JG, Verleye D, Li N (2002) Site specific forms of antifreeze proteins in the beetle Dendroides canadensis. J Comp Physiol B 172:547–552

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Evans CW, Hellman L, Middleditch M, Wojnar JM, Brimble MA, DeVries AL (2012) Synthesis and recycling of antifreeze glycoproteins in polar fishes. Antarct Sci 24:259–268

    Google Scholar 

  • Garnham CP, Gilbert JA, Hartman CP, Campbell RL, Laybourn-Parry J, Davies PL (2008) A Ca2+-dependent bacterial antifreeze protein domain has a novel beta-helical ice-binding fold. Biochem J 411:171–180

    CAS  PubMed  Google Scholar 

  • Garnham CP, Campbell RL, Davies PL (2011) Anchored clathrate waters bind antifreeze proteins to ice. Proc Natl Acad Sci USA 108:7363–7367

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gilbert JA, Hill PJ, Dodd CER, Laybourn-Parry J (2004) Demonstration of antifreeze protein activity in Antarctic lake bacteria. Microbiol 150:171–180

    CAS  Google Scholar 

  • Gilbert J, Davies P, Laybourn-Parry J (2005) A hyperactive, Ca2+-dependent antifreeze protein in an Antarctic bacterium. FEMS Microbiol Lett 245:67–72

    CAS  PubMed  Google Scholar 

  • Graether SP, Jia Z (2001) Modeling Pseudomonas syringae ice-nucleation protein as a beta-helical protein. Biophys J 80:1169–1173

    CAS  PubMed  PubMed Central  Google Scholar 

  • Graham LA, Davies PL (2005) Glycine-rich antifreeze proteins from snow fleas. Science 310:461

    PubMed  Google Scholar 

  • Green RL, Warren GJ (1985) Physical and functional repetition in a bacterial ice nucleation gene. Nature 317:645–648

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Guo S, Garnham CP, Whitney JC, Graham LA, Davies PL (2012) Re-evaluation of a bacterial antifreeze protein as an adhesin with ice-binding activity. PLoS One 7(11):e48805. https://doi.org/10.1371/journal.pone.0048805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hampton SE, Moore MV, Ozersky T, Stanley EH, Polashenski CM, Galloway AWE (2015) Heating up a cold subject: prospects for under-ice plankton research in lakes. J Plankton Res 37:277–284

    Google Scholar 

  • Hampton SE, Galloway AWE, Powers SM, Ozersky T, Woo KH, Batt RD, Labou SG, O’Reilly CM, Sharma S, Lottig NR, Stanley EH, North RL, Stockwell JD, Adrian R, Wyhenmeyer GA, Arvola L, Baulch HM, Bertani I, Bowmn LL, Carey CC, Catalan J, Colom-Montero W, Domine LM, Felip M, Granados I, Gries C, Grossart H-P, Haberman J, Haldna M, Hayden B, Higgins SN (2017) Ecology under lake ice. Ecol Lett 20:98–111

    PubMed  Google Scholar 

  • Hanada Y, Nishimiya Y, Miura A, Tsuda S, Hidemasa Kondo H (2014) Hyperactive antifreeze protein from an Antarctic sea ice bacterium Colwellia sp. has a compound ice-binding site without repetitive sequences. FEBS J 281:3576–3590

    CAS  PubMed  Google Scholar 

  • Hargens AR, Shabica SV (1973) Protection against lethal freezing temperatures by mucus in an Antarctic limpet. Cryobiology 10:331–337

    CAS  PubMed  Google Scholar 

  • Hashim NH, Bharudin I, Nguong DL, Higa S, Bakar FD, Nathan S, Rabu A, Kawahara H, Illias RM, Najimudin N, Mahadi NM, Murad AM (2013) Characterization of Afp1, an antifreeze protein from the psychrophilic yeast Glaciozyma antarctica PI12. Extremophiles 17:63–73

    CAS  PubMed  Google Scholar 

  • Hashim NHF, Sulaiman S, Bakar FDA, Illias RM, Kawahara H, Najimudin N, Mahadi NM, Murad AMA (2014) Molecular cloning, expression and characterisation of Afp4, an antifreeze protein from Glaciozyma antarctica. Polar Biol 37:1495–1505

    Google Scholar 

  • Hawes TC, Worland MR, Bale JS (2010) Freezing in the Antarctic limpet Nacella concinna. Cryobiology 61:128–132

    CAS  PubMed  Google Scholar 

  • Hawes TC, Marshall CJ, Wharton DA (2011) Antifreeze proteins in the Antarctic springtail, Gressittacantha terranova. J Comp Physiol B 181:713–719

    CAS  PubMed  Google Scholar 

  • Hawes TC, Marshall CJ, Wharton DA (2014) A 9kDa antifreeze protein from the Antarctic springtail Gomphiocephalus hodgsoni. Cryobiology 69:181–183

    CAS  PubMed  Google Scholar 

  • Heisig M, Abraham NM, Liu L, Neelakanta G, Mattessich S, Sultana H, Shang Z, Ansari JM, Killiam C, Walker W, Cooley L, Flavell RA, Agaisse H, Fikrig E (2014) Anti-virulence properties of an antifreeze protein. Cell Rep 9:417–424

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holmstrup M, Sømme L (1998) Dehydration and cold hardiness in the Arctic collembolan Onychiurus arcticus Tullberg 1876. J Comp Physiol B 168:197–203

    Google Scholar 

  • Hopkin SP (1997) The biology of springtails. Oxford University Press, Oxford, p 344

    Google Scholar 

  • Hoshino T, Matsumoto N, Araki T, Georges F, Goda T, Ohgiya S (1998) Freezing resistance among isolates of a psychrophilic fungus, Typhula ishikariensis, from Norway. Proc NIPR Symp Polar Biol 11:112–118

    Google Scholar 

  • Hoshino T, Kiriaki M, Nakajima T (2003a) Novel thermal hysteresis proteins from low temperature basidiomycete, Coprinus psychromorbidus. Cryo Lett 24:135–142

    CAS  Google Scholar 

  • Hoshino T, Kiriaki TM, Ohgiya S, Fujiwara M, Kondo H, Nishimiya Y, Yumoto I, Tsuda S (2003b) Antifreeze proteins from snow mold fungi. Can J Bot 8:1175–1181

    Google Scholar 

  • Husby JA, Zachariassen ZE (1980) Antifreeze agents in the body fluid of winter active insects and spiders. Experientia 36:963–964

    CAS  Google Scholar 

  • Kawahara H, Nakana Y, Omiya K, Muryoi N, Nishikawa J, Obata H (2004) Production of two types of ice crystal-controlling proteins in Antarctic bacterium. J Biosci Bioeng 98:220–223

    CAS  PubMed  Google Scholar 

  • Kawahara H, Iwanaka Y, Higa S, Muryoi N, Sato M, Honda M, Omura H, Obata H (2007) A novel, intracellular antifreeze protein in an antarctic bacterium, Flavobacterium xanthum. Cryo Letters 28:39–49

    CAS  PubMed  Google Scholar 

  • Kawahara H, Matsuda Y, Sakaguchi T, Arai N, Koide Y (2016) Antifreeze activity of xylomannan from the mycelium and fruit body of Flammulina velutipes. Biocontrol Sci 21:153–159

    CAS  PubMed  Google Scholar 

  • Khodayari S, Moharramipour S, Kamali K, Hidalgo K, Renault D (2012) Effects of acclimation and diapause on the thermal tolerance of the two-spotted spider mite Tetranychus urticae. J Thermal Biol 37:419–423

    Google Scholar 

  • Khodayari S, Moharramipour S, Larvor V, Hidalgo K, Renault D (2013) Deciphering the metabolic changes associated with diapause syndrome and cold acclimation in the two-spotted spider mite Tetranychus urticae. PLoS One 8:e54025. https://doi.org/10.1371/journal.pone.0054205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiko R (2008) Ecophysiology of Antarctic sea-ice meiofauna. Doctoral Dissertation. Christian Albrechts University of Kiel, 116 p

    Google Scholar 

  • Kiko R (2010) Acquisition of freeze protection in a sea-ice crustacean through horizontal gene transfer? Polar Biol 33:543–556

    Google Scholar 

  • Kim HJ, Lee JH, Do H, Jung W (2014) Production of antifreeze proteins in cold-adapted yeasts. In: Buzzini P, Margesin M (eds) Cold-adapted yeasts: biodiversity, adaptation strategies and biotechnological significance. Springer, Heidelberg, pp 259–280

    Google Scholar 

  • Kirchner W (1973) Ecological aspects of cold resistance in spiders (a comparative study). In: Weiser W (ed) Effects of temperature on ectothermic organisms. Springer, Berlin, pp 271–279

    Google Scholar 

  • Kirchner W, Kestler P (1969) Untersuchungen zur chilfradpinne Araneus cornutus (Araneidae). J Insect Physiol 15:41–53

    Google Scholar 

  • Knight CA (1967) The freezing of supercooled liquids. Van Nostrand, Princeton, p 246

    Google Scholar 

  • Knight CA, DeVries AL (1989) Melting inhibition by fish antifreeze glycopeptides. Science 254:505–507

    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  Google Scholar 

  • Knight CA, DeVries AL, Oolman LD (1984) Fish antifreeze protein and the freezing and recrystallization of ice. Nature 308:295–296

    CAS  PubMed  Google Scholar 

  • Kobashigawa Y, Nishimiya Y, Miura K, Ohgiya S, Miura A, Tsuda S (2005) A part of ice nucleation protein exhibits the ice-binding ability. FEBS Lett 579:1493–1497

    CAS  PubMed  Google Scholar 

  • Kolb JH (2013) Short circuit co-evolution by the perfect parasites: antifreeze glycoproteins in Antarctic fish leeches (Hirudinea Piscicolid). PhD dissertation, Massey University, New Zealand, 290 pp

    Google Scholar 

  • Kondo H, Hanada Y, Sugimoto H, Hoshino T, Garnham CP, Davies PL, Tsuda S (2012) Ice-binding site of snow mold fungus antifreeze protein deviates from structural regularity and high conservation. PNAS USA 109:9360–9365

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kostal V (2010) Cell structural modifications in insects at low temperatures. In: Denlinger DL, Lee RE (eds) Low temperature biology of insects. Cambridge University Press, Cambridge, pp 116–140

    Google Scholar 

  • Krog JO, Zachariassen KE, Larsen B, Smidsrød O (1979) Thermal buffering in afro-alpine plants due to nucleating agent-induced water freezing. Nature 282(5736):300–301

    Google Scholar 

  • Larson D, Middle L, Vu H, Zhang W, Serianni AS, Duman JG, Barnes BM (2014) Wood frog adaptations to overwintering in Alaska: new limits to freezing tolerance. J Exp Biol 217:2193–2200

    PubMed  Google Scholar 

  • Layne JR (1991) External ice triggers freezing in freeze-tolerant frogs at temperatures above their supercooling point. J Herpetol 25:129–130

    Google Scholar 

  • Layne JR, Lee RE (1987) Freeze tolerance and the dynamics of ice formation in wood frogs (Rana sylvatica) from southern Ohio. Can J Zool 65:2062–2065

    Google Scholar 

  • Lee RE (2010) A primer on insect cold tolerance. In: Denlinger DL, Lee RE (eds) Low temperature biology of insects. Cambridge University Press, Cambridge, pp 3–34

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lee RE, Denlinger DL (2010) Rapid cold hardening: ecological significance and underpinning mechanisms. In: Denlinger DL, Lee RE (eds) Low temperature biology of insects. Cambridge University Press, Cambridge, pp 35–58

    Google Scholar 

  • Lee RE, Warren GJ, Gusta LV (eds) (1995) Biological ice nucleation and its applications. Americal Phytological Society Press, St Paul, MN, p 370

    Google Scholar 

  • Lee JK, Park KS, Park S, Park H, Song YH, Kang SH, Kim HJ (2010) An extracellular ice-binding glycoprotein from an Arctic psychrophilic yeast. Cryobiology 60:222–228

    CAS  PubMed  Google Scholar 

  • Lee JH, Park AK, Do H, Park KS, Moh SH, Chi YM, Kim HJ (2012) Structural basis for antifreeze activity of ice-binding protein from Arctic yeast. J Biol Chem 287:11460–11468

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li N, Andorfer CA, Duman JG (1998) Enhancement of insect antifreeze protein activity by low molecular weight solutes. J Exp Biol 201:2243–2251

    CAS  PubMed  Google Scholar 

  • Lin Y, Duman JG, DeVries AL (1972) Studies on the structure and activity of low molecular weight glycoproteins from an Antarctic fish. Biochem Biophys Res Comm 46:87–92

    CAS  PubMed  Google Scholar 

  • Lin F-H, Graham LA, Campbell RL, Davies PL (2007) Structural modeling of snow flea antifreeze protein. Biophys J 92(5):1717–1723

    CAS  PubMed  Google Scholar 

  • Lindow SE (1983) The role of bacterial ice nucleation in frost injury to plants. Annu Rev Phytopathol 21:363–384

    Google Scholar 

  • Lindow SE, Arny DC, Upper CD (1978) Erwinia herbicola: a bacterial ice nucleus active in increasing frost injury to corn. Phytopathology 68:523–527

    Google Scholar 

  • Lundheim R, Zachariassen KE (1993) Water balance of overwintering beetles in relation to strategies for cold tolerance. J Comp Physiol B 163:1–4

    Google Scholar 

  • Mangiagalli M, Bar-Dolev M, Tedesco P, Natalello A, Kaleda A, Brocca S, Pascale D, Pucciarelli S, Miceli C, Bravslavsky I (2017) Cryo-protective effect of an ice-binding protein derived from Antarctic bacteria. FEBS J 284:163–177

    Google Scholar 

  • Marshall CJ (2003) Ice active proteins from an Antarctic nematode Panogrolaimus davidii. Cryo-Lett 24:404

    Google Scholar 

  • Martof BS, Humphries RL (1959) Geographic variation in the wood frog, Rana sylvatica. Am Midl Nat 61:350–389

    Google Scholar 

  • Meier P, Zettel J (1997) Cold hardiness in Entomobrya nivalis (Collembola, Entomobryidae): annual cycle of polyols and antifreeze proteins, and antifreeze triggering by temperature and photoperiod. J Comp Physiol 167:297–304

    CAS  Google Scholar 

  • Michaud MR, Denlinger DL (2010) Genomics, proteomics and metabolomics: finding the other players in insect cold tolerance. In: Denlinger DL, Lee RE (eds) Low temperature biology of insects. Cambridge University Press, Cambridge, pp 91–115

    Google Scholar 

  • Mock T, Thomas DN (2005) Recent advances in sea-ice microbiology. Environ Microbiol 7:605–619

    CAS  PubMed  Google Scholar 

  • Mok Y-F, Lin F-H, Laurie A, Graham LA, Celik Y, Braslavsky I, Davies PL (2010) Structural basis for the superior activity of the large isoform of snow flea antifreeze protein. Biochemistry 49:2593–2603

    CAS  PubMed  Google Scholar 

  • Mueller GM, Wolber PK, Warren GJ (1990) Clustering of ice nucleation protein correlates with ice nucleation activity. Cryobiology 27:416–422

    CAS  PubMed  Google Scholar 

  • Muñoz PA, Márquez SL, González-Nilo FD, Márquez-Miranda V, Blamey JM (2017) Structure and application of antifreeze proteins from Antarctic bacteria. Microb Cell Factories 16:138. Article number: 138

    Google Scholar 

  • Neelakanta G, Sultana H, Fish D, Anderson JF, Fikrig E (2010) Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold. J Clin Invest 120:3179–3190

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nickell PK, Sass S, Verleye D, Blumenthall EM, Duman JG (2013) Antifreeze proteins in the primary urine of larvae of the beetle Dendroides canadensis (Latreille). J Exp Biol 216:1695–1703

    CAS  PubMed  Google Scholar 

  • Olive LC, Meister K, DeVries AL, Duman JG, Guo S, Bakker HJ, Voets IK (2016) Blocking rapid ice crystal growth through non-basal plane adsorption of antifreeze proteins. Proc Natl Acad Sci USA 113:3740–3745

    Google Scholar 

  • Park AK, Park KS, Kim HJ, Park H, Ahn IY, Chi YM, Moon JH (2011) Crystallization and preliminary x-ray crystallographic studies of the ice-binding protein from the Antarctic yeast Leucosporidium sp. AY30. Acta Cryststallogr Sect F Struct Biol Cryst Commun 67:800–802

    CAS  Google Scholar 

  • Pentelute BL, Gates ZP, Tereshko V, Dashnau JL, Vanderkooi JM, Kossiakoff AA, Kent SB (2008) X-ray structure of snow flea antifreeze protein determined by racemic crystallization of synthetic protein enantiomers. J Am Chem Soc 130:9695–9701

    CAS  PubMed  PubMed Central  Google Scholar 

  • Poinsot-Balaguer N, Barra JA (1983) Experimental and ultrastructural data on freezing resistance in Folsomides angularis (Insecta, Collembola). Pedobiologia 25:357–363

    Google Scholar 

  • Priddle J, Heywood RB, Theriot E (1986) Some environmental factors influencing phytoplankton in the Southern Ocean around South Georgia. Polar Biol 5:65–79

    Google Scholar 

  • Pucciarelli S, Chiappori F, Devaraj RR, Yang G, Yu T, Ballarini P, Miceli C (2014) Identification and analysis of two sequences encoding ice-binding proteins obtained from a putative bacterial symbiont of the psychrophilic Antarctic ciliate Euplotes focardii. Antarct Sci 26:491–501

    Google Scholar 

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

    PubMed  Google Scholar 

  • Ramløv H, Wharton D, Wilson P (1996) Recrystallization in a freezing tolerant Antarctic nematode, Panagrolaimus davidi, and an alpine Weta, Hemideina maori (Orthoptera; Stenopelmatidae). Cryobiology 33:607–613

    PubMed  Google Scholar 

  • Raymond JA, Lin Y, DeVries AL (1975) Glycoprotein and protein antifreezes in two Alaskan fishes. J Exp Zool 193(1):125–130

    CAS  PubMed  Google Scholar 

  • Raymond JA (2016) Dependence on epiphytic bacteria for freezing protection in an Antarctic moss, Bryum argenteum. Environ Microbiol Rep 8:14–19

    CAS  PubMed  Google Scholar 

  • Raymond JA, Janech MG (2009) Ice-binding proteins from enoki and shiitake mushrooms. Cryobiology 58:151–156

    CAS  PubMed  Google Scholar 

  • Raymond JA, Kim KJ (2012) Possible role of horizontal gene transfer in the colonization of sea ice by algae. PLoS One 2012(7):e35968. https://doi.org/10.1371/journal.pone.0035968.pmid:22567121

    Article  Google Scholar 

  • Raymond JA, Knight C (2003) Ice binding, recrystallization inhibition, and cryoprotective properties of ice-active substances associated with Antarctic sea ice diatoms. Cryobiology 46:174–181

    CAS  PubMed  Google Scholar 

  • Raymond JA, Fritsen C, Shen K (2007) An ice-binding protein from an Antarctic sea ice bacterium. FEMS Microbiol Ecol 61:214–221

    CAS  PubMed  Google Scholar 

  • Raymond JA, Christner BC, Schuster SC (2008) A bacterial ice-binding protein from the Vostok ice core. Extremophiles 12:713–717

    CAS  PubMed  Google Scholar 

  • Raymond JA, Rachael M-K, Valentin K (2017) Multiple ICE-binding proteins of probable prokaryotic origin in an Antarctic lake alga, sp. ICE-MDV (Chlorophyceae). J Phycol 53(4):848–854

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  • Rozsypal J, Kostal V (2018) Supercooling and freezing as eco-physiological alternatives rather than mutually exclusive strategies: a case study in Pyrrhocoris apterus. J Insect Physiol 111:53–62

    CAS  PubMed  Google Scholar 

  • Schmid WD (1982) Survival of frogs in low temperature. Science 215:697–698

    CAS  PubMed  Google Scholar 

  • Schnenker R (1983) Effects of temperature acclimation of cold-hardiness of alpine micro-arthropods. Rev Ecol Biol Sol 20:37–47

    Google Scholar 

  • Schünemann H, Werner I (2005) Seasonal variations in distribution patterns of sympagic meiofauna in Arctic pack ice. Mar Biol 146:1091–1102

    Google Scholar 

  • Shah SHH, Kar RK, Asmawi AA, Rahman MBA, Murad AMA, Mahadi NM, Basri M, Rahman RNZA, Salleh AB, Chatterjee S (2012) Solution structures, dynamics, and ice growth inhibitory activity of peptide fragments derived from an Antarctic yeast protein. https://doi.org/10.1371/journal.pone.0049788.s006

  • Shier WT, DeVries AL (1975) Carbohydrates of antifreeze proteins from an Antarctic fish. FEBS Lett 54:135–142

    CAS  PubMed  Google Scholar 

  • Shoulders MD, Raines RT (2009) Collagen structure and stability. Annu Rev Biochem 78:929–958

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sinclair BJ, Chown SL (2002) Haemolymph osmolality and thermal hysteresis activity in 17 species of arthropods from sub-Antarctic Marion Island. Polar Biol 25:928–933

    Google Scholar 

  • Sinclair BJ, Sjursen H (2001) Cold tolerance of the Antarctic springtail Gomphiocephalus hodgsoni (Collembola, Hypogastruridae). Antarct Sci 13:271–279

    Google Scholar 

  • Singh P, Hanada Y, Mohan Singh S, Tsuda (2014) Antifreeze protein activity in Arctic cryconite bacteria. FEMS Microbiol Lett 351:14-22

    Google Scholar 

  • Sjursen H, Sømme L (2000) Seasonal changes in tolerance to cold and desiccation in Phauloppia sp. (Acari, Oribatida) from Finse, Norway. J Insect Physiol 46:1387–1396

    CAS  PubMed  Google Scholar 

  • Sømme L, Conradi-Larsen EM (1977) Cold hardiness of Collembolans and oribatid mites from windswept mountain ridges. Oikos 29:118–126

    Google Scholar 

  • Sømme L, Stromme A, Zacchariassen KE (1993) Notes on the ecology and physiology of the Antarctic oribatid mite Maudheimia wilsoni. Polar Res 12:21–25

    Google Scholar 

  • Southworth MW, Wolber PK, Warren GJ (1988) Nonlinear relationship between concentration and activity of a bacterial ice nucleation protein. J Biol Chem 263:15211–15216

    CAS  PubMed  Google Scholar 

  • Storey KB, Storey JM (1984) Biochemical adaption for freezing tolerance in the wood frog, Rana sylvatica. J Comp Physiol B 155(1):29–36

    CAS  Google Scholar 

  • Storey KB, Storey JM (2004) Physiology, biochemistry, and molecular biology of vertebrate freeze tolerance: the wood frog. In: Fuller BJ, Lane N, Benson EE (eds) Life in the frozen state. CRC, Washington, DC, pp 243–274

    Google Scholar 

  • Storey KB, Storey JM (2010) Oxygen: stress and adaptation in cold-hardy insects. In: Denlinger DL, Lee RE (eds) Low temperature biology of insects. Cambridge University Press, Cambridge, pp 141–165

    Google Scholar 

  • Storey KB, Storey JM (2017) Molecular physiology of freeze tolerance in vertebrates. Physiol Rev 97:623–665

    CAS  PubMed  Google Scholar 

  • Sullivan KJ, Biggar KK, Storey KB (2015) Transcript expression of the freeze responsive gene fr10 in Rana sylvatica during freezing, anoxia, dehydration, and development. Mol Cell Biochem 399:17–25

    CAS  PubMed  Google Scholar 

  • Sun X, Griffith M, Pasternak J, Glick BR (1995) Low temperature growth, freezing survival, and production of antifreeze protein by the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Can J Microbiol 41:776–784

    CAS  PubMed  Google Scholar 

  • Sun T, Feng-Hsu Lin F-H, Campbell RL, Allingham JS, Davies PL (2014) An antifreeze protein folds with an interior network of more than 400 semi-clathrate waters. Science 343:795–798

    CAS  PubMed  Google Scholar 

  • Tereshina VM, Memorskaya AS (2005) Adaptation of Flammulina velutipes to hypothermia in natural environments: the role of lipids and carbohydrates. Microbiology 74:279–283

    CAS  Google Scholar 

  • Theede HR, Schneppenheim R, Bevess L (1976) Frostschutz- glycoproteine bei Mytilus edulis? Mar Biol 36:183–189

    CAS  Google Scholar 

  • Thomas DN, Dieckmann GS (2002) Antarctic Sea ice - a habitat for extremophiles. Science 295:641–644

    CAS  PubMed  Google Scholar 

  • Thorne M, Kagoshima H, Clark M, Marshall C, Wharton D (2014) Molecular analysis of the cold tolerant Antarctic nematode, Panagrolaimus davidi. PLoS One 9(8):e104526. http://doi.org/1371/journal.pone.0104526

    PubMed  PubMed Central  Google Scholar 

  • Thorne MAS, Seybold A, Marshall C, Wharton D (2017) Molecular snapshot of an intracellular freezing event in an Antarctic nematode. Cryobiology 75:117–124

    CAS  PubMed  Google Scholar 

  • Todde G, Whitman C, Hovmoller S, Laaksonen A (2014) Induced ice melting by the snow flea antifreeze protein from molecular dynamics simulations. J Phys Chem B 118:13527–13534

    CAS  PubMed  Google Scholar 

  • Treonis AM, Wall DH, Virginia RA (2000) The use of anhydrobiosis by soil nematodes in the Antarctic dry valleys. Funct Ecol 14:460–467

    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

    CAS  Google Scholar 

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

    Google Scholar 

  • Upper CD, Vali G (1995) The discovery of ice nucleation-active bacteria and its role in the injury of plants by frost. In: Lee RE, Warren GJ, Gusta LV (eds) Biological ice nucleation and its applications. Americal Phytological Society Press, St Paul, MN, pp 29–40

    Google Scholar 

  • Vali G (1995) The principles of ice nucleation. In: Lee RE, Warren GJ, Gusta LV (eds) Biological ice nucleation and its applications. American Phytological Society Press, St Paul, MN, pp 1–28

    Google Scholar 

  • VanVoorhies WV, Raymond JA, DeVries AL (1978) Glycoproteins as biological antifreeze agents in the cod, Gadus ogac. Physiol Zool 51:347–353

    CAS  Google Scholar 

  • Verpoorter C, Kutser T, Seekell DA, Tranvik LJ (2014) A global inventory of lakes based on high-resolution satellite imagery. Geophys Res Lett 41:6396–6402

    Google Scholar 

  • Walker VK, Palmer GR, Voordouw G (2006) Freeze-thaw tolerance and clues to the winter survival of a soil community. Appl Environ Microbiol 72:1784–1792

    CAS  PubMed  PubMed Central  Google Scholar 

  • Waller CL, Worland MR, Convey P, Barnes DKA (2006) Ecophysiological strategies of Antarctic intertidal invertebrates faced with freezing stress. Polar Biol 29:1077–1083

    Google Scholar 

  • Walsh LL, Tucker PK (2017) Contemporary range expansion of the Virginia opossum (Didelphis virginiana) impacted by humans and snow cover. Can J Zool 2018:107–115

    Google Scholar 

  • Walters KR, Serianni AS, Sformo T, Barnes BM, Duman JG (2009) A non-protein thermal hysteresis-producing xylomannan antifreeze in a freeze tolerant Alaskan beetle. Proc Natl Acad Sci USA 106:20210–20215

    CAS  PubMed  PubMed Central  Google Scholar 

  • Walters KR, Serianni AS, Voituron Y, Sformo T, Barnes BM, Doman JG (2011) A thermal hysteresis-producing xylomannan glycolipid antifreeze associated with cold-tolerance is found in diverse taxa. J Comp Physiol B 181:631–640

    CAS  PubMed  Google Scholar 

  • Wang SY, Damodoran S (2009) Ice-structuring peptides derived from bovine collagen. J Agric Food Chem 57:5501–5509

    CAS  PubMed  Google Scholar 

  • Wang L, Duman JG (2005) Antifreeze proteins of the beetle Dendroides canadensis enhance one another’s activities. Biochemist 44:10305–10312

    CAS  Google Scholar 

  • Wang S, Zhao J, Chen L, Zhou Y, Wu J (2014) Preparation, isolation and hypothermia protection activity of antifreeze peptides from shark skin collagen. Food Sci Technol 55:210–217

    CAS  Google Scholar 

  • Warren G, Corotto L (1989) The consensus sequence of ice nucleation proteins from Erwinia herbicola, Pseudomonas fluorescens and Pseudomonas syringae. Gene 85:239–242

    CAS  PubMed  Google Scholar 

  • Weyhenmeyer GA, Westöö A-K, Willén E (2008) Increasingly ice-free winters and their effects on water quality in Sweden’s largest lakes. Hydrobiology 599:111–118

    CAS  Google Scholar 

  • Weyhenmeyer GA, Livingstone DM, Meili M, Jensen O, Benson B, Magnuson JJ (2011) Large geographical differences in the sensitivity of ice-covered lakes and rivers in the northern hemisphere to temperature changes. Glob Chang Biol 17(1):268–275

    Google Scholar 

  • Wharton DA (1995) Cold tolerance strategies in nematodes. Biol Rev 70:161–185

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wharton D, Ferns D (1995) Survival of intracellular freezing by the Antarctic nematode Panagrolaimus davidi. J Exp Biol 198:381–387

    Google Scholar 

  • Wharton D, Raymond MR (2015) Cold tolerance of the Antarctic nematodes Plectus murrayi and Scottnema lindsayae. J Comp Physiol B 185:281–285

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Wharton D, Downes M, Goodall G, Marshall C (2005a) Freezing and cryoprotective dehydration in an Antarctic nematode (Panagrolaimus davidi) visualised using a freeze substitution techniques. Cryobiology 50:21–28

    CAS  PubMed  Google Scholar 

  • Wharton D, Barrett J, Goodall G, Marshall C, Ramløv H (2005b) Ice-active proteins from the Antarctic nematode, Panagrolaimus davidi. Cryobiology 51:198–207

    CAS  PubMed  Google Scholar 

  • Whitmore DH, Gonzalez R, Baust JG (1985) Scorpion cold hardiness. Physiol Zool 58:526–537

    Google Scholar 

  • Wilkins SP, Blum AJ, Burkepile DE, Rutland TJ, Wierzbicki A, Kelly AM, Hamann MT (2002) Isolation of an antifreeze peptide from the Antarctic sponge Homaxinella balfourensis. Cell Mol Life Sci 59:2210–2215

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wolber PK, Warren GJ (1989) Bacterial ice nucleating proteins. Trends Biochem Sci 14:179–182

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Worland MR, Grubor-Lajsik 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  PubMed  Google Scholar 

  • Xiao N, Suzuki K, Nishimiya Y, Kondo H, Miura A, Tsuda S, Hoshino T (2010) Comparison of functional properties of two fungal antifreeze proteins from Antarctomyces psychrotrophicus and Typhula ishikariensis. FEBS J 277:394–403

    CAS  PubMed  Google Scholar 

  • Xu H, Griffith M, Patten CL, Glick BR (1998) Isolation and characterization of an antifreeze protein with ice nucleation activity from the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Can J Microbiol 44:64–73

    CAS  Google Scholar 

  • Yamashita Y, Nakamura N, Omiya K, Nishikawa J, Kawahara H, Obata H (2002) Identification of an antifreeze lipoprotein from Moraxella sp. of Antarctic origin. Biosci Biotechnol Biochem 66:239–247

    CAS  PubMed  Google Scholar 

  • Yeung KL, Wolf EE, Duman JG (1991) A scanning tunneling microscopy study of an insect lipoprotein ice nucleator. J Vac Sci Technol B 9:1197–1201

    CAS  Google Scholar 

  • Young SR, Block W (1980) Experimental studies of cold tolerance in an Antarctic terrestrial mite. J Insect Physiol 26:189–200

    Google Scholar 

  • Zachariassen KE, Hammel HT (1988) The effect of ice-nucleating agents on ice-nucleating activity. Cryobiology 25(2):143–147

    Google Scholar 

  • Zachariassen KE, Kristiansen E (2000) Ice nucleation and Antinucleation in nature. Cryobiology 41(4):257–279

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Zachariassen KE, Duman JG, Kristiansen E, Pedersen S, Li N (2010) Ice nucleation and antifreeze proteins in animals. In: Graether S (ed) Biochemistry and function of antifreeze proteins. Nova Science, New York, pp 73–104

    Google Scholar 

  • Zettel J (1984) Cold hardiness strategies and thermal hysteresis in Collembola. Rev Ecol Biol Sol 21:189–203

    Google Scholar 

  • Zettel J, von Allmen H (1982) Jahresverlauf der Kalteresistenz zweir Collembola-Arten in den Berner Voralpen. Rev Suisse Zool 89:927–939

    Google Scholar 

  • Zimmerman SL, Frisbie J, Goldstein DL, West J, Rivera JK, Krane CM (2007) Excretion and conservation of glycerol, and expression of aquaporins and glyceroporins, during cold acclimation in Cope’s gray tree frog Hyla chrysoscelis. Am J Physiol 292:R544–R555

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, USA

    John G. Duman

  2. Sanford School of Medicine, University of South Dakota, Vermillion, SD, USA

    Samuel S. Newton

Authors
  1. John G. Duman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Samuel S. Newton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John G. Duman .

Editor information

Editors and Affiliations

  1. Department of Natural Sciences, Roskilde University, Roskilde, Denmark

    Hans Ramløv

  2. Copenhagen, Denmark

    Dennis Steven Friis

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Duman, J.G., Newton, S.S. (2020). Antifreeze Proteins in Other Species. In: Ramløv, H., Friis, D. (eds) Antifreeze Proteins Volume 1. Springer, Cham. https://doi.org/10.1007/978-3-030-41929-5_8

Download citation

Publish with us

Policies and ethics

Search

Navigation