Skip to main content

Cryoprotectants and Ice-Binding Proteins

  • Chapter

Some bacteria have developed a variety of strategies to survive and colonize extremely cold environments such as the Antarctic and the Arctic (Russell 1997; Chattopadhyay 2006). In these frozen environments, bacteria are exposed to conditions that necessitate the partial removal of water from the intracellular space in order to maintain the structure and function of the cell. As water is essential for the function of various macromolecular structures, i.e. proteins, polysaccharides, lipids, and nucleic acids, any significant deviation in the accessibility of water due to dehydration, desiccation or the alteration of its physical state, from the aqueous phase to an ice crystal, will pose a severe threat to the normal function and survival of organisms (Beall 1983).

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD   169.99
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

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abe K, Watabe S, Emori Y, Watanabe M, Arai S (1989) An ice nucleation active gene of Erwinia ananas. FEBS Lett 258:297–300.

    Article  CAS  PubMed  Google Scholar 

  • Anderson JO, Nath J, Harner EJ (1978) Effect of freeze preservation on some pollen enzyme. II. Freezing and freeze-drying stresses. Cryobiology 15:468–477.

    Google Scholar 

  • Arai S, Watanabe M (1985) The protein that prevent the formation of ice nuclei. Kagaku To Seibutsu 23:363–373 (in Japanese).

    Google Scholar 

  • Barrett J (2001) Thermal hysteresis proteins. Int J Biochem Cell Biol 33:105–117.

    Article  CAS  PubMed  Google Scholar 

  • Beall PT (1983) States of water in biological systems. Cryobiology 20: 324–334.

    Article  CAS  PubMed  Google Scholar 

  • Chattopadhyay MK (2002) The cryoprotective effects of glycine betaine. Trends Microbiol 10: 311.

    Article  CAS  Google Scholar 

  • Chattopadhyay MK (2006) Mechanism of bacterial adaptation to low temperature. J Biosci 31:157–165.

    Article  CAS  PubMed  Google Scholar 

  • Chilson OP, Costello LA, Kaplan NO (1965) Effects of freezing on enzymes. Fed Proc 24:55–65.

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • Fall R, Wolber PK (1995) Biochemistry of bacterial ice nuclei. In: Lee RE Jr, Warren GJ, Gusta LV (ed.). Biological ice nucleation and its applications. APS Press, St. Paul, MN, pp 64–78.

    Google Scholar 

  • Franks F (1985) Biophysics and biochemistry at low temperatures, pp 36–37. Japan UNI Agency, Tokyo.

    Google Scholar 

  • Fujikawa S (1987) Mechanisms of freezing injury in cellular level. Trans of the JAR 14:11–25.

    Google Scholar 

  • Fukuoka S, Kamishima H, Tamiya E, Karube I (1992) Spontaneous release of outer membrane vesicles by Erwinia carotovora. Microbios 72:167–173.

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Govindarajan A, Lindow SE (1988) Phospholipid requirement for expression of ice nuclei in Pseudomonas syringae and in vitro. J Biol Chem 263:9333–9338.

    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.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Guriansherman D, Lindow SE (1993) Bacterial ice nucleation: significance and molecular basis. FASEB J 7:1338–1343.

    CAS  Google Scholar 

  • Hew CL, Yang DSC (1992) Protein interaction with ice. Eur J Biochem 203:33–42.

    Article  CAS  PubMed  Google Scholar 

  • Hirano SS, Nordheim EV, Arny DC, Upper CD (1982) Longnormal distribution of epiphytic bacterial population of leaf surfaces. Appl Environ Microbiol 44:697–700.

    Google Scholar 

  • Honjoh K, Matsumoto H, Shimizu H, Ooyama K, Tanaka K, Oda Y, Takata R, Joh T, Suga K, Miyamoto T, Iio M, Hatano S (2000) Cryoprotective activities of group 3 late embryogenesis abundant proteins from Chlorella vulgaris C-27. Biosci Biotechnol Biochem 64:1656–1663.

    Article  CAS  PubMed  Google Scholar 

  • Kajava AV, Lindow SE (1993) A model of the three-dimensional structure of ice nucleation proteins. J Mol Biol 232:709–717.

    Article  CAS  PubMed  Google Scholar 

  • Kawahara H, Mano Y, Obata H (1993) Purification and characterization of extracellular ice-nucleating matter from Erwinia urdovora KUIN-3. Biosci Biotechnol Biochem 57:1429–1432.

    Article  CAS  Google Scholar 

  • Kawahara H, Mano Y, Hamada R, Obata H (1994) Role of spermidine in ice-nucleating activity of the EIM from Erwinia uredovora KUIN-3. Biosci Biotechnol Biochem 59:2201–2206.

    Article  Google Scholar 

  • Kawahara H, Ikugawa H, Obata H (1996a) Isolation and characterization of a marine ice-nucleating bacterium, Pseudomonas sp. KUIN-5, which produces cellulose and secretes it in the culture broth. Biosci Biotech Biochem 60:1474–1478.

    Article  CAS  Google Scholar 

  • Kawahara H, Nagae I, Obata H (1996b) Purification and characterization of a new anti-nucleating protein isolated from Acinetobacter calcoaceticus KINI-1. Biocontrol Sci 1:11–17.

    CAS  Google Scholar 

  • Kawahara H, Matsushita M, Yamada K, Obata H (1999) The control of the production and secretion of extracellular ice-nucleating materials of Erwinia uredovora KUIN-3. Biocontrol Sci 4:9–16.

    CAS  Google Scholar 

  • Kawahara H, Masuda K, Obata H (2000 a) Identification of a compound in Chamaecyparis taiwanensis inhibiting the ice-nucleating activity of Pseudomonas fluorescens KUIN-1. Biosci Biotechnol Biochem 64:2651–2656.

    Article  CAS  PubMed  Google Scholar 

  • Kawahara H, Koda N, Oshio M, Obata H (2000b) A cold acclimation protein with refolding activity on frozen denatured enzymes. Biosci Biotechnol Biochem 64:2668–2674.

    Article  CAS  PubMed  Google Scholar 

  • Kawahara H, Li J, Griffith M, Gluck BR (2001) Relationship between antifreeze protein and freezing resistance in Pseudomonas putida GR12–2. Curr Microbiol 43:365–370.

    Article  CAS  PubMed  Google Scholar 

  • Kawahara H (2002) The structure and function of ice crystal-controlling proteins from bacteria. J Biosci Bioeng 94:492–496.

    CAS  PubMed  Google Scholar 

  • Kawahara H, Nakano 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, Takemura T, Obata H (2005) Ice crystal-controlling protein from Thamnolia vermicularis. Lichenology 4:97–104.

    Google Scholar 

  • Kim HK, Orser C, Lindow SE, Sands DC (1987) Xanthomonas campestris pv. translucens strains active in ice nucleation. Plant Dis 71:994–997.

    Article  Google Scholar 

  • Ko R, Smith LT, Smith GM (1994) Glycine betaine confers enhanced osmotorelance and cryotolerance on Listeria monocytogenes. J Bacteriol 176:426–431.

    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.

    Article  CAS  PubMed  Google Scholar 

  • Koda N, Aoki M, Kawahara H, Obata H (2000) Characterization and properties of intracellular proteins after cold acclimation of ice-nucleating bacterium Pantoea agglomerans (Erwinia herbicola) IFO12686. Cryobiology 41:195–203.

    Article  CAS  PubMed  Google Scholar 

  • Koda N, Asaeda T, Yamade K, Kawahara H, Obata H (2001) A novel cryoprotective protein (CRP) with high activity from the ice-nucleating bacterium, Pantoea agglomerance IFO12686. Biosci Biotechnol Biochem 65:888–894.

    Article  CAS  PubMed  Google Scholar 

  • Koda N, Inada Y, Nakayama S, Kawahara H, Obata H (2002) Response of the ice-nucleating bacterium Pantoea ananas KUIN-3 during cold acclimation. Biosci Biotechnol Biochem 66:866–868.

    Article  CAS  PubMed  Google Scholar 

  • Kozloff LM, Turner MA, Arellano F, Lute M (1991) Phosphatidylinositol, a phospholipid of ice-nucleating bacteria. J Bacteriol 173:2053–2060.

    CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Lindow SE, Arny DC, Upper CD (1983) Biological control of frost injury: An isolate of Erwinia herbicola antagonistic to ice nucleation active bacteria. Phytopathology 73:1097–1102.

    Article  Google Scholar 

  • Li J, Lee TC (1998) Bacterial extracellular ice nucleator effects on freezing of foods. J Food Sci 63:375–381.

    Article  CAS  Google Scholar 

  • Lin C, Thomashow MF (1992) DNA sequence analysis of a complementary DNA for cold-regulated Arabidopsis gene cor15 and characterization of the COR15. Plant Physiol 99:519–525.

    Article  CAS  PubMed  Google Scholar 

  • Maki LR, Galyan EL, Chang-Cheng MM, Caldwell DR (1974) Ice nucleation induced by Pseudomonas syringae. Appl Microbiol 28:456–459.

    Google Scholar 

  • Matsukawa H, Yagi Y, Matsuda H, Kawahara H, Yamamoto I, Matsuoka J, Tanaka N (2000) Ascorbic acid 2-glucoside prevents sinusoidal endothelial cell apoptosis in supercooled preserved grafts in rat liver transplantation. Transplant Proc 32:313–317.

    Article  CAS  PubMed  Google Scholar 

  • Mazur P (1970) Cryobiology: the freezing of biological systems. Science 168:939–949.

    Article  CAS  PubMed  Google Scholar 

  • Michigami Y, Watabe S, Abe K, Obata H, Arai S (1994) Cloning and sequencing of an ice nucleation active gene of Erwinia uredovoa. Biosci Biotechnol Biochem 58:762–764.

    Article  CAS  PubMed  Google Scholar 

  • Michigami Y, Abe K, Obata H, Arai S (1995a) Significance of the C-terminal domain of Erwinia uredovora ice nucleation-active protein (Ina U). J Biochem (Tokyo) 118:1279–1284.

    CAS  Google Scholar 

  • Michigami Y, Abe K, Iwabuchi K, Obata, H, Arai S (1995b) Formation of ice-nucleation-active vesicle in Erwinia uredovora at low temperature and transport InaU molecules into shed vesicles. Biosci Biotechnol Biochem 59:1996–1998.

    Article  CAS  Google Scholar 

  • Mills SV (1999) Novel biochemical compounds from Antarctic microorganisms. PhD thesis, Nottingham University, UK.

    Google Scholar 

  • Muryoi N, Sato M, Kaneko S, Kawahara H, Obata H, Yaish MWF, Griffith M, Glick BR (2004) Cloning and expression of afpA, a gene encoding an antifreeze protein from the Arctic plant growth-promoting rhizobacterium Pseudomonas putida GR12–2. J Bacteriol 186:5661–5667.

    Article  CAS  PubMed  Google Scholar 

  • Mizuno H (1989) Prediction of the conformation of ice-nucleation protein by conformational energy calculation. Proteins 5:47–65.

    Article  CAS  PubMed  Google Scholar 

  • Momma M, Haraguchi K, Saito M, Chikuni K, Harada K (1997) Purification and characterization of the acid soluble 26-kDa polypeptide from soybean seeds. Biosci Biotechnol Biochem 61:1286–1289.

    Article  CAS  PubMed  Google Scholar 

  • Morita Y, Nakamori, S, Takagi, H (2003) L-Proline accumulation and freeze tolerance in Saccharomyces cerevisiae are caused by a mutation in the PRO1 gene encoding t-glutamyl kinase. Appl Environ Microbiol 69:212–219.

    Article  CAS  PubMed  Google Scholar 

  • Neven LG, Haskell DW, Hong A, Li Q-B, Guy CL (1993) Characterization of a spinach gene responsive to low temperature and water stress. Plant Mol Biol 21:291–305.

    Article  CAS  PubMed  Google Scholar 

  • Obata H, Saeki Y, Tanishita J, Tokuyama T, Hori H, Higashi Y (1987) Identificationof an ice-nucleating bacterium KUIN-1 in Pseudomonas fluorescens and its nucleation properties. Agric Biol Chem 51:1761–1766.

    CAS  Google Scholar 

  • Obata H, Tanaka T, Kawahara H, Tokuyama T (1993) Properties of cell-free ice nuclei from ice nucleation-active Pseudomonas fluorescens KUIN-1. J Ferment Bioeng 76:19–24.

    Article  CAS  Google Scholar 

  • Obata H, Ishigaki H, Kawahara H, Yamade K (1998) Purification and characterization of a novel cold-regulated protein from an ice-nucleating bacterium, Pseudomonas fluorescens KUIN-1. Biosci Biotechnol Biochem 62:2091–2097.

    Article  CAS  PubMed  Google Scholar 

  • Obata H, Muryoi N, Kawahara H, Yamade K, Nishikawa J (1999) Identification of a novel ice-nucleating bacterium of Antarctic origin and its ice nucleation properties. Cryobiology 38:131–139.

    Article  CAS  PubMed  Google Scholar 

  • Obata H, Muryoi N, Kawahara H, Nishiyama A (2004) Purification and characterization of uridine phosphorylase from the ice-nucleating bacterium, Pantoea agglomerance NBRC12686. Cryo Lett 25:195–204.

    CAS  Google Scholar 

  • Obata H, Shiga N, Takemura T, Kawahara H, Yamamoto Y (2006) Properties of cell-free ice nuclei from a novel ice nucleation-active Heterodermia obscurata (Nyl.) Trevis. Lichenology 5:37–44.

    Google Scholar 

  • Phadtare S (2004) Recent developments in bacterial cold-shock response. Curr Issues Mol Biol 6:125–136.

    CAS  PubMed  Google Scholar 

  • Phelps P, Geddings TH, Prochoda M, Fall R (1986) Release of cell-free ice nuclei by Erwinia herbicola. J Bacteriol 167:496–502.

    CAS  PubMed  Google Scholar 

  • Pouleur S, Richard C, Martin JG, Autoun H (1992) Ice nucleation activity in Fusarium acuminatum and Fusarium avenaceum. Appl Environ Microbiol 58:2960–2964.

    PubMed  CAS  Google Scholar 

  • Regand A, Goff HD (2006) Ice recrystallization inhibition in ice cream as affected by ice structuring proteins from winter wheat grass. J Dairy Sci 89:49–57.

    Article  CAS  PubMed  Google Scholar 

  • Russell NJ (1997) Psychrophilic bacteria—molecular adaptations of membrane lipids. Comp Biochem Physiol Physiol 118:489–493.

    Article  CAS  Google Scholar 

  • Seguro K, Tamiya T, Tsuchiya T, Matsumoto J (1989) Effect of chemical modifications on freeze denaturation of lactate dehydrogenase. Cryobiology 26:154–161.

    Article  CAS  PubMed  Google Scholar 

  • Storey KB (1983) Metabolism and bound water in overwintering insects. Cryobiology 20:365–379.

    Article  CAS  PubMed  Google Scholar 

  • Storey KB, Storey JM (1986) Freeze tolerance and intorelance as strategies of winter survival in treestrially-hibernating amphibians. Comp Biochem Physiol 83:613–617.

    Article  CAS  Google Scholar 

  • Sun X, Griffith M, Pasternak JJ, 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 44, 64–73.

    Google Scholar 

  • Tamiya T, Okahashi N, Sakuma R, Aoyama T, Akahane T, Matsumoto J (1985) Freeze denaturation of enzymes and its prevention with additives. Cryobiology 22:446–456.

    Article  CAS  PubMed  Google Scholar 

  • Thomashow MF (1990) Molecular genetics of cold acclimation in higher plant. Adv Genet 28:99–131.

    Article  CAS  Google Scholar 

  • Tsuda S, Ito A, Matsushima N (1997) A hairpin-loop conformation in tandem repeat sequence of the ice nucleation protein revealed by NMR spectroscopy. FEBS Lett 409:227–231.

    Article  CAS  PubMed  Google Scholar 

  • Turner MA, Arellano F, Kozloff LM (1991) Components of ice nucleation structures of bacteria. J Bacteriol 173:6515–6527.

    CAS  PubMed  Google Scholar 

  • Warren G, Corotto L, Wolber P (1986) Conserved repeats in diverged ice nucleation structural genes from two species of Pseudomonas. Nucleic Acids Res 14:8047–8060.

    Article  CAS  PubMed  Google Scholar 

  • Warren G, Corotto L (1989) The consensus sequence of ice nucleation proteins from Erwinia herbicola, Pseudomonas fluorescens, and Pseudomonas syringae. Gene 85:241–244.

    Article  Google Scholar 

  • Warren G, Wolber P (1991) Molecular aspects of microbial ice nucleation. Mol Microbiol 5:239–243.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wilson SL, Kelley DL, Walker VK (2006) Ice-active characteristics of soil bacteria selected by ice affinity. Environ Microbiol 8:1816–1824.

    Article  CAS  PubMed  Google Scholar 

  • Wowk B, Fahy GM (2002) Inhibition of bacterial ice nucleation by polyglycerol polymers. Cryobiology 44:14–23.

    Article  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.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yamashita Y, Kawahara H, Obata H (2002b Identification of a novel anti-ice-nucleating polysaccharide from Bacillus thuringiensis YY529. Biosci Biotechnol Biochem 66:948–954.

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Orser CS (1990) Conserved repetition in the ice nucleation gene inaX from Xanthomonas campestris pv. translucens. Mol Gen Genet 223:163–166.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Kawahara, H. (2008). Cryoprotectants and Ice-Binding Proteins. In: Margesin, R., Schinner, F., Marx, JC., Gerday, C. (eds) Psychrophiles: from Biodiversity to Biotechnology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-74335-4_14

Download citation

Publish with us

Policies and ethics