Origin and Mechanism of Evolution of Antifreeze Glycoproteins in Polar Fishes

  • Chi-Hing C. Cheng


The frigid waters of the polar oceans delimit the cold extreme for marine life. This is particularly true in the case of the thermally isolated Antarctic Ocean which is perpetually near or at freezing (−1.9 °C) due to the thermal barrier imposed by the Antarctic Circumpolar Current [1]. The most fundamental survival challenge faced by teleost fishes in these waters is a physical one — the threat of being frozen. The body fluids of marine teleosts including polar species are hyposmotic to sea water, 300–600 mOsM [2,3] versus 1000 mOsM, and thus have a higher colligative freezing point than the latter, −0.56 °C to −1.1 °C versus −1.86 °C. By these simple physical considerations alone, freezing death would be unavoidable especially in the presence of ice. Unlike some reptiles and amphibians, fish cannot survive even partial freezing of their body fluids. A number of polar and subpolar fishes had overcome this environmental challenge with a biological solution — they evolved ice-binding antifreeze proteins which enabled them to successfully colonize icy habitats that were otherwise out of their reach. The impact of the evolution of these unique antifreezing proteins on organismal and ecological success is manifested most strikingly in the case of the Antarctic notothenioid fishes — a single teleost suborder (Notothenioidei) that has come to dominate today’s Antarctic fish fauna in terms of species number (∼50%) and biomass (≥90%) [2,4, 5, 6].


Antarctic Circumpolar Current Antifreeze Protein Antarctic Fish Slippage Replication Notothenioid Fish 


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  1. 1.
    Kennett JP (1982) Marine geology. Prentice-Hall, New JerseyGoogle Scholar
  2. 2.
    Prosser CL (1973) Water: osmotic balance; hormonal regulation. In: Prosser CL (ed) Comparative animal physiology. Saunders, Philadelphia, pp 1–78Google Scholar
  3. 3.
    Eastman JT (1993) Antarctic fish biology. Academic Press, CaliforniaGoogle Scholar
  4. 4.
    Hubold G (1991) Ecology of notothenioid fish in the Weddell Sea. In: di Prisco G, Maresca M, Tota (eds) Biology of Antarctic fish. Springer-Verlag, Berlin, pp 3–22CrossRefGoogle Scholar
  5. 5.
    Ekau W (1990) Demersal fish fauna of the Weddell Sea. Antarct Sci. 2:129–137CrossRefGoogle Scholar
  6. 6.
    Dewitt HH (1971) Coastal and deep-water benthic fishes of the Antarctic. In: Bushnell VC (ed) Antarctic map folio series folio 15. American Geographical Society, New York, pp 1–10Google Scholar
  7. 7.
    Cheng C-HC, DeVries AL (1991) The role of antifreeze glycopeptides and peptides in the freezing avoidance of cold-water fish. In: di Prisco G (ed) Life under extreme conditions. Springer-Verlag, Berlin-Heidelberg, pp 1–14CrossRefGoogle Scholar
  8. 8.
    Hew CL, Yang DSC (1992) Protein interaction with ice. Eur J Biochem 203:33–42PubMedCrossRefGoogle Scholar
  9. 9.
    DeVries AL (1971) Glycoproteins as biological antifreeze agents in Antarctic fishes. Science 172:1152–1155PubMedCrossRefGoogle Scholar
  10. 10.
    DeVries AL, Vandenheede J, Feeney RE (1971) Primary structure of freezing point-depressing glycoproteins. J Biol Chem 246:305–308PubMedGoogle Scholar
  11. 11.
    DeVries AL (1982) Biological antifreeze agents in coldwater fishes. Comp Biochem Physiol A73:627–640CrossRefGoogle Scholar
  12. 12.
    Cheng C-HC (1996) Genomic basis for antifreeze glycopeptide heterogeneity and abundance in Antarctic fishes. In: Ennion S, Goldspink G (eds) Gene expression and manipulation in aquatic organisms. Cambridge, United Kingdom, pp 1–20Google Scholar
  13. 13.
    Morris HR, Thompson MR, Osuga DT, Ahmed AT, Chan SM, Vandenheede JR, Feeney RF (1978) Antifreeze glycoproteins from the blood of an Antarctic fish. J Biol Chem. 253:5155–5162PubMedGoogle Scholar
  14. 14.
    O’Grady SM, Schrag JD, Raymond JA, DeVries AL (1982) Comparison of antifreeze glycopeptides from Arctic and Antarctic fishes. J Exp Zool 224:177–185CrossRefGoogle Scholar
  15. 15.
    Fletcher GL, Hew CL, Joshi SB (1982) Isolation and characterization of antifreeze glycoproteins from the frostfish, Microgadus tomcod. Can J Zool 60:348–355CrossRefGoogle Scholar
  16. 16.
    Duman JG, DeVries AL (1976) Isolation, characterization and physical properties of protein antifreeze from the winter flounder, Pseudopleuronectes americanus. Comp Biochem Physiol B54:375–380Google Scholar
  17. 17.
    Scott GK, Davies PL, Shears MA, Fletcher GL (1987) Structural variations in the alanine-rich antifreeze proteins of the Pleuronectinae. Eur J Biochem 168:629–633PubMedCrossRefGoogle Scholar
  18. 18.
    Hew CL, Joshi S, Wang N-C, Kao M-H, Ananthanarayanan VS (1985) Structures of shorthorn sculpin antifreeze polypeptides. Eur J Biochem 151:167–172PubMedCrossRefGoogle Scholar
  19. 19.
    Ewart KV, Fletcher GL (1993) Herring antifreeze protein primary structure and evidence for a C-type lectin evolutionary origin. Mol Mar Biol Biotech 2:20–27Google Scholar
  20. 20.
    Ng NF, Trinh YK, Hew CL (1986) Structure of an antifreeze polypeptide precursor from the sea raven, Hemitripterus americanus. J Biol Chem 261:15690–15696PubMedGoogle Scholar
  21. 21.
    Cheng C-HC, DeVries AL (1989) Structures of antifreeze peptides from the Antarctic fish Austrolycicthys brachycephalus. Biochim Biophy Acta 997:55–64CrossRefGoogle Scholar
  22. 22.
    Hew CL, Wang N-C, Joshi S, Fletcher GL, Scott GK, Hayes PH, Buettner B (1988) Multiple genes provide the basis for antifreeze protein diversity and dosage in the ocean pout, Macrozoarces americanus. J Biol Chem 263:12049–12055PubMedGoogle Scholar
  23. 23.
    Wang X, DeVries AL, Cheng C-HC (1996) Antifreeze peptide heterogeneity in an Antarctic eel pout includes an unusually large major variant composed of two 7 kDa type III AFPs linked in tandem. Biochim Biophy Acta 1247:163–172Google Scholar
  24. 24.
    Scott GK, Hayes PH, Fletcher GL, Davies PL (1988) Wolffish antifreeze protein genes are primarily organized as tandem repeats that each contain two genes in inverted orientation. Mol Cell Biol 8:3670–3675PubMedGoogle Scholar
  25. 25.
    Scott GK, Fletcher GL, Davies PL (1986) Fish antifreeze proteins: recent gene evolution. Can J Fish Aquat Sci 43:1028–1034CrossRefGoogle Scholar
  26. 26.
    Nelson JS (1994) Fishes of the world. Wiley, New YorkGoogle Scholar
  27. 27.
    Svetovidov AN (1948) Gadiformes. Israel program for scientific translation, JerusalemGoogle Scholar
  28. 28.
    Eastman JT (1991) Evolution and diversification of Antarctic notothenioid fishes. Am Zool 31:93–109Google Scholar
  29. 29.
    Chen L, DeVries AL, Cheng C-HC (1997) Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proc Natl Acad Sci USA 94:3811–3816PubMedCrossRefGoogle Scholar
  30. 30.
    Chen L, DeVries AL, Cheng C-HC (1997) Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod. Proc Natl Acad Sci USA 94:3817–3822PubMedCrossRefGoogle Scholar
  31. 31.
    Logsdon MJ, Doolittle WF (1977) Origin of antifreeze protein genes: a cool tale in molecular evolution. Proc Natl Acad Sci USA 94:3485–3487CrossRefGoogle Scholar
  32. 32.
    Hsiao KC, Cheng C-HC, Fernandes IE, Detrich HW, DeVries AL (1990) An antifreeze glycopeptide gene from the Antarctic cod Notothenia coriiceps neglecta encodes a polyprotein of high peptide copy number. Proc Natl Acad Sci USA 87: 9265–9269PubMedCrossRefGoogle Scholar
  33. 33.
    Leaver MJ, George SG (1996) unpublished. Genbank accession number X56744Google Scholar
  34. 34.
    Levinson G, Gutman GA (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4:203–221PubMedGoogle Scholar
  35. 35.
    Maeda N, Smithies O (1986) The evolution of multigene families: human haptoglobin genes. Annu Rev Genet 20:81–108PubMedCrossRefGoogle Scholar
  36. 36.
    Lewin B (1994) Genes V. Cell Press, MassachusettsGoogle Scholar
  37. 37.
    Martin AP, Palumbi SR (1993) Body size, metabolic rate, generation time, and the molecular clock. Proc Natl Acad Sci USA 90:4087–4091PubMedCrossRefGoogle Scholar
  38. 38.
    Clarke A, Johnston IA (1996) Evolution and adaptive radiation of Antarctic fishes. Trends Ecol Evol 11:187–228CrossRefGoogle Scholar
  39. 39.
    Bargelloni L, Ritchie PA, Patarnello T, Battaglia B, Lambert DM, Meyer A (1994) Molecular evolution at subzero temperatures: mitochondrial and nuclear phylogenies of fishes from Antarctica (suborder Notothenioidei) and the evolution of antifreeze glycopeptides. Mol Biol Evol 11:854–863PubMedGoogle Scholar
  40. 40.
    Ohta T (1989) Role of gene duplication in evolution. Genome 31:304–310PubMedCrossRefGoogle Scholar
  41. 41.
    Piatigorsky J, Wistow G (1991) The recruitment of crystallins: new functions precede gene duplication. Science 252:1078–1079CrossRefGoogle Scholar
  42. 42.
    Patthy L (1996) Exon shuffling and other ways of module exchange. Matrix Biol 15:301–310PubMedCrossRefGoogle Scholar
  43. 43.
    Doolittle RF (1994) Convergent evolution: the need to be explicit. TIBS 19:15–19PubMedGoogle Scholar
  44. 44.
    Hamada H, Petrino MG, Kakaunaga T (1982) A novel repeated element with Z-DNA forming potential is widely found in evolutionary diverse eukaryotic genomes. Proc Natl Acad Sci USA 79:6465–6469PubMedCrossRefGoogle Scholar
  45. 45.
    Pardue ML, Lowenhaupt K, Rich A, Nordheim A (1987) (dC-dA)n · (dG-dT)n sequences have evolutionarily conserved chromosomal locations in Drosophila with implications for roles in chromosome structure and factions, EMBO J 6:1781–1789PubMedGoogle Scholar
  46. 46.
    Estoup A, Presa P, Krieg F, Vaiman D, Guyomard R (1993) (CT)n and (GT)n microsatellites: a new class of genetic markers for Salmo trutta L. (brown trout). Heredity 71:488–496PubMedCrossRefGoogle Scholar
  47. 47.
    Harris AS, Wright JM (1995) Nucleotide sequence and genomic organization of cichlid fish minisatellites. Genome 38:177–184PubMedCrossRefGoogle Scholar
  48. 48.
    Deng G, Andrews DW, Laursen RA (1997) Amino acid sequence of a new type of antifreeze protein, from the longhorn sculpin, Myoxocephalus octodecimspinosus. FEBS Lett 402:17–20PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Italia 1998

Authors and Affiliations

  • Chi-Hing C. Cheng
    • 1
  1. 1.Department of Molecular and Integrative PhysiologyUniversity of IllinoisUrbanaUSA

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