Characterization of an antifreeze protein from the polar diatom Fragilariopsis cylindrus and its relevance in sea ice

Cryobiology

Volumn 63, Issue 3, 2011, Pages 210-219

  Bayer Giraldi, Maddalena ^a   Weikusat, Ilka ^a   Besir, Hüseyin ^b   Dieckmann, Gerhard ^a  

^a ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

AFP; Antifreeze activity; Antifreeze proteins; Crystal habit; Diatoms; Fragilariopsis cylindrus; Ice microstructure; Salt; Sea ice

Indexed keywords

ANTIFREEZE PROTEIN; RECOMBINANT PROTEIN; SODIUM CHLORIDE;

ARTICLE; COLD SENSITIVITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DIATOM; ENVIRONMENTAL EXPOSURE; FRAGILARIOPSIS CYLINDRUS; FREEZING; GROWTH RATE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SALINITY; SEA ICE;

ANTIFREEZE PROTEINS; CLONING, MOLECULAR; COLD CLIMATE; COLD TEMPERATURE; CRYSTALLIZATION; DIATOMS; ESCHERICHIA COLI; FREEZING; ICE COVER; OSMOMETRY; PLASMIDS; PROTEIN ISOFORMS; RECOMBINANT PROTEINS; SALINITY; SALTS; TRANSFORMATION, BACTERIAL;

BACILLARIOPHYTA; FRAGILARIOPSIS CYLINDRUS;

EID: 82155173437     PISSN: 00112240     EISSN: 10902392     Source Type: Journal    
DOI: 10.1016/j.cryobiol.2011.08.006     Document Type: Article

References (77)

1. Aletsee L., Jahnke J. Growth and productivity of the psychrophilic marine diatoms Thalassiosira antarctica Comber and Nitschia firgida Grunow in batch cultures at temperatures below the freezing point of water. Polar Biology 1992, 11:643-647.
2. Amir G., Horowitz L., Rubinsky B., Sheick Yousif B., Lavee J., Smolinsky A.K. Subzero non freezing cryopreservation of rat hearts using antifreeze protein I and antifreeze protein III. Cryobiology 2004, 48:273-282.
3. Baardsnes J., Jelokhani-Niaraki M., Kondejewski L.H., Kuiper M.J., Kay C.M., Hodges R.S., Davies P.L. Antifreeze protein from shorthorn sculpin: identification of the ice-binding surface. Protein Science 2001, 10:2566-2576.
4. Bar M., Celik Y., Fass D., Braslavsky I. Interactions of β-helical antifreeze protein mutants with ice. Crystal Growth and Design 2008, 8:2954-2963.
5. Barrett J. Thermal hysteresis proteins. The International Journal of Biochemistry and Cell Biology 2001, 33:105-117.
6. A. Bartsch, Die Eisalgenflora des Weddelmeeres (Antarktis): Artenzusammensetzung und Biomasse sowie ökophysiologie ausgewählter Arten, Berichte zur Polar- und Meeresforschung/Reports on Polar and Marine Research 63 (1989).
7. Bayer-Giraldi M., Uhlig C., John U., Mock T., Valentin K. Antifreeze proteins in polar sea ice diatoms: diversity and gene expression in the genus Fragilariopsis. Environmental Microbiology 2010, 12:1041-1062.
8. Bendtsen J.D., Nielsen H., Heijne G.V., Brunak S. Improved prediction of signal peptides: SignalP 3.0. Journal of Molecular Biology 2004, 340:783-795.
9. Budke C., Koop T. Ice recrystallization inhibition and molecular recognition of ice faces by poly(vinyl alcohol). ChemPhysChem 2006, 7:2601-2606.
10. Chakrabartty A., Hew C.L. The effect of enhanced α-helicity on the activity of a winter flounder antifreeze polypeptide. European Journal of Biochemistry 1991, 202:1057-1063.
11. Chao H., Davies P.L., Carpenter J.F. Effects of antifreeze proteins on red blood cell survival during cryopreservation. Journal of Experimental Biology 1996, 199:2071-2076.
12. Chao H., Houston M.E.J., Hodges R.S., Kay C.M., Sykes B.D., Loewen M.C., Davies P.L., Sönnichsen F.D. A diminished role for hydrogen bonds in antifreeze protein binding to ice. Biochemistry 1997, 36:14652-14660.
13. Cox G.F.N., Weeks W.F. Equation for determining the gas and brine volumes in sea-ice samples. Journal of Glaciology 1983, 29:306-316.
14. DeLuca C.I., Comley R., Davies P.L. Antifreeze proteins bind independently to ice. Biophysical Journal 1998, 74:1502-1508.
15. Eicken H. The role of sea ice in structuring Antarctic ecosystems. Polar Biology 1992, 12:3-13.
16. Ewart K.V., Lin Q., Hew C.L. Structure, function and evolution of antifreeze proteins. Cellular and Molecular Life Sciences 1999, 55:271-283.
17. Ewert M., Deming J.W. Selective retention in saline ice of extracellular polysaccharides prodiced by the cold-adapted marine strain bacterium Colwellia psychrerythraea strain 34H. Annals of Glaciology 2011, 52:111-117.
18. E. Gasteiger, C. Hoogland, A. Gattiker, S. Duvaud, M.R. Wilkins, R.D. Appel, A. Bairoch, Protein Identification and Analysis Tools on the ExPASy Server, in: J.M. Walker (Ed.), The Proteomics Protoclos Handbook, Humana Press, 2005, pp. 571-607.
19. Gaukel V.G., Spieß W.E.L. EInfluss von Antigefrierproteinen auf die Rekristallisation von Eis in Modelllösungen für Eiskrem. Chemie Ingenieur Technik 2004, 76:454-458.
20. 2+-dependent antifreeze protein in an Antarctic bacterium. FEMS Microbiology Letters 2005, 245:67-72.
21. Gordienko R., Ohno H., Singh V.K., Jia Z., Ripmeester J.A., Walker V.K. Towards a green hydrate inhibitor: imaging antifreeze proteins on clathrates. PLoS ONE 2010, 5:e8953.
22. S.P. Graether, M.J. Kulper, S.M. Gagné, V.K. Walker, Z. Jia, B.D. Sykes, P.L. Davies, b-Helix structure and ice-binding properties of a hyperactive antifreeze protein from an insect, Nature 406 (2000).
23. Griffith M., Ewart V.K. Antifreeze proteins and their potential use in frozen foods. Biotechnology Advances 1995, 13:375-402.
24. Guillard R.R.L., Ryther J.H. Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Canadian Journal of Microbiology 1962, 8:229-239.
25. Günther S., Dieckmann G.S. Vertical zonation and community transition of sea-ice diatoms in fast ice and platelet layer. Weddell Sea, Antarctica, Annals of Glaciology 2001, 33:287-296.
26. Gwak I.G., Jung W.S., Kim H.J., Kang S.-H., Jin E. Antifreeze protein in antarctic marine diatom Chaetoceros neogracile. Marine Biotechnology 2010, 12:630-639.
27. Hagiwara Y., Yamamoto D. Cooperative Effect of Winter Flounder Antifreeze Protein and Ions on the Unidirectional Freezing of their Solution in a Narrow Space, Physics and Chemistry of Ice 2010 2011, Hokkaido University Press, Sapporo, Japan, pp. 313-319.
28. Hoshino T., Kiriaki M., Ohgiya S., Fujiwara M., Kondo H., Nishimiya Y., Yumoto I., Tsuda S. Antifreeze proteins from snow mold fungi. Canadian Journal of Botany/Revue Canadienne de Botanique 2003, 81:1175-1181.
29. IFAM, IFAM Jahresbericht 2006/2007, Fraunhofer-Institut für Fertigungstechnik und Angewandte Materialforschung Bremen.
30. Janech M.G., Krell A., Mock T., Kang J.-S., Raymond J.A. Ice-binding proteins from sea ice diatoms (Bacillariophyceae). Journal of Phycology 2006, 42:410-416.
31. Kayitmazer A.B., Bohidar H.B., Mattison K.W., Bose A., Sarkar J., Hashidzume A., Russo P.S., Jaeger W., Dubin P.L. Mesophase separation and probe dynamics in protein-polyelectrolyte coacervates. Soft Matter 2007, 3:1064-1076.
32. Kiko R. Acquisition of freeze protection in a sea-ice crustacean through horizontal gene transfer?. Polar Biology 2010, 33:543-556.
33. Kipfstuhl S., Hamann I., Lambrecht A., Freitag J., Faria S.H., Grigoriev D., Azuma N. Microstructure mapping: a new method for imaging deformation-induced microstructural features of ice on the grain scale. Journal of Glaciology 2006, 52:398-406.
34. Knight C.A. Adding to the antifreeze agenda. Nature 2000, 406:249-250.
35. Knight C.A., Duman J.A. Inhibition of recrystallization of ice by insect thermal hysteresis proteins: a possible cryoprotective role. Cryobiology 1986, 23:256-262.
36. Krell A., Funck D., Plettner I., John U., Dieckmann G. Regulation of proline metabolism under salt stress in the psychrophilic diatom Fragilariopsis cylindrus (Bacillariophyceae). Journal of Phycology 2007, 43:753-762.
37. Krembs C., Deming J.W. The role of exopolymers in microbial adaptation to sea ice. Psychrophiles: From Biodiversity to Biotechnology 2008, 247-264. Springer Verlag, Berlin. R. Margesin, F. Schinner, J.-C. Marx, C. Gerday (Eds.).
38. Krembs C., Eicken H., Deming J.W. Exopolymer alterations of physical properties of sea ice and implications for ice habitability and biogeochemistry in a warmer Arctic. Proceedings of the National Academy of Science 2011, 108:3653-3658.
39. C. Krembs, H. Eicken, K. Junge, J.W. Deming, High concentrations of exopolymeric substances in Arctic winter sea ice: implications for the polar ocean carbon cycle and cryoprotection of diatoms, Deep Sea Research (Part I, Oceanographic Research Papers) 49 (2002) 2163-2181.
40. Krembs C., Engel A. Abundance and variability of microorganisms and transparent exopolymer particles across ice-water interface of melting first-year sea ice in the Laptev Sea (Arctic). Marine Biology 2001, 138:173-185.
41. Krembs C., Gradinger R., Spindler M. Implication of brine channels geometry and surface area for the interaction of sympagic organisms in Antarctic sea ice. Journal of Experimental Marine Biology and Ecology 2000, 243:55-80.
42. Kristiansen E., Pedersen S.A., Zachariassen K.E. Salt-induced enhancement of antifreeze protein activity: a salting-out effect. Cryobiology 2008, 57:122-129.
43. Kristiansen E., Zachariassen K.E. The mechanism by which fish antifreeze proteins cause thermal hysteresis. Cryobiology 2005, 51:262-280.
44. Lee J.K., Park K.S., Park S., Park H., Song Y.H., Kang S.-H., Kim H.J. An extracellular ice-binding glycoprotein from an Antarctic psychrophilic yeast. Cryobiology 2010, 60:222-228.
45. Li N., Andorfer C.A., Duman J.A. Enhancement of insect antifreeze protein activity by solutes of low molecular mass. The Journal of Experimental Biology 1998, 201:2243-2252.
46. Lizotte M.P. The contributions of sea ice algae to Antarctic marine primary production. American Zoologist 2001, 41:57-73.
47. Marshall C.B., Daley M.E., Sykes B.D., Davies P.L. Enhancing the activity of a β-helical antifreeze protein by the engineered addition of coils. Biochemistry 2004, 43:11637-11646.
48. Marshall C.B., Fletcher G.L., Davies P.L. Hyperactive antifreeze protein in a fish. Nature 2004, 429:153.
49. G.A. Maykut, The surface heat and mass balance, in: N. Untersteiner (Ed.), NATO ASI series, New York Plenum Pr., 1986, pp. 395-463.
50. Mock T., Hoch N. Long-term temperature acclimation of photosynthesis in steady-state cultures of the polar diatom Fragilariopsis cylindrus. Photosynthesis Research 2005, 85:307-317.
51. Mock T., Krell A., Glöckner G., Kolukisaoglu Ü., Valentin K. Analysis of expressed sequence tags (ESTs) from the polar diatom Fragilariopsis cylindrus. Journal of Phycology 2006, 42:78-85.
52. Mock T., Valentin K. Photosynthesis and cold acclimation: molecular evidence from a polar diatom. Journal of Phycology 2004, 40:732-741.
53. Mok Y.-F., Lin F.-H., Graham L.A., Celik Y., Braslavsky I., Davies P.L. Structural basis for the superior activity of the large isoform of snow flea antifreeze protein. Biochemistry 2010, 49:2593-2603.
54. Mugnano J.A., Wang T., Layne J.R., DeVries A.L., Lee R.E.J. Antifreeze glycoproteins promote intracellular freezing of rat cardiomyocytes at high subzero temperatures. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 1995, 269:R474-R479.
55. Payne S.R., Young O.A. Effects of pre-slaughter administration of antifreeze proteins on frozen meat quality. Meat Science 1995, 41:147-155.
56. Petrich C., Eicken H. Growth, structure and properties of sea ice. Sea Ice 2010, 23-77. Wiley-Blackwell, Chichester. D.N. Thomas, G. Dieckmann (Eds.).
57. Poulin M. Ice diatoms: the Arctic. Polar Marine Diatoms 1990, 15-18. British Antarctic Survey, Cambridge. L.K. Medlin, J. Priddle (Eds.).
58. Raymond J.A., Christner B.C., Schuster S.C. A bacterial ice-binding protein from the Vostok ice core. Extremophiles 2008, 12:713-717.
59. Raymond J.A., DeVries A.L. Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proceedings of the National Academy of Sciences, USA 1977, 74:2589-2593.
60. Raymond J.A., Fritsen C. Semipurification and ice recrystallization inhibition activity of ice-active substances associated with antarctic photosynthetic organisms. Cryobiology 2001, 43:63-70.
61. Raymond J.A., Fritsen C., Shen K. An ice-binding protein from an Antarctic sea ice bacterium. FEMS Microbiology Ecology 2007, 61:214-221.
62. Raymond J.A., Janech M.G. Ice-binding proteins from enoki and shiitake mushrooms. Cryobiology 2009, 58:151-156.
63. Raymond J.A., Wilson P., DeVries A.L. Inhibition of growth of nonbasal planes in ice by fish antifreezes. Proceedings of the National Academy of Sciences, USA 1989, 86:881-885.
64. Reverter D., Lima C.D. Structural basis for SENP2 protease interactions with SUMO precursors and conjugated substrates. Nature Structural and Molecular Biology 2006, 13:1060-1068.
65. Riebesell U., Schloss I., Smetack V. Aggregation of algae released from melting sea ice. Implications for seeding and sedimentation. Polar Biology 1991, 11:239-248.
66. Riedel A., Michel C., Gosselin M. Seasonal study of sea-ice exopolymeric substances on the Mackenzie shelf: implications for transport of sea-ice bacteria and algae. Aquatic Microbial Ecology 2006, 45:195-206.
67. Riedel A., Michel C., Gosselin M., LeBlanc B. Enrichment of nutrients, exoplymeric substances and microorganisms in newly formed sea ice on the Mackenzie shelf. Marine Ecology Progress Series 2007, 342:55-67.
68. Schägger H., von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamdie gel electrophoresis for the separation of protein in the range from 1 to 100kDa. Analytical Biochemistry 1987, 166:368-379.
69. Schrag J.D., O'Grady S.M., DeVries A.L. Relationship of amino acid composition and moleculra weight of antifreeze glycopeptides to non-colligative freezing point depression. Biochimica et Biophysica Acta 1982, 717:322-326.
70. Scotter A.J., Marshall C.B., Graham L.A., Gilbert J.A., Garnham C.P., Davies P.L. The basis for hyperactivity of antifreeze proteins. Cryobiology 2006, 53:229-239.
71. Sidebottom C., Buckley S., Pudney P., Twigg S., Jarman C., Holt C., Telford J., McArthur A., Worrall D., Hubbard R., Lillford P. Phytochemistry: heat-stable antifreeze protein from grass. Nature 2000, 406:256.
72. Smallwood M., Worrall D., Byass L., Elias L., Ashford D., Doucet C.J., Holt C., Telford L., Lillford P., Bowles D.J. Isolation and characterization of a novel antifreeze protein from carrot (Daucus carota). Biochemical Journal 1999, 340:385-391.
73. Tomczak M.M., Marshall C.B., Gilbert J.A., Davies P.L. A facile method for determining ice recrystallization inhibition by antifreeze proteins. Biochemical and Biophysical Research Communications 2003, 311:1041-1046.
74. Venketesh S., Dayananda C. Properties, potentials, and prospects of antifreeze proteins. Critical Reviews in Biotechnology 2008, 28:57-82.
75. Wilen L.A., Diprinzio C.L., Alley R.B., Azuma N. Development, principles, and applications of automated ice fabric analyzers. Microscopy Research and Technique 2003, 62:2-18.
76. Wu Y., Banoub J., Goddard S.V., Kao M.H., Fletcher G.L. Antifreeze glycoproteins: relationship between molecular weight Thermal hysteresis and the inhibition of leakage from liposomes during thermotropic phase transition. Comparative Biochemistry and Physiology B: Biochemistry and Molecular Biology 2001, 128:265-273.
77. Xiao N., Suzuki K., Nishimiya Y., Kondo H., Miura A., Tsuda S., Hoshino T. Comparison of functional properties of two fungal antifreeze proteins from Antarctomyces psychotrophicus and Typhula ishikariensis. FEBS Journal 2010, 277:394-403.