Algae at Extreme Low Temperatures

The Cryobank
  • Erica Benson
  • Keith Harding
  • John G. Day

In vitro cryopreservation is the storage of viable cells at ultra-low temperatures (196ºC), usually in liquid nitrogen or its vapor phase. Under these conditions it is assumed that metabolism is arrested and cells are stable for indefinite periods, so long as liquid nitrogen supply is maintained. The fact that cells tolerate cryogenic temperatures is remarkable as survival after cryopreservation is common to a wide range of biodiversity. The in vitro cryobank is one of the most, if not the most extreme low-temperature environment that an organism, or component part thereof, will ever encounter on earth. It is fascinating to speculate how, with the aid of cryoprotection (Fuller, 2004) so many diverse life-forms survive such extreme cold. Cryopreservation has important applications for astrobiology and in vivo studies of extremophiles; as water and temperature are physical determinants of life, indeed water is a prerequisite for life. This chapter considers cryoconservation in a wider context, appraising the comparative utilities of both natural and artificial cryobanks as repositories and research tools that may be used to help understand how life survives extreme cold. Algae are the subject of choice as they are one of the oldest and most diverse groups of organisms; their ancestral, fossil remains have been found in strata dating from 1.4 billion to 2.1 billion years (Cloud et al., 1969; Han and Runnegar, 1992). Algae are ubiquitous primary producers and formidable extremophiles, yet, compared with other biological resources, their preservation in cryobanks (Day et al., 2005) and their utilization as a valuable economic resource remains limited.

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References

  1. Adelman, R., Saul, R.L. and Ames, B.N. (1988) Oxidative damage to DNA: relation to species meta-bolic rate and life span. Proc. Natl. Acad. Sci. USA 85, 2706-2708.CrossRefPubMedGoogle Scholar
  2. Andersen, R.A. (1996) Algae, in: J.C. Hunter-Cevera and A. Belt (eds.) Maintaining Cultures for Biotechnology and Industry. Academic Press, London, UK, pp. 29-64.CrossRefGoogle Scholar
  3. Andersen, R.A. (2005) The Provasoli-Guillard National Center for Culture of Marine Phytoplankton: past, present and future, in: F. Kasai, K. Kaya and M.M. Watanabe (eds.) Culture Collections and Environmental Research. Tokai University Press, Tokyo, pp. 65-72. 73-86.Google Scholar
  4. Kaya K. and Kasai F. (eds.). Ball, P. (ed.) (2003) H2O A Biography of Water, Phoenix, Orion Books Ltd., London, UK.Google Scholar
  5. Benson, E.E. (2004) Cryo-conserving algal and plant diversity: historical perspectives and future chal-lenges, in: B. Fuller, N. Lane and E.E. Benson (eds.) Life in the Frozen State. CRC Press, London, UK, pp. 299-328.Google Scholar
  6. Benson, E.E. (2006) Cryopreservation theory, in: B.M. Reed(ed.) In Plant Cryopreservation: A Practical Guide. Springer, Heidelberg..Google Scholar
  7. Benson, E.E. and Bremner, D.H. (2004) Oxidative stress in the frozen plant: a free radical point of view, in: B. Fuller, N. Lane and E.E. Benson (eds.) Life in the Frozen State. CRC Press, London, UK, pp. 205-242.Google Scholar
  8. Benson, E.E., Johnston, J., Muthusamy, J. and Harding, K. (2005) Physical and engineering perspec-tives of in vitro plant cryopreservation, in: S. Dutta Gupta and Y. Ibaraki (eds.) Plant Tissue Culture Engineering. Springer, Dordrecht, Netherlands, pp. 441-473.Google Scholar
  9. Bodas, K., Brennig, C., Diller, K.R. and Brand, J.J. (1995) Cryopreservation of blue-green and eukary-otic algae in the culture collection at the University of Texas at Austin. Cryo Letters 16, 267-274.Google Scholar
  10. Buitink, J., LePrince, O., Hemminga, M.A. and Hoekstra, A.A. (2000) Molecular mobility in the cyto-plasm: an approach to describe and predict lifespan in dry germplasm. Proc. Natl. Acad. Sci. USA 97, 2385-2390.CrossRefPubMedGoogle Scholar
  11. Cloud, P.E. Jr., Licori, G.R., Wright, L.R. and Troxel, B.W. (1969) Proterozoic eukaryotes from Eastern California. Proc. Natl. Acad. Sci. USA 63, 623-630.CrossRefGoogle Scholar
  12. Day, J.G. and Brand, J.J. (2005) Cryopreservation methods for maintaining cultures, in: R.A. Andersen (ed.) Algal Culturing Techniques. Academic Press, New York. pp. 165-187.CrossRefGoogle Scholar
  13. Day, J.G. and Harding, K. (2006) Cryopreservation of algae, in: B.M. Reed (ed.) Plant Cryopreservation: A Practical Guide. Springer, Heidelberg.Google Scholar
  14. Day, J.G., Watanabe, M.M., Morris, G.J., Fleck, R.A. and McLellan, M.R. (1997) Long-term viabil-ity of preserved eukaryotic algae. J. Appl. Phycol. 9, 121-127.CrossRefGoogle Scholar
  15. Day, J.G., Benson, E.E. and Fleck, R.A. (1999) In Vitro culture and conservation of microalgae: applica-tions for aquaculture, biotechnology and environmental research. In Vitro Plant Cell 35, 127-136.CrossRefGoogle Scholar
  16. Day, J.G., Fleck, R.A. and Benson, E.E. (2000) Cryopreservation-recalcitrance in microalgae: novel approaches to identify and avoid cryo-injury. J. Appl. Phycol. 12, 369-377.CrossRefGoogle Scholar
  17. Day, J.G., Benson, E.E., Harding, K., Knowles, B., Idowu, M., Bremner, D., Santos, L., Santos, F., Friedl, T., Lorenz, M., Lukesova, A., Elster, J., Lukavsky, J., Herdman, M., Rippka, R. and Hall, T. (2005) Cryopreservation and conservation of microalgae: the development of a pan-European scientific and biotechnological resource (the COBRA project). Cryo Letters 26, 231-238.PubMedGoogle Scholar
  18. Diller, K.R. (1997) Pioneers in cryobiology: Nikolay Aleksandrovich Maximov (1890-1952). Cryo Letters 18, 81-92.Google Scholar
  19. Elster, J. and Benson, E.E. (2004) Life in the polar terrestrial environment: a focus on algae and cyanobacteria, in: B. Fuller, N. Lane and E.E. Benson (eds.) Life in the Frozen State. CRC Press, London, UK, pp. 111-150.Google Scholar
  20. Fahy, G.M., Wowk, B., Wu, J. and Paynter, S. (2004) Improved vitrification solutions based on the pre-dictability of vitrification solution toxicity. Cryobiology 48, 22-35.CrossRefPubMedGoogle Scholar
  21. Fleck, R.A., Pickup, R.W., Day, J.G. and Benson, E.E. (2006) Characterisation of cryoinjury in Euglena gracilis using flow-cytometry and cryomicroscopy. Cryobiology 52, 261-268.CrossRefPubMedGoogle Scholar
  22. Floyd, R.A., West, M. and Hensley, K. (2001) Oxidative biochemical markers: clues to understanding ageing in long-lived species. Experimental Geritology 36, 619-640.CrossRefGoogle Scholar
  23. Friedl, T. and Lorenz, M. (2002) The SAG culture collection: microalgal biodiversity and phylogeny research, in: Abstracts of Culture Collections of Algae: Increasing Accessibility and Exploring Algal Biodiversity. 2-6 September 2002, Sammlung von Algenkulturen (SAG), Göttingen University, Germany.Google Scholar
  24. Fuller, B. (2004) Cryoprotectants: the essential antifreezes to protect life in the frozen state. Cryo Letters 25, 375-388.PubMedGoogle Scholar
  25. Fuller, B., Lane, N. and Benson E.E. (eds.) (2004) Life in the Frozen State, CRC Press, Boca Raton, London, UK.Google Scholar
  26. Han, T.M. and Runnegar, B. (1992) Megascopic eukaryotic algae from the 2.1-billion-year-old Negaunee iron formation. Mich. Sci. 257, 232-235.Google Scholar
  27. Harding, K. (1999). Stability assessments of conserved plant germplasm, in: E.E. Benson (ed.) Plant Conservation and Biotechnology. Taylor and Francis Ltd., London, UK, pp. 97-107.Google Scholar
  28. Harding, K. (2004) Genetic integrity of cryopreserved plant cells: A review. Cryo Letters 25, 3-22.PubMedGoogle Scholar
  29. Harding, K., Day, J.G., Lorenz, M., Timmerman, H., Friedl, T., Bremner, D.H. and Benson, E.E. (2004) Introducing the concept and application of vitrification for the cryo-conservation of algae - A mini-review. Nova Hedwigia 79, 207-226.CrossRefGoogle Scholar
  30. Harding, K., Johnston, J. and Benson, E.E. (2005) Plant and algal cell cryopreservation: issues in genetic integrity, concepts in ‘Cryobionomics’ and current European applications, in: I.J. Benett, E. Bunn, H. Clarke and J.A. McComb (eds.) Conference of the Australian Branch of the IATPC and Biotechnology - Contributing to a Sustainable Future. Perth, WA, Australia, pp. 112-119.Google Scholar
  31. Hawksworth, D.L. (ed.) (1999) World Federation for Culture Collections guidelines for the establish-ment and operation of collections of cultures of microorganisms. WFCC Cambridge, UK.Google Scholar
  32. Hoover, R.B. (2006) Comets, carbonaceous meteorites and the origin of the biosphere. Biogeosci. Discuss. 3, 23-70.CrossRefGoogle Scholar
  33. Jaworski, G.H.M., Wiseman, S.W. and Reynolds, C.S. (1988) Variability in sinking rate of the fresh-water diatom Asterionella formosa: the influence of colony morphology. Br. Phycol. J. 23, 167-176.CrossRefGoogle Scholar
  34. Johnstone, C., Block, W., Benson, E.E., Day, J.G., Staines, H. and Illian, J.B. (2002) Assessing meth-ods for collecting and transferring viable algae from Signy Island, maritime Antarctic to the UK. Polar Biol. 25, 553-556.CrossRefGoogle Scholar
  35. Johnstone, C., Day, J.G., Staines, H. and Benson, E.E. (2006a) Development of 2,2′-azinobis-(3-ethyl-benzothiazoline-6-sulfonic acid)radical cation decolourisation assay for evaluating total antioxidant status in an alga used to monitor environmental impacts in urban aquatic habitats. Ecol. Indicators 6, 280-289.CrossRefGoogle Scholar
  36. Johnstone, C., Day, J.G., Staines, H. and Benson, E.E. (2006b) An in vitro oxidative stress test for determining pollutant tolerance in algae. Ecol. Indicators. 6, 770-779.CrossRefGoogle Scholar
  37. Jokipii, S., Ryynanen, L., Kallio, P.T., Aronen, T. and Haggman, H. (2004) A cryopreservation method maintaining the genetic fidelity of a model forest tree, Populus tremula L. X Populus tremuloides Michx. Plant Sci. 166, 799-806.CrossRefGoogle Scholar
  38. Kanervo, E., Lehto, K., Ståhle, K., Lehto, H. and Mäenpää, P. (2005) Characterization of growth and photosynthesis of Synechocystis sp. PCC 6803 cultures under reduced atmospheric pressures and enhanced CO2 levels. Int. J. Astrobiol. 4, 97-100.CrossRefGoogle Scholar
  39. Keys, B., Serra V., Saretzki, G. and von Zglinicki, T. (2004) Telomere shortening in human fibroblasts is not dependent upon the size of the telomeric-3′-overhang. Aging Cell 3, 103-114.CrossRefPubMedGoogle Scholar
  40. Kirsop, B.E. (1999) Service collections: their functions, in: B. Kirsop and A. Doyle (eds.) Maintenance of Microorganisms. Academic Press Ltd., London, pp. 5-20.Google Scholar
  41. Kobabe S., Wagner D. and Pfeiffer, E-V. (2004) Characterisation of microbial community composi-tion of a Siberian tundra soil by fluorescence in situ hybridization. FEMS Microbiol. Ecol. 50, 13-23.CrossRefPubMedGoogle Scholar
  42. Kuzmina, J. (2004) Progress Report on Cryopreservation at the University of Toronto Culture Collection of Algae and Cyanobacteria. University of Toronto, Toronto, Canada.Google Scholar
  43. Lane, N. (ed.) (2002) Oxygen the Molecule that Made the World. Oxford University Press, Oxford UK.Google Scholar
  44. Laybourn-Parry, J. (2002) Survival mechanisms in Antarctic lakes. Philos. Trans. R. Soc. Lond. B. 357, 863-869.CrossRefGoogle Scholar
  45. Lee, J.J. and Soldo, A.T. (eds.) (1992) Protocols in Protozoology. Society of Protozoologists, Lawrence, Kansas, USA.Google Scholar
  46. Leibo, S.P. (2004) The early history of gamete cryobiology, in: B. Fuller, N. Lane and E.E. Benson (eds.) Life in the Frozen State. CRC Press, London, UK, pp. 347-370.Google Scholar
  47. Leibo, S.P., Semple, M.E. and Kroetsch, T.G. (1994) In vitro fertilization of oocytes by 37-year-old cryopreserved bovine spermatozoa. Theriogenology 42, 1257-1262.CrossRefGoogle Scholar
  48. Liu, Y., Wang, X. and Liu, L (2004) Analysis of genetic variation in surviving apple shoots following cryopreservation by vitrification. Plant Sci. 166, 677-685.CrossRefGoogle Scholar
  49. Lorenz, M., Friedl, T. and Day, J.G. (2005) Perpetual Maintenance of Actively Metabolizing Microalgal Cultures, in: R.A. Andersen (ed.) Algal Culturing Techniques, Academic Press, New York, pp. 145-155.CrossRefGoogle Scholar
  50. Lovelock, J.E. (1953) The mechanism of the cryoprotective effect of glycerol against haemolysis by freezing and thawing. Biochim. Biophys. Acta 11, 28-36.CrossRefPubMedGoogle Scholar
  51. , J. (2003) Sbirka autotrofnich organismu AV CR (Collection of autotrophic organisms of the AS CR), Ziva 3, 36-37.Google Scholar
  52. Mazur, P. (2004) Principles of cryobiology, in: B. Fuller, N. Lane and E.E. Benson (eds.) Life in the Frozen State. CRC Press, London, UK, pp. 3-66.Google Scholar
  53. McCormick, P.V. and Cairns, J. (1994) Algae as indicators of environmental change. J. Appl. Phycol. 6,509-526.CrossRefGoogle Scholar
  54. McLellan, M.R., Cowling, A.J., Turner, M.F. and Day, J.G. (1991) Maintenance of algae and proto-zoa, in: B. Kirsop and A. Doyle (eds.) Maintenance of Microorganisms. Academic Press Ltd., London, pp. 183-208.Google Scholar
  55. Meryman, H.T. and Williams, R.J. (1985) Basic principles of freezing injury to plant cells: natural tol-erance and approaches to cryopreservation, in: K.K. Kartha (ed) Cryopreservation of plant cells and organs. CRC Press Inc. Boca Raton, Florida, USA, pp. 14-47.Google Scholar
  56. Mileikowsky, C., Cucinotta, F.A., Wilson, J.W., Gladman, B., Horneck, G., Lindegren, L., Melosh, J., Rickman, H., Valtonen, M. and Zheng, J.Q. (2000) Natural transfer of viable microbes in space 1. From Mars to Earth and Earth to Mars. Icarus 145, 391-427.CrossRefPubMedGoogle Scholar
  57. Morris, G.J. (1978) Cryopreservation of 250 strains of Chlorococcales by the method of two step cool-ing. Br. Phycol. J. 13, 15-24.CrossRefGoogle Scholar
  58. Müller, J., Friedl, T., Hepperle, D., Lorenz, M. and Day, J.G. (2005) Distinction of isolates among multiple strains of Chlorella vulgaris (Chlorophyta, Trebouxiophyceae) and Testing Conspecificity with Amplified Fragment Length Polymorphism and ITS RDNA sequences. J. Phycol. 41, 1236-1247.CrossRefGoogle Scholar
  59. Murthy, N.U.M., Kumar, P.P. and Sun, W.Q. (2003) Mechanisms of seed ageing under different stor-age conditions for Vigna radiate L. Wilczek: Lipid peroxidation, sugar hydrolysis and their relationship to glass transition state. J. Exp. Bot. 54, 1057-1067.CrossRefPubMedGoogle Scholar
  60. Osorio, H., Laranjeriro, N., Santos, L.M.A. and Santos, M.F. (2004) First attempts at cryopreserva-tion of ACOI strains and use of image analysis to assess viability. Nova Hedwigia 79, 227-236.CrossRefGoogle Scholar
  61. Polge, C., Smith, A.U. and Parkes, A.S. (1949) Revival of spermatozoa after vitrification and dehy-dration at low temperatures. Nature 164, 666.CrossRefPubMedGoogle Scholar
  62. Ponder, M., Vishnivetskaya, T., McGrath, J. and Tiedje, J. (2004) Microbial life in permafrost: extended times in extreme conditions, in: B. Fuller, N. Lane and E.E. Benson (eds.) Life in the Frozen State. CRC Press, London, UK, pp. 151-169.Google Scholar
  63. Rhodes, L., Smith, J., Tervit, R., Roberts, R., Adamson, J., Adams, S. and Decker, M. (2006) Cryopreservation of economically valuable marine micro-algae in the classes of Bacillariophyceae, Chlorophyceae, Cyano phyceae, Haptophyceae, Prasinophyceae, and Rhodophyceae. Cryobiology 52, 152-156.CrossRefPubMedGoogle Scholar
  64. Rippka, R., Iteman, I., Coursin, T., Comte, K., Singer, A., Araoz, R., Laurent, T., Herdman, M. and Tandeau de Marsac, N. (2002) Recent progress in the Pasteur culture collection of cyanobacte-ria, in: Abstracts of Culture Collections of Algae: increasing accessibility and exploring Algal Biodiversity. 2-6 September 2002, Sammlung von Algenkulturen (SAG), Göttingen University, Germany.Google Scholar
  65. Rosing, M.T. (2005) Thermodynamics of life on the planetary scale. Int. J. Astrobiol. 4, 9-11.CrossRefGoogle Scholar
  66. Rothschild, L.J. and Mancinelli, R.L. (2001) Life in extreme environments. Nature 409, 1092-1101.CrossRefPubMedGoogle Scholar
  67. Smith, L.C., MacDonald, G.M., Velchiko, A.A., Beilman, D.W., Borisova, O.K., Frey, K.E., Kremenetski, K.V. and Sheng, Y. (2004) Siberian peatlands a net carbon sink and global methane sources since the early halocene. Science 308, 353-356.CrossRefGoogle Scholar
  68. Soina, V.S., Mulyukin, A.L., Demkina, E.V., Vorobyova, E.A. and El-Registan, G.I. (2004) The struc-ture of resting bacterial populations in soil and subsoil permafrost. Astrobiology 4, 345-358.CrossRefPubMedGoogle Scholar
  69. Stacey, G.N. and Day, J.G. (2006) Long-term ex situ conservation of biological resources and the role of biological resource centres, in: J.G. Day and G.N. Stacey (eds.) Cryopreservation and Freezedrying Protocols. Humana Press, Totowa, NJ, USA.Google Scholar
  70. Vishnivetskaya, T., Kathariou, S., McGrath, J., Gilichinsky, D. and Tiedje, J.M. (2000) Low-temperature recovery strategies for the isolation of bacteria from ancient permafrost sediments. Extremophiles 4,165-173.CrossRefPubMedGoogle Scholar
  71. Vishnivetskaya, T.A., Spirina, E.V., Shatilovich, A.V., Erokhina, L.G., Vorobyova, E.A. and Gilichinsky, D.A. (2003) The resistance of viable permafrost algae to simulated environmental stresses: implications for astrobiology. Int. J. Astrobiol. 2, 171-177.CrossRefGoogle Scholar
  72. Volk, G.M. and Walters, C. (2006) Plant vitrification solution 2 lowers water content and alters freez-ing behaviour in shoot tips during cryoprotection. Cryobiology 52, 48-61.CrossRefPubMedGoogle Scholar
  73. Vorobyova, E., Soina, V., Gorlenko, M., Minkovskaya, N., Zalinova, N., Mamukelashvili, A., Gilichinsky, D., Rivkina, E. and Vishnivetskaya, T. (1997) The deep cold biosphere: facts and hypothesis. FEMS Microbiol. Rev. 20, 277-290.Google Scholar
  74. Wainwright, M., Wickramasinghe, N.C., Narlikar, J.V., Rajaratnam, P. and Perkins, J. (2004) Confirmation of the presence of viable but non-culturable bacteria in the stratosphere. Int. J. Astrobiol. 3, 13-15.CrossRefGoogle Scholar
  75. Wallis, M.K. and Wickramasinghe, N.C. (2004) Interstellar transfer of planetary microbiota. Mon. Not. R. Astron. Soc. 348, 52-61.CrossRefGoogle Scholar
  76. Walters, C. (2004) Temperature dependency of molecular mobility in preserved seeds. Biophys. J. 86, 1253-1258.CrossRefPubMedGoogle Scholar
  77. Walters, C., Wheeler, L. and Stanwood, P.C. (2004) Longevity of cryogenically stored seeds. Cryobiology 48, 229-244.CrossRefPubMedGoogle Scholar
  78. Watanabe, M.M., Shimizu, A. and Satake, K. (1992) NIES-Microbial Culture Collection at the National Institute of Environmental Studies: cryopreservation and database of culture strains of microalgae, in: M.M. Watanabe (ed.) Proceedings of Symposium on Culture Collection of Algae. NIES, Tsukuba, Japan, pp. 33-41.Google Scholar
  79. Watanabe, M.M., Nozaki, H., Kasai, H., Sano, S., Kato, N., Omori, Y. and Hohara, S. (2005) Threatened states of the Charales in the Lakes of Japan, in: F. Kasai, K. Kaya and M.M. Watanabe (eds) Culture Collections and Environmental Research. Tokai University Press, Tokyo, Japan, pp. 217-236.Google Scholar
  80. Wickramasinghe, C. (2004) The Universe as a cryogenic habitat for microbial life. Cryobiology 48, 113-125.CrossRefPubMedGoogle Scholar
  81. Wiessner, W., Schnepf, E. and Starr, R.C. (eds.) (1995) Algae, Environment and Human Affairs, Biopress Ltd., Bristol, UK.Google Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Erica Benson
    • 1
  • Keith Harding
    • 1
  • John G. Day
    • 2
  1. 1.Research Scientists, ConservationEnvironmental Science and BiotechnologyDamarUK
  2. 2.Curator, Culture Collection of Algae and Protozoa, Scottish Association for Marine ScienceDunstaffnage Marine LaboratoryDunbegUK

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