Cryopreservation of eukaryotic algae - A review of methodologies

Journal of Applied Phycology

Volumn 10, Issue 5, 1998, Pages 481-501

  Taylor, Rebecca ^a   Fletcher, Robert L ^b  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF PORTSMOUTH   (United Kingdom)

Author keywords

Cooling rate; Cryopreservation; Cryoprotectant; Freezing tolerance; Macroalgae; Microalgae; Storage

Indexed keywords

ALGAL CELL CULTURE; CELL DAMAGE; CELL VIABILITY; CRYOPRESERVATION; FREEZING; METHODOLOGY; TEMPERATURE;

ALGA; CRYOPRESERVATION; METHODOLOGY;

EID: 0032456625     PISSN: 09218971     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1008094622412     Document Type: Review

References (90)

1. Andersen RA (1996) Algae. In: Hunter-Cevera JC, Belt A (eds), Maintaining Cultures for Biotechnology and Industry. Academic Press, San Diego: 29-64.
2. Arbault S, Renard P, Pérez R, Kass R (1990) Essai de cryoconservation des gamétophytes de l'algue alimentaire Undaria pinnatifida (Laminariales). Aquat. Living Resour. 3: 207-215.
3. Arbault S, Delanoue F (1994) Cryoconservation du conchocelis de Porphyra linearis (Rhodophyceae). Cryoptogamie Algol. 15: 65-72.
4. Bajaj YPS, Reinert J (1977) Cryobiology of plant cell cultures and establishment of gene banks. In: Reinert J, Bajaj YPS (eds), Applied and Fundamental Aspects of Plant Cell, Tissue and Organ Culture. Springer-Verlag, Berlin: 575-789.
5. Ben-Amotz A, Gilboa A (1980a) Cryopreservation of marine unicellular algae. 1. A survey of algae with regard to size, culture, age, photosynthetic activity and chlorophyll-to-cell ratio. Mar. Ecol. Progr. Ser. 2: 157-161.
6. Ben-Amotz A, Gilboa A (1980b) Cryopreservation of marine unicellular algae. 2. Induction of freezing tolerance. Mar. Ecol. Progr. Ser. 2: 221-224.
7. Benhra A, Ferard JF, Vasseur P (1994) Factorial design to optimise the viability of the alga Scenedesmus subspicatus after cryopreservation. Cryo-Letters 15: 269-278.
8. Biebl R 1958) Temperature und osmotische Resistenz von Meeresalgen der bretonischen Kuste. Protoplasma 50: 217-242.
9. Biebl R (1962) Seaweeds. In: Lewin RA (ed.), Physiology and Biochemistry of the Algae. Academic Press, New York: 799-815.
10. Bird CJ, McLachlan J (1974) Cold hardiness of zygotes and embryos of Fucus (Phaeophyceae, Fucales). Phycologia 13: 215-225.
11. Bodas K, Brennig C, Diller KR, Brand JJ (1995) Cryopreservation of blue-green and eukaryotic algae in the culture collection at the University of Texas at Austin. Cryo- Letters 16: 267-274.
12. Brown S, Day JG (1993) An improved method for the long-term preservation of Naegleria gruben. Cryo-Letters 14: 347-352.
13. Cañavate JP, Lubian LM (1994) Tolerance of six marine microalgae to the cryoprotectants DMSO and methanol. J. Phycol. 30: 559-565.
14. Cañavate JP, Lubian LM (1995a) Some aspects of the cryopreservation of microalgae used as food for marine species. Aquaculture 136: 277-290.
15. Cañavate JP, Lubian LM (1995b) Relationship between cooling rates, cryoprotectant concentrations and salinities in the cryopreservation of marine microalgae. Mar. Biol. 124: 325-334.
16. Cañavate JP, Lubian LM (1997a) Effects of culture age on cryopreservation of marine microalgae. Eur. J. Phycol. 32: 87-90.
17. Cañavate JP, Lubian LM (1997b) Effects of slow and rapid warming on the cryopreservation of marine microalgae. Cryobiology 35: 143-149.
18. Cohn F (1871) Das Gefrieren der Zellen von Nitella syncarpa. Bot. Zeit. 29: 723-744.
19. Cordero B, Voltolina D (1997) Viability of mass algal cultures preserved by freezing and freeze-drying. Aquacultural Engineering 16: 205-211.
20. Day JG (1998) Cryo-conservation of microalgae and cyanobacteria. Cryo-Letters Supplement 1: 7-14.
21. Day JG, De Ville MM (1995) Cryopreservation of algae. In: Day JG, McLellan MR (eds), Methods in Molecular Biology, Volume 38: Cryopreservation and Freeze-Drying Protocols. Humana Press Inc., Totowa, NJ: 81-89.
22. Day JG, Fenwick C (1993) Cryopreservation of members of the genus Tetraselmis used in aquaculture. Aquaculture 118: 151-160.
23. Day JG, Fleck RA, Benson EE (1998) Cryopreservation of multicellular algae: problems and perspectives. Cryo-Letters 19: 205-206.
24. Day JG, Watanabe MM, Morris GJ, Fleck RA, McLellan MR (1997) Long-term viability of preserved eukaryotic algae. J. appl. Phycol. 9: 121-127.
25. Dudgeon SR, Davison IR, Validas RL (1989) Effect of freezing on photosynthesis of intertidal macroalgae: tolerance of Chondrus crispus and Mastocarpus stellatus (Rhodophyta). Mar. Biol. 101: 107-114.
26. Dudgeon SR, Davison IR, Vandas RL (1990) Freezing tolerance in the intertidal red algae Chondrus crispus and Mastocarpus stellatus: relative importance of acclimation and adaption. Mar. Biol. 106: 427-436.
27. Fahy GM (1986) The relevance of cryoprotectant toxicity to cryobiology. Cryobiology 23: 1-13.
28. Fenwick C, Day JG (1992) Cryopreservation of Tetraselmis suecica cultured under different nutrient regimes. J. appl. Phycol. 4: 105-109.
29. Fleck RA, Day JG, Rana KJ, Benson EE (1997) Visualisation of cryoinjury and freeze events in the coenocytic alga Vaucheria sessilis using cryomicroscopy. Cryo-Letters 18: 343-354.
30. Florio L, Stewart M, Mugrage ER (1943) The effect of freezing on erythrocytes. J. Lab. Clin. Med. 28: 1486-1491.
31. Gilboa A, Ben-Amotz A (1979) An improved method for rapid assaying of viability of cryopreserved unicellular algae. Plant Sci. Lett. 14: 317-320.
32. Ginsburger-Vogel T, Arbeult S, Pérez, R (1992) Ultrastructural study on the effect of freezing-thawing on the gametophytes of the brown alga Undaria pinnatifida. Aquaculture 106: 171-181.
33. Gresshoff PM (1977) Chlamydomonas reinhardi - a model plant system II. Cryopreservation. Plant Sci. Lett. 9: 23-25.
34. Grout BWW, Morris GJ (1987) Freezing and cellular organisation. In: Grout BWW, Morris GJ (eds), The effects of low temperature on biological systems. Edward Arnold, London: 147-174.
35. Hirata K, Phunchindawan M, Takamoto J, Goda S, Miyamoto K (1996) Cryopreservation of microalgae using encapsulation-dehydration. Cryo-Letters 17: 321-328.
36. Holm-Hansen O (1963) Viability of blue-green and green algae after freezing. Physiol. Pl. 16: 530-540.
37. Holm-Hansen O (1973) Preservation by freezing and freeze drying. In: Stein JR (ed.), Handbook of Phycological Methods - Culture Methods and Growth Measurements. Cambridge University Press, Cambridge: 195-205.
38. Hwang SW, Homeland W (1965) Survival of algal cultures after freezing by controlled and uncontrolled cooling. Cryobiology 1: 305-311.
39. Hwang SW, Hudock GA (1971) Stability of Chlamydomonas reinhardi in liquid nitrogen storage. J. Phycol. 7: 300-303.
40. Kanwisher JW (1957) Freezing and drying in intertidal algae. Biol. Bull. 113: 275-285.
41. Karha KK (1981) Meristem culture and cryopreservation - methods and applications. In: Thorpe TA (ed.), Plant Tissue Culture Methods and Applications in Agriculture. Academic Press, New York: 181-211.
42. Karlsson JOM, Toner M (1996) Long term storage of tissues by cryopreservation: critical issues. Biomaterials 17: 243-256.
43. Kuwano K, Aruga Y, Saga N (1992) Preliminary study on cryopreservation of the conchocelis of Porphyra yezoensis. Nippon Suisan Gakkaishi 58: 1793-1798.
44. Kuwano K, Aruga Y, Saga N (1993) Cryopreservation of the conchocelis of the marine alga Porphyra yezoensis Ueda (Rhodophyta) in liquid nitrogen. Plant Science 94: 215-225.
45. Kuwano K, Aruga Y, Saga N (1994) Cryopreservation of the conchocelis phase of Porphyra (Rhodophyta) by applying a simple prefreezing system. J. Phycol. 30: 566-570.
46. Kuwano K, Aruga Y, Saga N (1996) Cryopreservation of clonal gametophytic thalli of Porphyra (Rhodophyta). Plant Science 116: 117-124.
47. Kylin H (1917) Uber die Kalteresistenz der Meeresalgen. Ber. deutsch. bot. Ges. 35: 370-384.
48. Lee JJ, Soldo AT (1992) Protocols in protozoology. Society of Protozoologists, Lawrence, Kansas.
49. Leeson EA, Cann JP, Morris GJ (1984) Maintenance of algae and protozoa. In: Kirsop BE, Snell JJS (eds), Maintenance of Microorganisms. Academic Press, London: 131-160.
50. Leibo SP, Jones RF (1963) Effects of subzero temperatures on the unicellular red alga Porphyridiwn cruentum. J. Cell Comp. Physiol. 62: 295-302.
51. Leibo SP, Mazur P (1978) Methods for the preservation of mammalian embryos by freezing. In: Joseph Jr C (ed.), Methods in Mammalian Reproduction. Academic Press, New York: 179-201.
52. Lovelock JE (1953) The haemolysis of human red blood cells by freezing and thawing. Biochim. Biophys. Acta. 10: 414-426.
53. Marré E (1962) Temperature. In: Lewin RA (ed.), Physiology and Biochemistry of Algae. Academic Press, New York: 541-550.
54. Maurer RR (1978) Freezing mammalian embryos: a review of the techniques. Theriogenology 9: 45-68.
55. Mazur P (1960) Physical factors implicated in the death of microorganisms at subzero temperatures. Ann. NY Acad. Sci. 85: 610-629.
56. Mazur P (1970) Cryobiology: the freezing of biological systems. Science 168: 939-949.
57. Mazur P (1984) Freezing of living cells: mechanisms and implications. Am. J. Physiol. 247: 125-142.
58. Mazur P, Leibo S, Chu EHY (1972) A two-factor hypothesis of freezing injury. Exp. Cell Res. 71: 345-355.
59. McGee HA Jr, Martin WJ (1962) Cryochemistry. Cryogenics 2: 1-11.
60. McGrath MS, Dagget PM (1977) Cryopreservation of flagellar mutants of Chlamydomonas reinhardi. Can J. Bot. 55: 1794-1796.
61. McLellan MR (1989) Cryopreservation of diatoms. Diatom Res. 4: 301-318.
62. McLellan MR, Cowling AJ, Turner M, Day JG (1991) Maintenance of algae and protozoa. In: Kirsop BE, Doyle A (eds), Maintenance of Microorganisms and Cultured Cells. Academic Press, London: 183-208.
63. Meryman HT (1966) Review of biological freezing. In: Meryman HT (ed.), Cryobiology. Academic Press, New York: 1-114.
64. Meryman HT (1970) The exceeding of a minimum tolerable cell volume in hypertonic suspension as a cause of freezing injury. In: Wolstenholme GEW, O'Connor M (eds), The Frozen Cell: Ciba Foundation Symposium. Churchill, London: 51-64.
65. Meyer MA (1985) Cryopreservation of a marine diatom. PhD thesis, Texas A & M University, College Station. 112 pp.
66. Migita S (1964) Freeze-preservation of Porphyra thalli in a viable state. I. Viability of Porphyra tenera preserved at low temperature after freezing in seawater and freezing under half-dried conditions. Bull. Fac. Fish. Nagasaki Univ. 17: 44-54.
67. Migita S (1966) Freeze-preservation of Porphyra thalli in a viable state. II. Effect of cooling velocity and water content of thalli on the frost resistance. Bull. Fac. Fish. Nagasaki Univ. 21: 131-138.
68. Migita S (1967) Viability and spore liberation of the conchocelisphase of Porphyra tenera freeze preserved in seawater. Bull. Fac. Fish. Nagasaki Univ. 22: 33-43.
69. Morris GJ (1976a) The cryopreservation of Chlorella, 1. Interactions of rate of cooling, protective additive and warming rate. Arch. Microbiol. 107: 57-62.
70. Morris GJ (1976b) The cryopreservation of Chlorella. 2. Effect of growth temperature on freezing tolerance. Arch. Microbiol. 107: 309-312.
71. Morris GJ (1978) Cryopreservation of 250 Strains of Chlorococcales by the method of two-step cooling. Br. phycol. J. 13: 15-24.
72. Morris GJ (1981) Cryopreservation. An introduction of cryopreservation in culture collections. Institute of Terrestrial Ecology, Cambridge. 27 pp.
73. Morris GJ, Canning CE (1978) The cryopreservation of Euglena gracilis. J. gen. Microbiol. 108: 27-31.
74. Mortain-Bertrand A, Etchart F, Deboucaud MT (1996) A method for the cryoconservation of Dunaliella salina (Chlorophyceae) - Effect of glycerol and cold adaptation. J. Phycol. 32: 346-352.
75. Muldrew K, McGann LE (1990) Mechanisms of intracellular ice formation. Biophys. J. 57: 525-532.
76. Parker J (1960) Seasonal changes in cold-hardiness of Fucus vesiculosus. Biol. Bull. 119: 474-478.
77. Polge C, Smith AU, Parkes AS (1949) Revival of spermatozoa after vitrification and dehydration at low temperature. Nature 164: 166.
78. Rall WF, Fahy GM (1985) Ice-free cryopreservation of mouse embryos by vitrification. Nature 313: 573-575.
79. Renard P, Arbault S, Kaas R, Perez R (1992) A method for the cryopreservation of the gametophytes of the food alga Undaria pinnatifida (Laminariales). Comptes Red. Acad. Sci. serie III - Life Sciences 315: 445-451.
80. Saks NM (1978) The preservation of salt marsh algae by controlled liquid nitrogen freezing. Cryobiology 15: 563-568.
81. Snell JJS (1991) General introduction to maintenance methods. In: Kirsop BE, Doyle A (eds), Maintenance of Microorganisms and Cultured Cells. Academic Press, London: 21-30.
82. Steponkus PL, Dowgert MF, Gordon-Kamm WJ (1983) Destabilization of the plasma membrane of isolated plant protoplasts during a freeze-thaw cycle: the influence of cold acclimation. Cryobiology 20: 448-465.
83. Steponkus PL, Langis R, Fujikawa S (1992) Cryopreservation of plant tissues by vitrification. In: Steponkus PL (ed.), Advances in Low-Temperature Biology, Volume 1. JAI Press, London: 1-61.
84. Terumoto I (1961) Frost resistance in the marine alga Enteromorpha intestinalis (L) Link. Low Temp. Sci. Ser. 19: 23-28.
85. Tsuru S (1973) Preservation of marine and freshwater algae by means of freezing and freez-drying. Cryobiology 10: 445-452.
86. van den Hoek C, Mann DG, Jahns HM (1995) Algae - An Introduction to Phycology. Cambridge University Press, Cambridge. 623 pp.
87. van der Meer JP, Simpson FJ (1984) Cryopreservation of Gracilaria tikvahiae (Rhodophyta) and other macrophytic marine algae. Phycologia 23: 195-202.
88. Vigneron T, Arbeult S, Kaas R (1997) Cryopreservation of gametophytes of Laminaria digitata (L) Lamouroux by encapsulated dehydration. Cryo-Letters 18: 93-98.
89. Warren A, Day JG, Brown S (1997) Cultivation of algae and protozoa: In: Hurst CJ, Knudsen GR, McInerney MJ, Stezenbach LD, Walter MV (eds), Manual of Environmental Microbiology. ASM Press, Washington: 61-71.
90. Woodcock AH, Thistle MW, Cook WH, Gibbons NE (1941) The ability of sheep's erythrocytes to survive freezing. Can. J. Res. 19: 206-212.