About this Journal Submit a Manuscript Table of Contents
Scientifica
Volume 2014 (2014), Article ID 976895, 20 pages
http://dx.doi.org/10.1155/2014/976895
Review Article

Bacterial Ice Crystal Controlling Proteins

Department of Biology, University of Waterloo, Waterloo, ON, Canada N2L 3G1

Received 26 November 2013; Accepted 15 December 2013; Published 20 January 2014

Academic Editors: G. Berta and L. Chistoserdova

Copyright © 2014 Janet S. H. Lorv et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. Kawahara, “Cryoprotectants and ice-binding proteins,” in Psychrophiles: From Biodiversity to Biotechnology, pp. 229–246, Springer, Heidelberg, Germany, 2008.
  2. N. Smolin and V. Daggett, “Formation of ice-like water structure on the surface of an antifreeze protein,” Journal of Physical Chemistry B, vol. 112, no. 19, pp. 6193–6202, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. V. Bouvet and R. N. Ben, “Antifreeze glycoproteins: structure, conformation, and biological applications,” Cell Biochemistry and Biophysics, vol. 39, no. 2, pp. 133–144, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. X. Sun, M. Griffith, J. J. Pasternak, and B. R. Glick, “Low temperature growth, freezing survival, and production of antifreeze protein by the plant growth promoting rhizobacterium Pseudomonas putida GR12-2,” Canadian Journal of Microbiology, vol. 41, no. 9, pp. 776–784, 1995. View at Scopus
  5. R. Margesin and V. Miteva, “Diversity and ecology of psychrophilic microorganisms,” Research in Microbiology, vol. 162, no. 3, pp. 346–361, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. S. L. Wilson and V. K. Walker, “Selection of low-temperature resistance in bacteria and potential applications,” Environmental Technology, vol. 31, no. 8-9, pp. 943–956, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Xu, M. Griffith, C. L. Patten, and B. R. Glick, “Isolation and characterization of an antifreeze protein with ice nucleation activity from the plant growth promoting rhizobacterium Pseudomonas putida GR12-2,” Canadian Journal of Microbiology, vol. 44, no. 1, pp. 64–73, 1998. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Griffith and K. V. Ewart, “Antifreeze proteins and their potential use in frozen foods,” Biotechnology Advances, vol. 13, no. 3, pp. 375–402, 1995. View at Scopus
  9. R. N. Ben, “Antifreeze glycoproteins—preventing the growth of ice,” ChemBioChem, vol. 2, no. 3, pp. 161–166, 2001. View at Scopus
  10. S. P. Graether and Z. Jia, “Modeling Pseudomonas syringae ice-nucleation protein as a β-helical protein,” Biophysical Journal, vol. 80, no. 3, pp. 1169–1173, 2001. View at Scopus
  11. N. Muryoi, M. Sato, S. Kaneko et al., “Cloning and expression of afpA, a gene encoding an antifreeze protein from the arctic plant growth-promoting rhizobacterium Pseudomonas putida GR12-2,” Journal of Bacteriology, vol. 186, no. 17, pp. 5661–5671, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. N. Du, X. Y. Liu, and C. L. Hew, “Aggregation of antifreeze protein and impact on antifreeze activity,” Journal of Physical Chemistry B, vol. 110, no. 41, pp. 20562–20567, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. C. P. Garnham, R. L. Campbell, V. K. Walker, and P. L. Davies, “Novel dimeric β-helical model of an ice nucleation protein with bridged active sites,” BMC Structural Biology, vol. 11, article 36, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. H. Kawahara, Y. Nakano, K. Omiya, N. Muryoi, J. Nishikawa, and H. Obata, “Production of two types of ice crystal-controlling proteins in antarctic bacterium,” Journal of Bioscience and Bioengineering, vol. 98, no. 3, pp. 220–223, 2004. View at Scopus
  15. S. L. Wilson, D. L. Kelley, and V. K. Walker, “Ice-active characteristics of soil bacteria selected by ice-affinity,” Environmental Microbiology, vol. 8, no. 10, pp. 1816–1824, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. J. A. Raymond and A. L. DeVries, “Adsorption inhibition as a mechanism of freezing resistance in polar fishes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 74, no. 6, pp. 2589–2593, 1977. View at Scopus
  17. C. P. Garnham, R. L. Campbell, and P. L. Davies, “Anchored clathrate waters bind antifreeze proteins to ice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 18, pp. 7363–7367, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. J. A. Gilbert, P. J. Hill, C. E. R. Dodd, and J. Laybourn-Parry, “Demonstration of antifreeze protein activity in Antarctic lake bacteria,” Microbiology, vol. 150, no. 1, pp. 171–180, 2004. View at Scopus
  19. H. Kondo, Y. Hanada, H. Sugimoto et al., “Ice-binding site of snow mold fungus antifreeze protein deviates from structural regularity and high conservation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 24, pp. 9360–9365, 2012.
  20. Y. Celik, L. A. Graham, Y.-F. Mok, M. Bar, P. L. Davies, and I. Braslavsky, “Superheating of ice crystals in antifreeze protein solutions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 12, pp. 5423–5428, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. J. A. Gilbert, P. L. Davies, and J. Laybourn-Parry, “A hyperactive, Ca2+-dependent antifreeze protein in an Antarctic bacterium,” FEMS Microbiology Letters, vol. 245, no. 1, pp. 67–72, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. A. J. Scotter, C. B. Marshall, L. A. Graham, J. A. Gilbert, C. P. Garnham, and P. L. Davies, “The basis for hyperactivity of antifreeze proteins,” Cryobiology, vol. 53, no. 2, pp. 229–239, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. D. Doucet, M. G. Tyshenko, M. J. Kuiper et al., “Structure-function relationships in spruce budworm antifreeze protein revealed by isoform diversity,” European Journal of Biochemistry, vol. 267, no. 19, pp. 6082–6088, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Sidebottom, S. Buckley, P. Pudney et al., “Heat-stable antifreeze protein from grass,” Nature, vol. 406, no. 6793, p. 256, 2000. View at Publisher · View at Google Scholar · View at Scopus
  25. Y.-F. Mok, F.-H. Lin, L. A. Graham, Y. Celik, I. Braslavsky, and P. L. Davies, “Structural basis for the superior activity of the large isoform of snow flea antifreeze protein,” Biochemistry, vol. 49, no. 11, pp. 2593–2603, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. F.-H. Lin, T. Sun, G. L. Fletcher, and P. L. Davies, “Thermolabile antifreeze protein produced in Escherichia coli for structural analysis,” Protein Expression and Purification, vol. 82, no. 1, pp. 75–82, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. R. S. Hobbs, M. A. Shears, L. A. Graham, P. L. Davies, and G. L. Fletcher, “Isolation and characterization of type i antifreeze proteins from cunner, Tautogolabrus adspersus, order Perciformes,” FEBS Journal, vol. 278, no. 19, pp. 3699–3710, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. C. P. Garnham, J. A. Gilbert, C. P. Hartman, R. L. Campbell, J. Laybourn-Parry, and P. L. Davies, “A Ca2+-dependent bacterial antifreeze protein domain has a novel β-helical ice-binding fold,” Biochemical Journal, vol. 411, no. 1, pp. 171–180, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. A. J. Middleton, C. B. Marshall, F. Faucher et al., “Antifreeze protein from freeze-tolerant grass has a beta-roll fold with an irregularly structured ice-binding site,” Journal of Molecular Biology, vol. 416, no. 5, pp. 713–724, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. S. O. Yu, A. Brown, A. J. Middleton, M. M. Tomczak, V. K. Walker, and P. L. Davies, “Ice restructuring inhibition activities in antifreeze proteins with distinct differences in thermal hysteresis,” Cryobiology, vol. 61, no. 3, pp. 327–334, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. Q. Li, Q. Yan, J. Chen et al., “Molecular characterization of an ice nucleation protein variant (InaQ) from Pseudomonas syringae and the analysis of its transmembrane transport activity in Escherichia coli,” International Journal of Biological Sciences, vol. 8, no. 8, 2012.
  32. J. Barrett, “Thermal hysteresis proteins,” International Journal of Biochemistry and Cell Biology, vol. 33, no. 2, pp. 105–117, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. Z. Cheng, E. Park, and B. R. Glick, “1-Aminocyclopropane-1-carboxylate deaminase from Pseudomonas putida UW4 facilitates the growth of canola in the presence of salt,” Canadian Journal of Microbiology, vol. 53, no. 7, pp. 912–918, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Kawahara, Y. Iwanaka, S. Higa et al., “A novel, intracellular antifreeze protein in an antarctic bacterium, Flavobacterium xanthum,” Cryo-Letters, vol. 28, no. 1, pp. 39–49, 2007. View at Scopus
  35. Y. Yamashita, N. Nakamura, K. Omiya, J. Nishikawa, H. Kawahara, and H. Obata, “Identification of an antifreeze lipoprotein from Moraxella sp. of Antarctic origin,” Bioscience, Biotechnology and Biochemistry, vol. 66, no. 2, pp. 239–247, 2002. View at Scopus
  36. V. K. Walker, G. R. Palmer, and G. Voordouw, “Freeze-thaw tolerance and clues to the winter survival of a soil community,” Applied and Environmental Microbiology, vol. 72, no. 3, pp. 1784–1792, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. J. G. Duman and T. M. Olsen, “Thermal hysteresis protein activity in bacteria, fungi, and phylogenetically diverse plants,” Cryobiology, vol. 30, no. 3, pp. 322–328, 1993. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Guo, C. P. Garnham, J. C. Whitney, L. A. Graham, and P. L. Davies, “Re-evaluation of a bacterial antifreeze protein as an adhesin with ice-binding activity,” PLoS ONE, vol. 7, no. 11, Article ID e48805, 2012.
  39. J. Duan, W. Jiang, Z. Cheng, J. J. Heikkila, and B. R. Glick, “The complete genome sequence of the plant growth-promoting bacterium Pseudomonas sp. UW4,” PLoS ONE, vol. 8, no. 3, Article ID e58640, 2013.
  40. Z. Wu, F. W. K. Kan, Y. M. She, and V. K. Walker, “Biofilm, ice recrystallization inhibition and freeze-thaw protection in an epiphyte community,” Applied Biochemistry and Microbiology, vol. 48, no. 4, pp. 363–370, 2012.
  41. S. L. Wilson, P. Grogan, and V. K. Walker, “Prospecting for ice association: characterization of freeze-thaw selected enrichment cultures from latitudinally distant soils,” Canadian Journal of Microbiology, vol. 58, no. 4, pp. 402–412, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Kajava and S. E. Lindow, “A model of the three-dimensional structure of ice nucleation proteins,” Journal of Molecular Biology, vol. 232, no. 3, pp. 709–717, 1993. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Hartmann, S. Augustin, T. Clauss et al., “Immersion freezing of ice nucleation active protein complexes,” Atmospheric Chemistry and Physics, vol. 13, no. 11, pp. 5751–5766, 2013.
  44. M. A. Turner, F. Arellano, and L. M. Kozloff, “Components of ice nucleation structures of bacteria,” Journal of Bacteriology, vol. 173, no. 20, pp. 6515–6527, 1991. View at Scopus
  45. L. M. Kozloff, M. A. Turner, F. Arellano, and M. Lute, “Phosphatidylinositol, a phospholipid of ice-nucleating bacteria,” Journal of Bacteriology, vol. 173, no. 6, pp. 2053–2060, 1991. View at Scopus
  46. L. R. Maki, E. L. Galyan, M. M. Chang-Chien, and D. R. Caldwell, “Ice nucleation induced by Pseudomonas syringae,” Applied Microbiology, vol. 28, no. 3, pp. 456–459, 1974. View at Scopus
  47. Z. Wu, L. Qin, and V. K. Walker, “Characterization and recombinant expression of a divergent ice nucleation protein from ‘Pseudomonas borealis’,” Microbiology, vol. 155, no. 4, pp. 1164–1169, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. P. Phelps, T. H. Giddings, M. Prochoda, and R. Fall, “Release of cell-free ice nuclei by Erwinia herbicola,” Journal of Bacteriology, vol. 167, no. 2, pp. 496–502, 1986. View at Scopus
  49. H. Kawahara, Y. Mano, and H. Obata, “Purification and characterization of extracellular ice-nucleating matter from Erwinia uredovora KUIN-3,” Bioscience, Biotechnology, and Biochemistry, vol. 57, no. 9, pp. 1429–1432, 1993.
  50. S. Fukuoka, H. Kamishima, E. Tamiya, and I. Karube, “Spontaneous release of outer-membrane vesicles by Erwinia Carotovora,” Microbios, vol. 72, no. 292-93, pp. 167–173, 1992.
  51. H. Obata, T. Tanaka, H. Kawahara, and T. Tokuyama, “Properties of cell-free ice nuclei from ice nucleation-active Pseudomonas fluorescens KUIN-1,” Journal of Fermentation and Bioengineering, vol. 76, no. 1, pp. 19–24, 1993. View at Publisher · View at Google Scholar · View at Scopus
  52. N. Muryoi, K. Matsukawa, K. Yamade, H. Kawahara, and H. Obata, “Purification and properties of an ice-nucleating protein from an ice-nucleating bacterium, Pantoea ananatis KUIN-3,” Journal of Bioscience and Bioengineering, vol. 95, no. 2, pp. 157–163, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. H. Nada, S. Zepeda, H. Miura, and Y. Furukawa, “Significant alterations in anisotropic ice growth rate induced by the ice nucleation-active bacteria Xanthomonas campestris,” Chemical Physics Letters, vol. 498, no. 1–3, pp. 101–106, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. A. M. Anesio and J. Laybourn-Parry, “Glaciers and ice sheets as a biome,” Trends in Ecology and Evolution, vol. 27, no. 4, pp. 219–225, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Junge and B. D. Swanson, “High-resolution ice nucleation spectra of sea-ice bacteria: implications for cloud formation and life in frozen environments,” Biogeosciences, vol. 5, no. 3, pp. 865–873, 2008. View at Scopus
  56. V. I. Miteva, P. P. Sheridan, and J. E. Brenchley, “Phylogenetic and physiological diversity of microorganisms isolated from a deep greenland glacier ice core,” Applied and Environmental Microbiology, vol. 70, no. 1, pp. 202–213, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. M. A. Cambours, P. Nejad, U. Granhall, and M. Ramstedt, “Frost-related dieback of willows. Comparison of epiphytically and endophytically isolated bacteria from different Salix clones, with emphasis on ice nucleation activity, pathogenic properties and seasonal variation,” Biomass and Bioenergy, vol. 28, no. 1, pp. 15–27, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. R. D. O'Brien and S. E. Lindow, “Effect of plant species and environmental conditions on ice nucleation activity of Pseudomonas syringae on leaves,” Applied and Environmental Microbiology, vol. 54, no. 9, pp. 2281–2286, 1988.
  59. S. S. Hirano and C. D. Upper, “Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae—a pathogen, ice nucleus, and epiphyte,” Microbiology and Molecular Biology Reviews, vol. 64, no. 3, pp. 624–653, 2000. View at Scopus
  60. A. Nicolai, P. Vernon, M. Lee, A. Ansart, and M. Charrier, “Supercooling ability in two populations of the land snail Helix pomatia (Gastropoda: Helicidae) and ice-nucleating activity of gut bacteria,” Cryobiology, vol. 50, no. 1, pp. 48–57, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. C. Tang, F. Sun, and T. Zhao, “Construction of ice nucleation active Enterobacter cloacae for control of insect pests,” Chinese Science Bulletin, vol. 48, no. 2, pp. 175–180, 2003. View at Publisher · View at Google Scholar · View at Scopus
  62. C. Tang, F. Sun, X. Zhang, T. Zhao, and J. Qi, “Transgenic ice nucleation-active Enterobacter cloacae reduces cold hardiness of corn borer and cotton bollworm larvae,” FEMS Microbiology Ecology, vol. 51, no. 1, pp. 79–86, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. N. Cochet and P. Widehem, “Ice crystallization by Pseudomonas syringae,” Applied Microbiology and Biotechnology, vol. 54, no. 2, pp. 153–161, 2000. View at Publisher · View at Google Scholar · View at Scopus
  64. J. A. Anderson and E. N. Ashworth, “The effects of streptomycin, desiccation, and uv radiation on ice nucleation by Pseudomonas viridiflava,” Plant Physiology, vol. 80, no. 4, pp. 956–960, 1986.
  65. E. Attard, H. Yang, A. Delort et al., “Effects of atmospheric conditions on ice nucleation activity of Pseudomonas,” Atmospheric Chemistry and Physics Discussions, vol. 12, no. 4, pp. 9491–9516, 2012.
  66. O. Möhler, D. G. Georgakopoulos, C. E. Morris et al., “Heterogeneous ice nucleation activity of bacteria: new laboratory experiments at simulated cloud conditions,” Biogeosciences, vol. 5, no. 5, pp. 1425–1435, 2008. View at Scopus
  67. D. E. Waturangi, “Distribution of ice nucleation-active (INA) bacteria from rain-water and air,” HAYATI Journal of Biosciences, vol. 18, no. 3, 2011.
  68. A. L. Savvides, C. P. Andriopoulos, K. K. Kormas, D. G. Hatzinikolaou, E. A. Katsifas, and A. D. Karagouni, “Selective isolation of indigenous Pseudomonas syringae strains with ice nucleation activity properties from a ski resort,” Journal of Biological Research, vol. 15, pp. 67–73, 2011. View at Scopus
  69. M. Joly, E. Attard, M. Sancelme et al., “Ice nucleation activity of bacteria isolated from cloud water,” Atmospheric Environment, vol. 70, pp. 392–400, 2013.
  70. T. J. Near, A. Dornburg, K. L. Kuhn et al., “Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 9, pp. 3434–3439, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. C. P. Garnham, A. Natarajan, A. J. Middleton, M. J. Kuiper, I. Braslavsky, and P. L. Davies, “Compound ice-binding site of an antifreeze protein revealed by mutagenesis and fluorescent tagging,” Biochemistry, vol. 49, no. 42, pp. 9063–9071, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. K. Modig, J. Qvist, C. B. Marshall, P. L. Davies, and B. Halle, “High water mobility on the ice-binding surface of a hyperactive antifreeze protein,” Physical Chemistry Chemical Physics, vol. 12, no. 35, pp. 10189–10197, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. C. P. Garnham, Y. Nishimiya, S. Tsuda, and P. L. Davies, “Engineering a naturally inactive isoform of type III antifreeze protein into one that can stop the growth of ice,” FEBS Letters, vol. 586, no. 21, pp. 3876–3881, 2012.
  74. N. Pertaya, C. B. Marshall, C. L. DiPrinzio et al., “Fluorescence microscopy evidence for quasi-permanent attachment of antifreeze proteins to ice surfaces,” Biophysical Journal, vol. 92, no. 10, pp. 3663–3673, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. P. W. Wilson, “Explaining thermal hysteresis by the Kelvin effect,” Cryo-Letters, vol. 14, pp. 31–36, 1993.
  76. S. N. Patel and S. P. Graether, “Structures and ice-binding faces of the alaninerich type I antifreeze proteins,” Biochemistry and Cell Biology, vol. 88, no. 2, pp. 223–229, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. Z. Jia and P. L. Davies, “Antifreeze proteins: an unusual receptor-ligand interaction,” Trends in Biochemical Sciences, vol. 27, no. 2, pp. 101–106, 2002. View at Publisher · View at Google Scholar · View at Scopus
  78. Z. Jia, C. I. DeLuca, H. Chao, and P. L. Davies, “Structural basis for the binding of a globular antifreeze protein to ice,” Nature, vol. 384, no. 6606, pp. 285–288, 1996. View at Publisher · View at Google Scholar · View at Scopus
  79. A. C. Doxey, M. W. Yaish, M. Griffith, and B. J. McConkey, “Ordered surface carbons distinguish antifreeze proteins and their ice-binding regions,” Nature Biotechnology, vol. 24, no. 7, pp. 852–855, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. K. K. Kandaswamy, K.-C. Chou, T. Martinetz et al., “AFP-Pred: a random forest approach for predicting antifreeze proteins from sequence-derived properties,” Journal of Theoretical Biology, vol. 270, no. 1, pp. 56–62, 2011. View at Publisher · View at Google Scholar · View at Scopus
  81. A. G. Govindarajan and S. E. Lindow, “Phospholipid requirement for expression of ice nuclei in Pseudomonas syringae and in vitro,” Journal of Biological Chemistry, vol. 263, no. 19, pp. 9333–9338, 1988. View at Scopus
  82. E. Sarron, N. Cochet, and P. Gadonna-Widehem, “Effects of aqueous ozone on Pseudomonas syringae viability and ice nucleating activity,” Process Biochemistry, vol. 48, no. 7, pp. 1004–1009, 2013.
  83. F. Yu, X. Liu, Y. Tao, and K. Zhu, “High saturated fatty acids proportion in Escherichia coli enhances the activity of ice-nucleation protein from Pantoea ananatis,” FEMS Microbiology Letters, vol. 345, no. 2, pp. 141–146, 2013.
  84. Y. Kumaki, K. Kawano, K. Hikichi, T. Matsumoto, and N. Matsushima, “A circular loop of the 16-residue repeating unit in ice nucleation protein,” Biochemical and Biophysical Research Communications, vol. 371, no. 1, pp. 5–9, 2008. View at Publisher · View at Google Scholar · View at Scopus
  85. A. Hakim, J. B. Nguyen, K. Basu et al., “Crystal structure of an insect antifreeze protein and its implications for ice binding,” Journal of Biological Chemistry, 2013. View at Publisher · View at Google Scholar
  86. H. Kawahara, J. Li, M. Griffith, and B. R. Glick, “Relationship between antifreeze protein and freezing resistance in Pseudomonas putida GR12-2,” Current Microbiology, vol. 43, no. 5, pp. 365–370, 2001. View at Publisher · View at Google Scholar · View at Scopus
  87. M. Nemecek-Marshall, R. LaDuca, and R. Fall, “High-level expression of ice nuclei in a Pseudomonas syringae strain is induced by nutrient limitation and low temperature,” Journal of Bacteriology, vol. 175, no. 13, pp. 4062–4070, 1993. View at Scopus
  88. M.-L. Chen, T.-K. Chiou, C.-Y. Tsao, and S.-T. Jiang, “Enhancement of the expression of ice-nucleation activity of Pseudomonas fluorescens MACK-4 isolated from mackerel,” Fisheries Science, vol. 69, no. 1, pp. 195–203, 2003. View at Publisher · View at Google Scholar · View at Scopus
  89. S. Shivaji and J. S. S. Prakash, “How do bacteria sense and respond to low temperature?” Archives of Microbiology, vol. 192, no. 2, pp. 85–95, 2010. View at Publisher · View at Google Scholar · View at Scopus
  90. J. W. Jo, B. C. Jee, J. R. Lee, and C. S. Suh, “Effect of antifreeze protein supplementation in vitrification medium on mouse oocyte developmental competence,” Fertility and Sterility, vol. 96, no. 5, pp. 1239–1245, 2011. View at Publisher · View at Google Scholar · View at Scopus
  91. S. Lee, H. Koh, J. Lee, S. Kang, and H. Kim, “Cryopreservative effects of the recombinant ice-binding protein from the arctic yeast Leucosporidium sp. on red blood cells,” Applied Biochemistry and Biotechnology, vol. 167, no. 4, pp. 824–834, 2012.
  92. K. Muldrew, J. Rewcastle, B. J. Donnelly et al., “Flounder antifreeze peptides increase the efficacy of cryosurgery,” Cryobiology, vol. 42, no. 3, pp. 182–189, 2001. View at Publisher · View at Google Scholar · View at Scopus
  93. H. Koushafar and B. Rubinsky, “Effect of anti freeze proteins on frozen primary prostatic adenocarcinoma cells,” Urology, vol. 49, no. 3, pp. 421–425, 1997. View at Publisher · View at Google Scholar · View at Scopus
  94. S. R. Payne and O. A. Young, “Effects of pre-slaughter administration of antifreeze proteins on frozen meat quality,” Meat Science, vol. 41, no. 2, pp. 147–155, 1995. View at Scopus
  95. R. E. Feeney and Y. Yeh, “Antifreeze proteins: current status and possible food uses,” Trends in Food Science and Technology, vol. 9, no. 3, pp. 102–106, 1998. View at Publisher · View at Google Scholar · View at Scopus
  96. C. Zhang, H. Zhang, L. Wang, H. Gao, N. G. Xiao, and Y. Y. Hui, “Improvement of texture properties and flavor of frozen dough by carrot (Daucus carota) antifreeze protein supplementation,” Journal of Agricultural and Food Chemistry, vol. 55, no. 23, pp. 9620–9626, 2007. View at Publisher · View at Google Scholar · View at Scopus
  97. A. P. Esser-Kahn, V. Trang, and M. B. Francis, “Incorporation of antifreeze proteins into polymer coatings using site-selective bioconjugation,” Journal of the American Chemical Society, vol. 132, no. 38, pp. 13264–13269, 2010. View at Publisher · View at Google Scholar · View at Scopus
  98. H. Ohno, R. Susilo, R. Gordienko, J. Ripmeester, and V. K. Walker, “Interaction of antifreeze proteins with hydrocarbon hydrates,” Chemistry, vol. 16, no. 34, pp. 10409–10417, 2010. View at Publisher · View at Google Scholar · View at Scopus
  99. J. S. Rosen, M. D. Szkutak, S. M. Jaskolka, M. S. Connolly, and K. A. Notarianni, “Engineering performance of water mist fire protection systems with antifreeze,” Journal of Fire Protection Engineering, vol. 23, no. 3, pp. 190–225, 2013.
  100. J. Li, M. P. Izquierdo, and T.-C. Lee, “Effects of ice-nucleation active bacteria on the freezing of some model food systems,” International Journal of Food Science and Technology, vol. 32, no. 1, pp. 41–49, 1997. View at Scopus
  101. M. A. A. Sarhan, “Ice nucleation protein as a bacterial surface display protein,” Archives of Biological Sciences, vol. 63, no. 4, pp. 943–948, 2011. View at Publisher · View at Google Scholar · View at Scopus
  102. S. Manulis, A. Haviv-Chesner, M. T. Brandl, S. E. Lindow, and I. Barash, “Differential involvement of indole-3-acetic acid biosynthetic pathways in pathogenicity and epiphytic fitness of Erwinia herbicola pv. gypsophilae,” Molecular Plant-Microbe Interactions, vol. 11, no. 7, pp. 634–642, 1998. View at Scopus
  103. P. B. Lindgren, R. Frederick, A. G. Govindarajan, N. J. Panopoulos, B. J. Staskawicz, and S. E. Lindow, “An ice nucleation reporter gene system: identification of inducible pathogenicity genes in Pseudomonas syringae pv. phaseolicola,” EMBO Journal, vol. 8, no. 5, pp. 1291–1301, 1989. View at Scopus
  104. K. Abe, S. Watabe, Y. Emori, M. Watanabe, and S. Arai, “An ice nucleation active gene of Erwinia ananas. Sequence similarity to those of Pseudomonas species and regions required for ice nucleation activity,” FEBS Letters, vol. 258, no. 2, pp. 297–300, 1989. View at Publisher · View at Google Scholar · View at Scopus
  105. G. Warren and L. Corotto, “The consensus sequence of ice nucleation proteins from Erwinia herbicola, Pseudomonas fluorescens and Pseudomonas syringae,” Gene, vol. 85, no. 1, pp. 239–242, 1989. View at Publisher · View at Google Scholar · View at Scopus
  106. H. Obata, N. Muryoi, H. Kawahara, K. Yamade, and J. Nishikawa, “Identification of a novel ice-nucleating bacterium of antarctic origin and its ice nucleation properties,” Cryobiology, vol. 38, no. 2, pp. 131–139, 1999. View at Publisher · View at Google Scholar · View at Scopus
  107. A. Hazra, M. Saha, U. K. De, J. Mukherjee, and K. Goswami, “Study of ice nucleating characteristics of Pseudomonas aeruginosa,” Journal of Aerosol Science, vol. 35, no. 11, pp. 1405–1414, 2004. View at Publisher · View at Google Scholar · View at Scopus
  108. G. Warren, L. Corotto, and P. Wolber, “Conserved repeats in diverged ice nucleation structural genes from two species of Pseudomonas,” Nucleic Acids Research, vol. 14, no. 20, pp. 8047–8060, 1986. View at Publisher · View at Google Scholar · View at Scopus
  109. R. L. Green and G. J. Warren, “Physical and functional repetition in a bacterial ice nucleation gene,” Nature, vol. 317, no. 6038, pp. 645–648, 1985. View at Scopus
  110. Y. Michigami, K. Abe, H. Obata, and S. Arai, “Significance of the C-terminal domain of Erwinia uredovora ice nucleation-active protein (Ina U),” Journal of Biochemistry, vol. 118, no. 6, pp. 1279–1284, 1995. View at Scopus
  111. J. Zhao and C. S. Orser, “Conserved repetition in the ice nucleation gene inaX from Xanthomonas campestris pv. translucens,” Molecular and General Genetics, vol. 223, no. 1, pp. 163–166, 1990. View at Publisher · View at Google Scholar · View at Scopus
  112. J. A. Raymond, C. Fritsen, and K. Shen, “An ice-binding protein from an Antarctic sea ice bacterium,” FEMS Microbiology Ecology, vol. 61, no. 2, pp. 214–221, 2007. View at Publisher · View at Google Scholar · View at Scopus