Naturwissenschaften

, Volume 94, Issue 2, pp 77–99 | Cite as

Cold-loving microbes, plants, and animals—fundamental and applied aspects

Review

Abstract

Microorganisms, plants, and animals have successfully colonized cold environments, which represent the majority of the biosphere on Earth. They have evolved special mechanisms to overcome the life-endangering influence of low temperature and to survive freezing. Cold adaptation includes a complex range of structural and functional adaptations at the level of all cellular constituents, such as membranes, proteins, metabolic activity, and mechanisms to avoid the destructive effect of intracellular ice formation. These strategies offer multiple biotechnological applications of cold-adapted organisms and/or their products in various fields. In this review, we describe the mechanisms of microorganisms, plants, and animals to cope with the cold and the resulting biotechnological perspectives.

Keyword

Cryoprotectants Cold adaptation Freeze tolerance Supercooling Proteins Membranes Antioxidant defenses Gene expression 

References

  1. Adams WW, Zarter CR, Ebbert V, Demmig-Adams B (2004) Photoprotective strategies of overwintering evergreens. Bioscience 54:41–49Google Scholar
  2. Aguilar PS, Cronan JE Jr, de Mendoza D (1998) A Bacillus subtilis gene induced by cold shock encodes a membrane phospholipids desaturase. J Bacteriol 180:2194–2200PubMedGoogle Scholar
  3. Alexander M (1999) Biodegradation and bioremediation, 2nd edn. Academic, LondonGoogle Scholar
  4. Alkasrawi M, Nandakumar R, Margesin R, Schinner F, Mattiasson B (1999) A microbial biosensor based on Yarrowia lipolytica for the off-line determination of middle-chain alkanes. Biosens Bioelectron 14:723–727PubMedGoogle Scholar
  5. Allagulova CR, Gimalov FR, Shakirova FM, Vakhitov VA (2003) The plant dehydrins: structure and putative functions. Biochemistry (Mosc) 68:945–951Google Scholar
  6. Anchordoguy TJ, Rudolph AS, Carpenter JF, Crowe JH (1987) Modes of interaction of cryoprotectants with membrane phospholipids during freezing. Cryobiology 24:324–331PubMedGoogle Scholar
  7. Ashworth EN, Pearce RS (2002) Extracellular freezing in leaves of freezing-sensitive species. Planta 214:798–805PubMedGoogle Scholar
  8. Atici O, Nalbantoglu B (2003) Antifreeze proteins in higher plants. Phytochemistry 64:1187–1196PubMedGoogle Scholar
  9. Benson E, Bremner D (2004) Oxidative stress in the frozen plant: a free radical point of view. In: Benson E, Fuller B, Lane N (eds) Life in the frozen state. CRC Press, Boca Raton, FL, pp 205–241Google Scholar
  10. Benson E, Fuller B, Lane N (eds) (2004) Life in the frozen state. CRC Press, Boca Raton, FL, pp 645–657Google Scholar
  11. Bilgen T, English TE, McMullen DC, Storey KB (2001) EsMlp, a muscle-LIM protein gene, is up-regulated during cold exposure in the freeze-avoiding larvae of Epiblema scudderiana. Cryobiology 43:11–20PubMedGoogle Scholar
  12. Block W (2003) Water or ice?—The challenge for invertebrate cold survival. Sci Prog 86:77–101PubMedCrossRefGoogle Scholar
  13. Bodner M, Larcher W (1987) Chilling susceptibility of different organs and tissues of Saintpaulia ionantha and Coffea arabica. Angew Bot 61:225–242Google Scholar
  14. Bowles DJ, Lillford PJ, Rees DA, Shanks IA (eds) (2002) Coping with the cold: the molecular and structural biology of cold stress survivors. Philos Trans R Soc Lond B Biol Sci 357:829–955Google Scholar
  15. Braddock JF, Ruth ML, Walworth JL, McCarthy KA (1997) Enhancement and inhibition of microbial activity in hydrocarbon-contaminated arctic soils: implications for nutrient-amended bioremediation. Environ Sci Technol 31:2078–2084Google Scholar
  16. Bravo L-A, Griffith M (2005) Characterization of antifreeze activity in Antarctic plants. J Exp Bot 56:1189–1196PubMedGoogle Scholar
  17. Buchholz DR, Fu L, Shi YB (2004) Cryopreservation of Xenopus transgenic lines. Mol Reprod Dev 67:65–69PubMedGoogle Scholar
  18. Burke MJ, Gusta LV, Quamme HA, Weiser CJ, Li PH (1976) Freezing and injury in plants. Annu Rev Plant Physiol 27:507–528Google Scholar
  19. Carpenter EJ, Lin S, Capone DG (2000) Bacterial activity in South Pole snow. Appl Environ Microbiol 66(10):4514–4517PubMedGoogle Scholar
  20. Carter J, Brennan R, Wisniewski M (2001) Patterns of ice formation and movement in blackcurrant. HortScience 36:855–859Google Scholar
  21. Cavicchioli R, Siddiqui KS, Andrews D, Sowers KR (2002) Low-temperature extremophiles and their applications. Curr Opin Biotechnol 13:253–261PubMedGoogle Scholar
  22. Chen TH, Gusta LV (1983) Abscisic acid-induced freezing resistance in cultured plant cells. Plant Physiol 73:71–75PubMedGoogle Scholar
  23. Chinnusamy V, Zhu J, Zhu J-K (2006) Gene regulation during cold acclimation in plants. Phys Plant 126:52–61Google Scholar
  24. Chintalapati S, Kiran MD, Shivaji S (2004) Role of membrane lipid fatty acids in cold adaptation. Cell Mol Biol (Noisy-le-grand) 50:631–642Google Scholar
  25. Christner BC (2002) Incorporation of DNA and protein precursors into macromolecules by bacteria at −15°C. Appl Environ Microbiol 68:6435–6438PubMedGoogle Scholar
  26. Costanzo JP, Iverson JB, Wright MF, Lee RE (1995) Cold-hardiness and overwintering strategies of hatchlings in an assemblage of northern turtles. Ecology 76:1772–1785Google Scholar
  27. Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:570–599Google Scholar
  28. Cummings SP, Black GW (1999) Polymer hydrolysis in a cold climate. Extremophiles 3:81–87PubMedGoogle Scholar
  29. D’Amico S, Claverie P, Collins T, Georlette D, Gratia E, Hoyoux A, Meuwis MA, Feller G, Gerday C (2002) Molecular basis of cold adaptation. Philos Trans R Soc Lond B Biol Sci 357:917–925PubMedGoogle Scholar
  30. Davies PL, Baardsnes J, Kuiper MJ, Walker VK (2002) Structure and function of antifreeze proteins. Philos Trans R Soc Lond B Biol Sci 357:927–935PubMedGoogle Scholar
  31. Delille D, Coulon F, Pelletier E (2004) Biostimulation of natural microbial assemblages in oil-amended vegetated and desert sub-Antarctic soils. Microb Ecol 47:407–415PubMedGoogle Scholar
  32. Deming JW (2002) Psychrophiles and polar regions. Curr Opin Microbiol 5:301–309PubMedGoogle Scholar
  33. Du X, Takagi H (2005) N-acetyltransferase Mpr1 confers freeze tolerance on Saccharomyces cerevisiae by reducing reactive oxygen species. J Biochem (Tokyo) 138:391–397Google Scholar
  34. Duilio A, Madonna S, Tutino ML, Pirozzi M, Sannia G, Marino G (2004) Promoters from a cold-adapted bacterium: definition of a consensus motif and molecular characterization of UP regulative elements. Extremophiles 8:125–132PubMedGoogle Scholar
  35. Duman JG (2001) Antifreeze and ice nucleator proteins in terrestrial arthropods. Annu Rev Physiol 63:327–357PubMedGoogle Scholar
  36. Duman JG, Verleye D, Li N (2002) Site-specific forms of antifreeze protein in the beetle Dendroides canadensis. J Comp Physiol [B] 172:547–552Google Scholar
  37. Duman JG, Bennett V, Sformo T, Hochstrasser R, Barnes BM (2004) Antifreeze proteins in Alaskan insects and spiders. J Insect Physiol 50:259–266PubMedGoogle Scholar
  38. Duncker BP, Davies PL, Walker VK (1999) Increased gene dosage augments antifreeze protein levels in transgenic Drosophila melanogaster. Transgenic Res 8:45–50PubMedGoogle Scholar
  39. Edashige K, Yamaji Y, Kleinhans FW, Kasai M (2003) Artificial expression of aquaporin-3 improves the survival of mouse oocytes after cryopreservation. Biol Reprod 68:87–94PubMedGoogle Scholar
  40. Eddy SF, Storey KB (2002) Dynamic use of cDNA arrays: heterologous probing for gene discovery and exploration of organismal adaptation to environment stress. In: Storey KB, Storey JM (eds) Cell and molecular responses to stress, vol 3. Elsevier, Amsterdam, pp 315–325Google Scholar
  41. Feller G, Gerday C (1997) Psychrophilic enzymes: molecular basis of cold adaptation. Cell Mol Life Sci 53:830–841PubMedGoogle Scholar
  42. Feller G, Narinx E, Arpigny JL, Aittaleb M, Baise E, Genicot S, Gerday C (1996) Enzymes from psychrophilic bacteria. FEMS Microbiol Rev 18:189–202Google Scholar
  43. Ferrer M, Chernikova TN, Yakimov MM, Golyshin PN, Timmis KN (2003) Chaperonins govern growth of Escherichia coli at low temperatures. Nat Biotechnol 21:1266–1267PubMedGoogle Scholar
  44. Fletcher GL, Hew CL, Davies PL (2001) Antifreeze proteins of teleost fishes. Annu Rev Physiol 63:359–390PubMedGoogle Scholar
  45. Franks F, Mathias SF, Hatley RH (1990) Water, temperature and life. Phil Trans R Soc Lond B Biol Sci 326:517–533Google Scholar
  46. Fuller B, Paynter S (2004) Fundamentals of cryobiology in reproductive medicine. Reprod Biomed Online 9:680–691PubMedCrossRefGoogle Scholar
  47. Gerday C, Hoyoux A, Francois JM, Dubois P, Baise E, Jennes I, Genicot S (2001) Cold-active beta galactosidase, the process for its preparation and the use thereof. Patent WO104276, January 18Google Scholar
  48. Glansdorff N, Xu J (2002) Microbial life at low temperatures: mechanisms of adaptation and extreme biotopes. Implications for exobiology and the origin of life. Recent Res Devel Microbiol 6:1–21Google Scholar
  49. Glenister PH, Whittingham DG, Wood MJ (1990) Genome cryopreservation: a valuable contribution to mammalian genetic research. Genet Res 56:253–258PubMedCrossRefGoogle Scholar
  50. Goodchild A, Raftery M, Saunders NFW, Guilhaus M, Cavicchioli R (2004) Biology of the cold adapted archaeon, Methanococcoides burtonii determined by proteomics using liquid chromatography-tandem mass spectrometry. J Proteome Res 3:1164–1176PubMedGoogle Scholar
  51. Gounot AM, Russell NJ (1999) Physiology of cold-adapted microorganisms. In: Margesin R, Schinner F (eds) Cold-adapted organisms. Springer, Berlin Heidelberg New York, pp 33–55Google Scholar
  52. Graether SP, Sykes BD (2004) Cold survival in freeze-intolerant insects: the structure and function of beta-helical antifreeze proteins. Eur J Biochem 271:3285–3296PubMedGoogle Scholar
  53. Griffith M, Ewart KV (1995) Antifreeze proteins and their potential use in frozen foods. Biotechnol Adv 13:375–402PubMedGoogle Scholar
  54. Griffith M, Antikainen M, Hon W-C, Pihakaski-Maunsbach K, Yu X-M, Chun JU, Yang DSC (1997) Antifreeze proteins in winter rye. Physiol Plant 100:327–332Google Scholar
  55. Gusta LV, Burke MJ, Kapoor AC (1975) Determination of unfrozen water in winter cereals at sub-freezing temperatures. Plant Physiol 56:707–709PubMedGoogle Scholar
  56. Hacker J, Neuner G (2006) Photosynthetic capacity and PS II efficiency of the evergreen alpine cushion plant Saxifraga paniculata during winter at different altitudes. Arct Antarct Alp Res 38(2):198–205Google Scholar
  57. Hagedorn M, Peterson A, Mazur P, Kleinhans FW (2004) High ice nucleation temperature of zebrafish embryos: slow-freezing is not an option. Cryobiology 49:181–189PubMedGoogle Scholar
  58. Häggblom M, Margesin R (2005) Microbial life in cold ecosystems. FEMS Microbiol Ecol, Thematic Issue, 53:186Google Scholar
  59. Hew C, Poon R, Xiong F, Gauthier S, Shears M, King M, Davies P, Fletcher G (1999) Liver-specific and seasonal expression of transgenic Atlantic salmon harboring the winter flounder antifreeze protein gene. Transgenic Res 8:405–414PubMedGoogle Scholar
  60. Hightower R, Baden K, Penzes E, Lund P, Dunsmuir P (1991) Expression of antifreeze proteins in transgenic plants. Plant Mol Biol 17:1013–1021PubMedGoogle Scholar
  61. Hiilovaara-Teijo M, Palva ET (1999) Molecular responses in cold-adapted plants. In: Margesin R, Schinner F (eds) Cold-adapted organisms. Ecology, physiology, enzymology and molecular biology. Springer, Berlin Heidelberg New York, pp 349–384Google Scholar
  62. Hincha DK, DeVries AL, Schmitt JM (1993) Cryotoxicity of antifreeze proteins and glycoproteins to spinach thylakoid membranes—comparison with cryotoxic sugar acids. Biochim Biophys Acta 1146:258–264PubMedGoogle Scholar
  63. Hirsh AG, Williams RJ, Meryman HT (1985) A novel method of natural cryoprotection. Intracellular glass formation in deeply frozen Populus. Plant Physiol 79:41–56PubMedGoogle Scholar
  64. Hochachka PW, Somero GN (eds) (1984) Biochemical adaptations. Princeton University Press, Princeton, pp 355–449Google Scholar
  65. Hoshino T, Fujiwara M, Suzuki K, Miura K, Kondo H, Ohgiya S, Tsuda S, Yumoto I (2006) Antifreeze proteins in cold-adapted fungi. In: Margesin R (ed) Abstracts of the International Conference on Alpine and Polar Microbiology, Innsbruck, AustriaGoogle Scholar
  66. Huner NPA, Öquist G, Melis A (2003) Photostasis in plants, green algae and cyanobacteria: the role of light harvesting antenna complexes. In: Green BR, Parson WW (eds) Advances in photosynthesis and respiration. Light-harvesting antennas in photosynthesis, vol 13. Kluwer, Dordrecht, pp 402–421Google Scholar
  67. Ingraham JL, Stokes JL (1959) Psychrophilic bacteria. Bacteriol Rev 23:97–108PubMedGoogle Scholar
  68. Izawa S, Ikeda K, Maeta K, Inoue Y (2004) Deficiency in the glycerol channel Fps1p confers increased freeze tolerance to yeast cells: application of the fps1delta mutant to frozen dough technology. Appl Microbiol Biotechnol 66:303–305PubMedGoogle Scholar
  69. Jagannadham MV, Chattopadhyay MK, Subbalakshmi C, Vairamani M, Narayanan K, Rao CM, Shivaji S (2000) Carotenoids of an Antarctic psychrotolerant bacterium, Sphingobacterium antarcticus, and a mesophilic bacterium, Sphingobacterium multivorum. Arch Microbiol 173:418–424PubMedGoogle Scholar
  70. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106PubMedGoogle Scholar
  71. Joanisse DR, Storey KB (1996) Oxidative damage and antioxidants in Rana sylvatica, the freeze tolerant wood frog. Am J Physiol 271:R545–R553PubMedGoogle Scholar
  72. Johnston IA (2003) Muscle metabolism and growth in Antarctic fishes (suborder Notothenioidei): evolution in a cold environment. Comp Biochem Physiol B Biochem Mol Biol 136:701–713PubMedGoogle Scholar
  73. Junge K, Eicken H, Deming JW (2003) Motility of Colwellia psychrerythraea strain 34H at subzero temperatures. Appl Environ Microbiol 69:4282–4284PubMedGoogle Scholar
  74. Karner MB, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507–510PubMedGoogle Scholar
  75. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress inducible transcription factor. Nat Biotechnol 17:287–291PubMedGoogle Scholar
  76. Kolesnichenko AV, Pobezhimova TP, Voinikov VK (2000) Cold-shock proteins in plants. Russ J Plant Physiol 47:549–554Google Scholar
  77. Kourkoutas Y, Douma M, Koutinas AA, Kanellaki M, Banat IM, Marchant R (2003) Continuous winemaking fermentation using quince-immobilized yeast at room and low temperatures. Process Biochem 39:143–148Google Scholar
  78. Kristiansen E, Zachariassen KE (2005) The mechanism by which fish antifreeze proteins cause thermal hysteresis. Cryobiology 51(3):262–280PubMedGoogle Scholar
  79. Kristjansdottir S, Gudmundsdottir A (2000) Propeptide dependent activation of the Antarctic krill euphauserase precursor produced in yeast. Eur J Biochem 267:2632–2639PubMedGoogle Scholar
  80. Larcher W (2003) Physiological plant ecology. Ecophysiology and stress physiology of functional groups, 4th edn. Springer, Berlin Heidelberg New YorkGoogle Scholar
  81. Lettinga G, Rebac S, van Lier J, Zeman G (1999) The potentials of sub-mesophilic and/or psychrophilic anaerobic treatment of low strength wastewaters. In: Margesin R, Schinner F (eds) Biotechnological applications of cold-adapted organisms. Springer, Berlin Heidelberg New York, pp 221–234Google Scholar
  82. Levitt J (1980) Responses of plants to environmental stresses, vol 1, 2nd edn. Academic, New YorkGoogle Scholar
  83. Lewis JM, Ewart KV, Driedzic WR (2004) Freeze resistance in rainbow smelt (Osmerus mordax): seasonal pattern of glycerol and antifreeze protein levels and liver enzyme activity associated with glycerol production. Physiol Biochem Zool 77:415–422PubMedGoogle Scholar
  84. Lindow SE, Leveau JH (2002) Phyllosphere microbiology. Curr Opin Biotechnol 13:238–243PubMedGoogle Scholar
  85. Liu HC, He Z, Rosenwaks Z (2003) Mouse ovarian tissue cryopreservation has only a minor effect on in vitro follicular maturation and gene expression. J Assist Reprod Genet 20:421–431PubMedGoogle Scholar
  86. Loik ME, Still CJ, Huxman TE, Harte J (2004) In situ photosynthetic freezing tolerance for plants exposed to a global warming manipulation in the Rocky Mountains, Colorado, USA. New Phytol 162:331–341Google Scholar
  87. Lundheim R (2002) Physiological and ecological significance of biological ice nucleators. Philos Trans R Soc Lond B Biol Sci 357:937–943PubMedGoogle Scholar
  88. Marentes E, Griffith M, Mlynarz A, Brush RA (1993) Proteins accumulate in the apoplast of winter rye leaves during cold acclimation. Physiol Plant 87:499–507Google Scholar
  89. Margesin R (2004) Bioremediation of petroleum hydrocarbon-polluted soils in extreme temperature environments. In: Singh A, Ward OP (eds) Applied bioremediation and phytoremediation, soil biology, vol 1. Springer, Berlin Heidelberg New York, pp 215–234Google Scholar
  90. Margesin R, Nogi Y (2004) Psychropiezophilic microorganisms (review). Cell Mol Biol (Noisy-le-grand) 50:429–436Google Scholar
  91. Margesin R, Schinner F (1992) A comparison of extracellular proteases from three psychrotrophic strains of Pseudomonas fluorescens. J Gen Appl Microbiol 38:209–225Google Scholar
  92. Margesin R, Schinner F (eds) (1999a) Cold-adapted organisms. Ecology, physiology, enzymology and molecular biology. Springer, Berlin Heidelberg New YorkGoogle Scholar
  93. Margesin R, Schinner F (eds) (1999b) Biotechnological applications of cold-adapted organisms. Springer, Berlin Heidelberg New YorkGoogle Scholar
  94. Margesin R, Schinner F (2001) Biodegradation and bioremediation of hydrocarbons in extreme environments. Appl Microbiol Biotechnol 56:650–663PubMedGoogle Scholar
  95. Margesin R, Zacke G, Schinner F (2002a) Characterization of heterotrophic microorganisms in alpine glacier cryoconite. Arct Antarct Alp Res 34:88–93Google Scholar
  96. Margesin R, Feller G, Gerday C, Russell NJ (2002b) Cold-adapted microorganisms: adaptation strategies and biotechnological potential. In: Bitton G (ed) The encyclopedia of environmental microbiology, vol 2. Wiley, New York, pp 871–885Google Scholar
  97. Margesin R, Gander S, Zacke G, Gounot AM, Schinner F (2003a) Hydrocarbon degradation and enzyme activities of cold-adapted bacteria and yeasts. Extremophiles 7:451–458PubMedGoogle Scholar
  98. Margesin R, Labbé D, Schinner F, Greer CW, Whyte LG (2003b) Characterization of hydrocarbon-degrading microbial populations in contaminated and pristine alpine soils. Appl Environ Microbiol 69:3085–3092PubMedGoogle Scholar
  99. Margesin R, Fonteyne PA, Redl B (2004) Low-temperature biodegradation of high amounts of phenol by Rhodococcus spp. and basidiomycetous yeasts. Res Microbiol 156:68–75Google Scholar
  100. Margesin R, Fauster V, Fonteyne PA (2005) Characterization of cold-active pectate lyases from psychrophilic Mrakia frigida. Lett Appl Microbiol 40:453–459PubMedGoogle Scholar
  101. Marx JC, Blaise V, Collins T, D’Amico S, Delille D, Gratia E, Hoyoux A, Huston AL, Sonan G, Feller G, Gerday C (2004) A perspective on cold enzymes: current knowledge and frequently asked questions. Cell Mol Biol (Noisy-le-grand) 50:643–655Google Scholar
  102. Mautner MN (2005) Life in the cosmological future: resources, biomass and populations. JBIS J Br Interplanet Soc 58:167–180Google Scholar
  103. Medigue C, Krin E, Pascal G, Barbe V, Bernsel A, Bertin PN, Cheung F, Cruveiller S, D’Amico S, Duilio A, Fang G, Feller G, Ho C, Mangenot S, Marino G, Nilsson J, Parrilli E, Rocha EPC, Rouy Z, Sekowska A, Tutino ML, Vallenet D, von Heijne G, Danchin A (2005) Coping with cold: the genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125. Genome Res 15:1325–1335PubMedGoogle Scholar
  104. Methe BA, Nelson KE, Deming JW, Momen B, Melamud E, Zhang XJ, Moult J, Madupu R, Nelson WC, Dodson RJ, Brinkac LM, Daugherty SC, Durkin AS, DeBoy RT, Kolonay JF, Sullivan SA, Zhou LW, Davidsen TM, Wu M, Huston AL, Lewis M, Weaver B, Weidmann JF, Khouri H, Utterback TR, Feldblyum TV, Fraser CM (2005) The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc Natl Acad Sci USA 102:10913–10918PubMedGoogle Scholar
  105. Miteva VI, Sheridan PP, Brenchley JE (2004) Phylogenetic and physiological diversity of microorganisms isolated from a deep Greenland glacier ice core. Appl Environ Microbiol 70:202–213PubMedGoogle Scholar
  106. Mueller DR, Vincent WF, Bonilla S, Laurion I (2005) Extremotrophs, extremophiles and broadband pigmentation strategies in a high arctic shelf ecosystem. FEMS Microbiol Ecol 53:73–87PubMedGoogle Scholar
  107. Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi H, Tasaka Y, Nishida I (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356:710–713Google Scholar
  108. Nakasone K (2004) Whole-genome analysis of deep-sea piezophilic and psychrophilic bacterium, Shewanella violacea strain DSS12. J Jpn Soc Biosci Biotechnol Agrochem 78:402–406Google Scholar
  109. Neuner G, Ambach D, Aichner K (1999) Impact of snow cover on photoinhibition and winter desiccation in evergreen Rhododendron ferrugineum leaves during subalpine winter. Tree Physiol 19:725–732PubMedGoogle Scholar
  110. Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol 47:541–568Google Scholar
  111. Nomura M, Muramoto Y, Ýasuda S, Takabe T, Kishitani S (1995) The accumulation of glycine betaine during cold acclimation in early and late cultivars of barley. Euphytica 83:247–250Google Scholar
  112. Odani M, Komatsu Y, Oka S, Iwahashi H (2003) Screening of genes that respond to cryopreservation stress using yeast DNA microarray. Cryobiology 47:155–164PubMedGoogle Scholar
  113. Ohgiya S, Hoshino T, Okuyama H, Tanka S, Ishizaki K (1999) Biotechnology f enzymes from cold-adapted microorganisms. In: Margesin R, Schinner F (eds) Biotechnological applications of cold-adapted organisms. Springer, Berlin Heidelberg New York, pp 17–34Google Scholar
  114. Öquist G, Huner NPA (2003) Photosynthesis of overwintering evergreen plants. Annu Rev Plant Biol 54:329–355PubMedGoogle Scholar
  115. Ottander C, Campbell D, Öquist G (1995) Seasonal changes in photosystem II organisation and pigment composition in Pinus sylvestris. Planta 197:176–183Google Scholar
  116. Ouellet F (2002) Out of the cold: unveiling the elements required for low temperature induction of gene expression in plants. In Vitro Cell Dev Biol-Plant 38:396–403Google Scholar
  117. Ouellet F, Vazquez-Tello A, Sarhan F (1998) The wheat WCS120 promotor is cold-inducible in both monocotyledonous and dicotyledonous species. FEBS Lett 423:324–328PubMedGoogle Scholar
  118. Papa R, Rippa V, Marino G, Duilio A (2006) Regulation of gene expression in cold living micro organisms: molecular aspects and biotechnological applications. In: Margesin R (ed) Abstracts of the International Conference on Alpine and Polar MicrobiologyGoogle Scholar
  119. Pearce RS (1999) Molecular analysis of acclimation to cold. Plant Growth Regul 29:47–76Google Scholar
  120. Pearce RS (2001) Plant freezing and damage. Ann Bot (Lond) 87:417–424Google Scholar
  121. Pearce RS, Fuller MP (2001) Freezing of barley studied by infrared video thermography. Plant Physiol 125:227–240PubMedGoogle Scholar
  122. Peters ID, Rancourt DE, Davies PL, Walker VK (1993) Isolation and characterization of an antifreeze protein precursor from transgenic Drosophila: evidence for partial processing. Biochim Biophys Acta 1171:247–254PubMedGoogle Scholar
  123. Prevost D, Drouin P, Laberge S, Bertrand A, Cloutier J, Levesque G (2003) Cold-adapted rhizobia for nitrogen fixation in temperate regions. Can J Bot 81:1153–1161Google Scholar
  124. Price PB (2004) Life in solid ice on earth and other planetary bodies. In: Norris R, Stootman F (eds) Bioastronomy 2002: life among the stars, proceedings of IAU symposium #213. Astronomical Society of the Pacific, San Francisco 2003, pp 363–366Google Scholar
  125. Puhakainen T, Hess MW, Makela P, Svensson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54:743–753PubMedGoogle Scholar
  126. Rabus R, Ruepp A, Frickey T, Rattei T, Fartmann B, Stark M, Bauer M, Zibat A, Lombardot T, Becker I, Amann J, Gellner K, Teeling H, Leuschner WD, Glockner FO, Lupas AN, Amann R, Klenk HP (2004) The genome of Desulfotalea psychrophila, a sulfate-reducing bacterium from permanently cold Arctic sediments. Environ Microbiol 6:887–902PubMedGoogle Scholar
  127. Rajashekar CB, Burke MJ (1996) Freezing characteristics of rigid plant tissues. Plant Physiol 111:597–603PubMedGoogle Scholar
  128. Renaut J, Hausman J-F, Wisniewski M (2006) Proteomics and low-temperature studies: bridging the gap between gene expression and metabolism. Physiol Plant 126:97–109Google Scholar
  129. Ristic Z, Ashworth EN (1993) Changes in leaf ultrastructure and carbohydrates in Arabidopsis thaliana L. (Heyn) cv. Columbia during rapid cold acclimation. Protoplasma 172:111–123Google Scholar
  130. Rivkina EM, Friedmann EI, McKay CP, Gilichinsky DA (2000) Metabolic activity of permafrost bacteria below the freezing point. Appl Environ Microbiol 66:3230–3233PubMedGoogle Scholar
  131. Romanenko LA, Schumann P, Rohde M, Lysenko AM, Mikhailov VV, Stackebrandt E (2002) Psychrobacter submarinus sp nov and Psychrobacter marincola sp nov., psychrophilic halophiles from marine environments. Int J Syst Evol Microbiol 52:1291–1297PubMedGoogle Scholar
  132. Rossi G (1999) Biohydrometallurgical processes and temperature. In: Margesin R, Schinner F (eds) Biotechnological applications of cold-adapted organisms. Springer, Berlin Heidelberg New York, pp 291–308Google Scholar
  133. Russell NJ (1990) Cold adaptation of microorganisms. Philos Trans R Soc Lond B Biol Sci 329:595–611Google Scholar
  134. Russell NJ (1998) Molecular adaptations in psychrophilic bacteria: potential for biotechnological applications. Adv Biochem Eng Biotechnol 61:1–21PubMedGoogle Scholar
  135. Russell NJ (2000) Toward a molecular understanding of cold activity of enzymes from psychrophiles. Extremophiles 4:83–90PubMedGoogle Scholar
  136. Russell NJ, Nichols DS (1999) Polyunsaturated fatty acids in marine bacteria—a dogma rewritten. Microbiology 145:767–779PubMedCrossRefGoogle Scholar
  137. Sakai A, Larcher W (1987) Frost survival of plants. Responses and adaptation to freezing stress. In: Billings WD, Golley F, Lange OL, Olson S, Remmert H (eds) Ecological studies, vol 62. Springer, Berlin Heidelberg New YorkGoogle Scholar
  138. Savitch LV, Leonardos ED, Krol M, Jansson S, Grodzinski B, Huner NPA, Oquist G (2002) Two different strategies for light utilization in photosynthesis in relation to growth and cold acclimation. Plant Cell Environ 25:761–771Google Scholar
  139. Schulze E-D, Beck E, Müller-Hohenstein K (2005) Plant ecology. Springer, Berlin Heidelberg New YorkGoogle Scholar
  140. Senser M, Beck E (1982) Frost resistance in spruce (Picea abies (L.) Karst). IV. The lipid composition of frost resistant and frost sensitive spruce chloroplasts. Z Pflanzenphysiol 105:241–253Google Scholar
  141. Sheridan PP, Panasik N, Coombs JM, Brenchely JE (2000) Approaches for deciphering the structural basis of low temperature enzyme activity. Biochim Biophys Acta 1543:417–433PubMedGoogle Scholar
  142. Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223PubMedGoogle Scholar
  143. Shivaji S (ed) (2004) Microbes from cold habitats: biodiversity, biotechnology and cold adaptation. Cell Mol Biol 50:501–667Google Scholar
  144. Siddiqui KS, Poljak A, Cavicchioli R (2004) Improved activity and stability of alkaline phosphatases from psychrophillic and mesophilic organisms by chemically modifying aliphatic or amino groups using tetracarboxy-benzophenone derivatives. Cell Mol Biol 50:657–667PubMedGoogle Scholar
  145. Sinclair BJ, Addo-Bediako A, Chown SL (2003) Climatic variability and the evolution of insect freeze tolerance. Biol Rev Camb Philos Soc 78:181–195PubMedGoogle Scholar
  146. Singh KS, Viraraghavan T (2004) Municipal wastewater treatment by UASB process: start-up at 20 degrees C and operation at low temperatures. Environ Technol 25:621–634PubMedCrossRefGoogle Scholar
  147. Skirvin RM, Kohler E, Steiner H, Ayers D, Laughnan A, Norton MA, Warmund M (2000) The use of genetically engineered bacteria to control frost on strawberries and potatoes. Whatever happened to all of that research? Sci Hortic 84:179–189Google Scholar
  148. Somero GN (2004) Adaptation of enzymes to temperature: searching for basic “strategies”. Comp Biochem Physiol B Biochem Mol Biol 139:321–333PubMedGoogle Scholar
  149. Steponkus PL, Webb MS (1992) Freeze-induced dehydration and membrane destabilization in plants. In: Somero GN, Osmond CB, Bolis CL (eds) Water and life: comparative analysis of water relationships at the organismic, cellular and molecular level. Springer, Berlin Heidelberg New York, pp 338–362Google Scholar
  150. Storey KB (1997) Organic solutes in freezing tolerance. Comp Biochem Physiol A Physiol 117:319–326PubMedGoogle Scholar
  151. Storey KB (2004) Strategies for exploration of freeze responsive gene expression: advances in vertebrate freeze tolerance. Cryobiology 48:134–145PubMedGoogle Scholar
  152. Storey KB (2006) Reptile freeze tolerance: metabolism and gene expression. Cryobiology 52(1):1–16PubMedGoogle Scholar
  153. Storey KB, McMullen DC (2004) Insect cold-hardiness: new advances using gene screening technology. In: Barnes BM, Carey HV (eds) Life in the cold: evolution, mechanisms, adaptation and application. Biological Papers of the University of Alaska #27, Fairbanks, pp 275–281Google Scholar
  154. Storey KB, Storey JM (1996) Natural freezing survival in animals. Ann Rev Ecolog Syst 27:365–386Google Scholar
  155. Storey JM, Storey KB (2004a) Cold hardiness and freeze tolerance. In: Storey KB (ed) Functional metabolism: regulation and adaptation. Wiley, Hoboken, pp 473–503Google Scholar
  156. Storey KB, Storey JM (2004b) Physiology, biochemistry and molecular biology of vertebrate freeze tolerance: the wood frog. In: Benson E, Fuller B, Lane N (eds) Life in the frozen state. CRC Press, Boca Raton, FL, pp 243–274Google Scholar
  157. Storey KB, Baust JG, Wolanczyk JP (1992) Biochemical modification of the plasma ice nucleating activity in a freeze tolerant frog. Cryobiology 29:374–384PubMedGoogle Scholar
  158. Stroud RM, Miercke LJ, O’Connell J, Khademi S, Lee JK, Remis J, Harries W, Robles Y, Akhavan D (2003) Glycerol facilitator GlpF and the associated aquaporin family of channels. Curr Opin Struct Biol 13:424–431PubMedGoogle Scholar
  159. Suzuki I, Kanesaki Y, Mikami K, Kanehisa M, Murata N (2001) Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol Microbiol 40:235–244PubMedGoogle Scholar
  160. Tahtiharju S, Sangwan V, Monroy AF, Dhinsda RS, Borg M (1997) The induction of kin genes in cold-acclimating Arabidopsis thaliana. Evidence of a role of calcium. Planta 203:442–447PubMedGoogle Scholar
  161. Tanghe A, Van Dijck P, Colavizza D, Thevelein JM (2004) Aquaporin-mediated improvement of freeze tolerance of Saccharomyces cerevisiae is restricted to rapid freezing conditions. Appl Environ Microbiol 70:3377–3382PubMedGoogle Scholar
  162. Tanghe A, Kayingo G, Prior BA, Thevelein JM, Van Dijck P (2005) Heterologous aquaporin (AQY2-1) expression strongly enhances freeze tolerance of Schizosaccharomyces pombe. J Mol Microbiol Biotechnol 9:52–56PubMedGoogle Scholar
  163. Tantau H, Balko C, Brettschneider B, Melz G, Dörffling K (2004) Improved frost tolerance and winter survival in winter barley (Hordeum vulgare L.) by in vitro selection of proline over-accumulating lines. Euphytica 139:19–32Google Scholar
  164. Taschler D, Neuner G (2004) Summer frost resistance and freezing patterns measured in situ in leaves of major alpine plant growth forms in relation to their upper distribution boundary. Plant Cell Environ 27:737–746Google Scholar
  165. Tervit HR, Adams SL, Roberts RD, McGowan LT, Pugh PA, Smith JF, Janke AR (2005) Successful cryopreservation of Pacific oyster (Crassostrea gigas) oocytes. Cryobiology 51:142–151PubMedGoogle Scholar
  166. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599PubMedGoogle Scholar
  167. Trotsenko YA, Khmelenina VN (2005) Aerobic methanotrophic bacteria of cold ecosystems. FEMS Microbiol Ecol 53:15–26PubMedGoogle Scholar
  168. Turkiewicz M, Pazgier M, Kalinowska H, Bielecki S (2003) A cold-adapted extracellular serine proteinase of the yeast Leucosporidium antarcticum. Extremophiles 7:435–442PubMedGoogle Scholar
  169. Tutino ML, Duilio A, Parrilli E, Remaut E, Sannia G, Marino G (2001) A novel replication element from an Antarctic plasmid as a tool for the expression of proteins at low temperatures. Extremophiles 5:257–264PubMedGoogle Scholar
  170. Tyshenko MG, Walker VK (2004) Hyperactive spruce budworm antifreeze protein expression in transgenic Drosophila does not confer cold shock tolerance. Cryobiology 49:28–36PubMedGoogle Scholar
  171. Uemura M, Yoshida S (1984) Involvement of plasma membrane alterations in cold acclimation of winter rye seedlings (Secale cereale L. cv Puma). Plant Physiol 75:818–826PubMedGoogle Scholar
  172. Uemura M, Joseph RA, Steponkus PL (1995) Cold acclimation of Arabidopsis thaliana. Effect on plasma membrane lipid composition and freeze-induced lesions. Plant Physiol 109:15–30PubMedGoogle Scholar
  173. Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A (2006) Responses of the plasma membrane to low temperatures. Physiol Plant 126:81–89Google Scholar
  174. Ulmer W (1937) Über den Jahresgang der Frosthärte einiger immergrüner Arten der alpinen Stufe, sowie Zirbe und Fichte. Jb Wiss Bot 84:553–592Google Scholar
  175. Van Buskirk HA, Thomashow MF (2006) Arabidopsis transcription factors regulating cold acclimation. Physiol Plant 126:72–80Google Scholar
  176. Vigh L, Los DA, Horvath I, Murata N (1993) The primary signal in the biological perception of temperature: Pd-catalyzed hydrogenation of membrane lipids stimulated the expression of the desA gene in Synechocystis PCC6803. Proc Natl Acad Sci USA 90:9090–9094PubMedGoogle Scholar
  177. Voituron Y, Servais S, Romestaing C, Douki T, Barré H (2005) Oxidative DNA damage and antioxidant defenses in the European common lizard (Lacerta vivipara) in supercooled and frozen states. Cryobiology 51(1):74–82Google Scholar
  178. Wallis JG, Wang H, Guerra DJ (1997) Expression of a synthetic antifreeze protein in potato reduces electrolyte release at freezing temperatures. Plant Mol Biol 35:323–330PubMedGoogle Scholar
  179. Webb MS, Uemura M, Steponkus PL (1994) A comparison of freezing injury in oat and rye—two cereals at the extremes of freezing tolerance. Plant Physiol 104:467–478PubMedGoogle Scholar
  180. Weber MHW, Marahiel MA (2002) Coping with the cold: the cold shock response in the soil bacterium Bacillus subtilis. Philos Trans R Soc Lond B Biol Sci 357:895–907PubMedGoogle Scholar
  181. Wharton DA (2003) The environmental physiology of Antarctic terrestrial nematodes: a review. J Comp Physiol [B] 173:621–628Google Scholar
  182. Wharton DA, Barrett J, Goodall G, Marshall CJ, Ramlov H (2005) Ice-active proteins from the Antarctic nematode Panagrolaimus davidi. Cryobiology 51:198–207PubMedGoogle Scholar
  183. Wildt DE (2000) Genome resource banking for wildlife research, management, and conservation. ILAR J 41:228–234PubMedGoogle Scholar
  184. Wise MJ, Tunnacliffe A (2004) Popp the question: what do Lea proteins do? Trends Plant Sci 9:13–17PubMedGoogle Scholar
  185. Wisniewski M, Fuller M (1999) Ice nucleation and deep supercooling in plants: new insights using infrared thermography. In: Margesin R, Schinner F (eds) Cold adapted organisms. Ecology, physiology, enzymology and molecular biology. Springer, Berlin Heidelberg New York, pp 105–118Google Scholar
  186. Wisniewski M, Lindow SE, Ashworth EN (1997) Observations of ice nucleation and propagation in plants using infrared video thermography. Plant Physiol 113:327–334PubMedGoogle Scholar
  187. Wisniewski M, Bassett C, Gusta LV (2003) An overview of cold hardiness in woody plants: seeing the forest through the trees. HortScience 38:952–959Google Scholar
  188. Wolfe DA, Hameedi MH, Galt JA, Watabayashi G, Shrot J, O’Claire C, Rice S, Michel J, Payne JR, Braddock J, Hanna S, Sale D (1994) The fate of the oil spilled from the Exxon Valdez. Environ Sci Technol 28:561A–568ACrossRefGoogle Scholar
  189. Wong PTW, McBeath JH (1999) Plant protection by cold-adapted fungi. In: Margesin R, Schinner F (eds) Biotechnological applications of cold-adapted organisms. Springer, Berlin Heidelberg New York, pp 177–190Google Scholar
  190. Xin Z, Browse J (2000) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23:893–902Google Scholar
  191. Yaginuma O, Yamashita O (1979) NAD-dependent sorbitol dehydrogenase activity in relation to the termination of diapause in eggs of Bombyx mori. Insect Biochem 9:547–553Google Scholar
  192. Yin LJ, Chen ML, Tzeng SS, Chiou TK, Jiang ST (2005) Properties of extracellular ice-nucleating substances from Pseudomonas fluorescens MACK-4 and its effect on the freezing of some food materials. Fisheries Sci 71:941–947Google Scholar
  193. Yokoigawa K, Okubo Y, Soda K, Misono H (2003) Improvement in thermostability and psychrophilicity of psychrophilic alanine racemase by site-directed mutagenesis. J Mol Catal B Enzym 23:389–395Google Scholar
  194. Zachariassen KE, Kristiansen E (2000) Ice nucleation and antinucleation in nature. Cryobiology 41:257–279PubMedGoogle Scholar
  195. Zbikowska HM (2003) Fish can be first—advances in fish transgenesis for commercial applications. Transgenic Res 12:379–389PubMedGoogle Scholar
  196. Zhu J-J, Beck E (1991) Water relations of Pachysandra leaves during freezing and thawing. Plant Physiol 97:1146–1153PubMedCrossRefGoogle Scholar

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© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Institute of MicrobiologyLeopold Franzens UniversityInnsbruckAustria
  2. 2.Institute of BotanyLeopold Franzens UniversityInnsbruckAustria
  3. 3.Department of BiologyCarleton UniversityOttawaCanada

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