Abstract
The Antarctic snailfish, Paraliparis devriesi (Liparididae), occupies an epibenthic habitat at a depth of 500–650 m in the subzero waters of McMurdo Sound, Antarctica. This species has watery (97%) gelatinous subdermal extracellular matrix (SECM) comprising a mean of 33.8% of the body weight, the largest known proportion of any adult fish. The protein concentration of the SECM was found to be 6–7 mg ml−1 (0.6–0.7% w/v). Separation of the polypeptides of the SECM by SDS-PAGE revealed 11 polypeptides ranging in relative molecular mass (Mr) from 67,000 to 13,000, with other unresolved polypeptides of less than 13,000. The isoelectric points of these proteins ranged from 4.85 to 8.05. Partial N-terminal amino acid sequence data were obtained for four of the major SECM polypeptides. The N-terminal amino acid sequences of three of these were not identical to or homologous with any other known sequences, whereas the N-terminal sequence of one polypeptide (Mr 51,000) was identical to partial sequence from the apolipoprotein A-I precursor of Atlantic salmon (Salmo salar). Although not isolated from either SECM or serum, melting point-freezing point behavior of body fluids suggest that Paraliparis possess modest amounts of a noncolligative antifreeze compound. Since relatively small amounts of antifreeze are present in the serum and even less in the SECM, freezing avoidance results from the combined effects of antifreeze and the elevated osmolality of body fluids. There are no special adaptations to prevent freezing in the superficially located high water content SECM.
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References cited
Andriashev, A.P. 1980. A new liparid fish in McMurdo Sound. Antarct. J. U.S. 15 (5): 150.
Argos, P. 1989. Predictions of protein structure from gene to amino acid sequences. In Protein Structure, A Practical Approach. pp. 169–190 Edited by T.E. Creighton IRL Press, Oxford.
Banerjee, T.K. and Yamada, K. 1985. The histochemistry of urea-unmasked glycosaminoglycans in the skin of the eel, Anguilla japonica. Histochemistry 82: 39–43.
Benjamin, M. 1988. Mucochondroid (mucous connective) tissues in the heads of teleosts. Anat. Embryol. 178: 461–474.
Benjamin, M. and Ralphs, J.R. 1991. Extracellular matrix of connective tissues in the heads of teleosts. J. Anat. 179: 137–148.
Cheng, C.C. and DeVries, A.L. 1991. The role of antifreeze glycopeptides and peptides in the freezing avoidance of coldwater fish. In Life Under Extreme Conditions: Biochemical Adaptation. pp. 1–14 Edited by G. di Prisco. Springer-Verlag, Berlin.
Comper, W.D. and Laurent, T.C. 1978. Physiological function of connective tissue polysaccharides. Physiol. Rev. 58: 255–315.
Davenport, J. and Kjørsvik, E. 1986. Buoyancy in the lump sucker Cyclopterus lumpus. J. Mar. Biol. Assoc. U.K. 66: 159–174.
Davies, P.L. and Hew, C.L. 1990. Biochemistry of fish antifreeze proteins. FASEB J. 4: 2460–2468.
Davies, P.L., Hew, C.L. and Fletcher, G.L. 1988. Fish antifreeze proteins: physiology and evolutionary biology. Can. J. Zool. 66: 2611–2617.
DeVries, A.L. 1986. Antifreeze glycopeptides and peptides: Interactions with ice and water. In Methods in Enzymology. Vol. 127. Biomembranes, Part O, Protons and Water: Structure and Translocation. pp. 293–303. Edited by L. Packer. Academic Press, Orlando.
DeVries, A.L. 1988. The role of antifreeze glycopeptides and peptides in the freezing avoidance of Antarctic fishes. Comp. Biochem. Physiol. 90B: 611–621.
DeVries, A.L. and Lin, Y. 1977. The role of glycoprotein antifreezes in the survival of Antarctic fishes. In Adaptations Within Antarctic Ecosystems. pp. 439–459. Edited by G.A. Llano. Smithsonian Institution, Washington.
DeWitt, H.H., Heemstra, P.C. and Gon, O. 1990. Nototheniidae. In Fishes of the Southern Ocean. pp 279–331. Edited by O. Gon and P.C. Heemstra. J.L.B. Smith Institute of Ichtyology, Grahamstown.
Dieckmann, G., Rohardt, G., Hellmer, H. and Kipfstuhl, J. 1986. The occurrence of ice platelets at 250 m depth near the Filchner Ice Shelf and its significance for sea ice biology. Deep-Sea Res. 33: 141–148.
Eastman, J.T. and Hikida, R.S. 1991. Skin structure and vascularization in the Antarctic notothenioid fish Gymnodraco acuticeps. J. Morphol. 208: 347–365.
Eastman, J.T., Hikida, R.S. and DeVries, A.L. 1994. Buoyancy studies and microscopy of skin and subdermal extracellular matrix of the Antarctic snailfish, Paraliparis devriesi. J. Morphol. 220: 85–101.
Ewart, K.V. and Fletcher, G.L. 1990. Isolation and characterization of antifreeze proteins from smelt (Osmerus mordax) and Atlantic herring (Clupea harengus harengus). Can. J. Zool. 68: 1652–1658.
Foldvik, A. and Kvinge, T. 1977. Thermohaline convection in the vicinity of an ice shelf. In Polar Oceans. pp. 247–255. Edited by M.J. Dunbar. Arctic Institute of North America, Calgary.
Hayes, P.H., Scott, G.K., Ng, N.F.L., Hew, C.L. and Davies, P.L. 1989. Cystine-rich type II antifreeze protein precursor is initiated from the third AUG codon of its mRNA. J. Biol. Chem. 264: 18761–18767.
Holmes, W.N. and Donaldson, E.M. 1969. The body compartments and the distribution of electrolytes. In Fish Physiology. Vol. 1. Exretion, Ionic Regulation, and Metabolism. pp. 1–89. Edited by W.S. Hoar and D.J. Randall. Academic Press, New York.
Johnson, P. and Saulinskas, E.F. 1993. Sequencing on ProBlott membranes of protein fragments produced in polyacrylamide gels. In Protein Analysis Renaissance. pp. 29–32. Edited by R. Giannella. Applied Biosystems, Foster City.
Kao, M.H., Fletcher, G.L., Wang, N.C. and Hew, C.L. 1986. The relationship between molecular weight and antifreeze activity in marine fish. Can. J. Zool. 64: 578–582.
Lewis, E.L. and Perkin, R.G. 1985. The winter oceanography of McMurdo Sound, Antarctica. In Antarctic Research Series. Vol. 43. Oceanology of the Antarctic Continental Shelf. pp. 145–165. Edited by S.S. Jacobs. American Geophysical Union, Washington.
Littlepage, J.L. 1965. Oceanographic investigations in McMurdo Sound, Antarctica. In Antarctic Research Series. Vol. 5. Biology of the Antarctic Seas II. pp. 1–37. Edited by G.A. Llano. American Geophysical Union, Washington.
McAllister, D.E. and Rees, E.I.S. 1963. A revision of the eelpout genus Melanostigma with a new genus and with comments on Maynea. Bull. Nat. Mus. Can., Contrib. Zool. No. 199: 85–110.
McDonald, D.G. and Milligan, C.L. 1992. Chemical properties of the blood. In Fish physiology. Vol. XII, Part B. The Cardiovascular System. pp. 53–133. Edited by W.S. Hoar, D.J. Randall and A.P. Farrell. Academic Press, San Diego.
Ng, N.F.L. and Hew, C.L. 1992. Structure of an antifreeze polypeptide from the sea raven. J. Biol. Chem. 267: 16069–16075.
Ng, N.F., Trinh, K.-Y. and Hew, C.L. 1986. Structure of an antifreeze polypeptide precursor from the sea raven, Hemitripterus americanus. J. Biol. Chem. 261: 15690–15695.
O'Grady, S.M. and DeVries, A.L. 1982. Osmotic and ionic regulation in polar fishes. J. Exp. Mar. Biol. Ecol. 57: 219–228.
Olson, K.R. 1985. Preparation of fish tissues for electron microscopy. J. Electr. Microscop. Tech. 2: 217–228.
Pfeiler, E. 1986. Towards an explanation of the developmental strategy in leptocephalous larvae of marine teleost fishes. Env. Biol. Fish. 15: 3–13.
Pfeiler, E. 1991. Glycosaminoglycan composition of anguilliform and elopiform leptocephali. J. Fish Biol. 38: 533–540.
Pfeiler, E. 1993. Characterization and distribution of undersulfated chondroitin sulfate and chondroitin in leptocephalous larvae of elopomorph fishes. Fish Physiol. Biochem. 12: 143–148.
Powell, R., Higgins, D.G., Wolff, J., Byrnes, L., Stack, M., Sharp, P.M. and Gannon, F. 1991. The salmon gene encoding apolipoprotein A-1: cDNA sequence, tissue expression and evolution. Gene 104: 155–161.
Raymond, J.A. 1989. Freezing resistance in some northern populations of Pacific herring, Clupea harengus pallasi. Can. J. Fish. Aquat. Sci. 46: 2104–2107.
Stein, D.L. and Andriashev, A.P. 1990. Liparididae. In Fishes of the Southern Ocean. pp. 231–255. Edited by O. Gon and P.C. Heemstra. J.L.B. Smith Institute of Ichthyology, Grahamstown.
Stein, D.L., Meléndez, C.R. and Kong, U.I. 1991. A review of Chilean snailfishes (Liparididae, Scorpaeniformes) with descriptions of a new genus and three new species. Copeia 1991: 358–373.
Valerio, P.F., Kao, M.H. and Fletcher, G.L. 1992. Fish skin: an effective barrier to ice crystal propagation. J. Exp. Biol. 164: 135–151.
Wyckoff, M., Rodbard, D. and Chrambach, A. 1977. Polyacrylamide gel electrophoresis in sodium dodecyl sulfate-containing buffers using multiphasic buffer systems: properties of the stack, valid Rf-measurement and optimized procedure. Anal. Biochem. 78: 459–482.
Yancey, P.H., Lawrence-Berrey, R. and Douglas, M.D. 1989. Adaptations in mesopelagic fishes. I. Buoyant glucosaminoglycan layers in species without diel vertical migrations. Mar. Biol. 103: 453–459.
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Jung, A., Johnson, P., Eastman, J.T. et al. Protein content and freezing avoidance properties of the subdermal extracellular matrix and serum of the Antarctic snailfish, Paraliparis devriesi . Fish Physiol Biochem 14, 71–80 (1995). https://doi.org/10.1007/BF00004292
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DOI: https://doi.org/10.1007/BF00004292