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Adaptations to environmental extremes by multicellular organisms

Published online by Cambridge University Press:  09 July 2007

Mohammed Riajul Islam  and
Dirk Schulze-Makuch
Mohammed Riajul Islam
Affiliation:
School of Earth and Environmental Sciences, Washington State University, Pullman, WA 99164, USA e-mail: dirksm@wsu.edu
Dirk Schulze-Makuch
Affiliation:
School of Earth and Environmental Sciences, Washington State University, Pullman, WA 99164, USA e-mail: dirksm@wsu.edu
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Abstract

Microbes, particularly Archaea, are well-known for their superb adaptation to extreme environments. However, amazing adaptations to extreme stresses do not only occur in microbes, but also in many multicellular organisms. Examples include tardigrades and their capability to survive freezing to near absolute zero, the Pompeii worm withstanding temperatures of up to 105°C, the Crucian carp remaining active in anoxic conditions for several months, and resurrection plants, which can survive near-complete desiccation. Here, we review some of the cryptobiotic strategies and adaptations exhibited in multicellular organisms, and point out their relevance to astrobiology.

Keywords

extremophilemulticellularextreme environmentcryptobiosishibernationanoxiccryobiosisthermobiosisanhydrobiosisadaptation
Type
Research Article
Information
International Journal of Astrobiology , Volume 6 , Issue 3 , July 2007 , pp. 199 - 215
Copyright
Copyright © Cambridge University Press 2007

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References

Airaksinen, M.S. & Panula, P. (1988). J. Comp. Neurol. 273, 163–186.CrossRefGoogle Scholar
Allison, S.D., Chang, B., Randolph, T.W. & Carpenter, J.F. (1999). Arch. Biochem. Biophys. 365, 289–298.CrossRefGoogle Scholar
Alpert, P. (2000). Plant. Ecol. 151, 5–17.CrossRefGoogle Scholar
Alpert, P. (2006). J. Exp. Biol. 209, 1575–1584.CrossRefGoogle Scholar
Andrews, M.T., Squire, T.L., Bowen, C.M. & Rollins, M.B. (1998). Proc. Natl Acad. Sci. USA 95, 8392–8397.CrossRefGoogle Scholar
Auerbach, G., Gaill, F., Jaenicke, R., Schulthess, T., Timpl, R. & Engel, J. (1995). Matrix Biol. 14, 589–592.CrossRefGoogle Scholar
Bale, J.S. (1996). Eur. J. Entomol. 93, 369–382.Google Scholar
Barnes, B.M. (1989). Science 244, 1593–1595.CrossRefGoogle Scholar
Baumann, H. (1922). Zool. Jahrb. 45, 501–556.Google Scholar
Beckman, A.L. & Stanton, T.L. (1982). The Neural Basis of behavior, ed. Beckman, A.L. & Stanton, T.L., pp. 19–45. Spectrum, New Orleans, LA.CrossRefGoogle Scholar
Becquerel, P. (1950). C. R. Acad. Sci. Paris 231, 261–263.Google Scholar
Behm, C.A. (1997). Int. J. Parasitol. 27, 215–229.CrossRefGoogle Scholar
Belke, D.D., Wang, L.C. & Lopaschuk, G.D. (1998). Biochim. Biophys. Acta 1391, 25–36.CrossRefGoogle Scholar
Ben-Zvi, A.P. & Goloubinoff, P. (2001). J. Struct. Biol. 135, 84–93.CrossRefGoogle Scholar
Bernacchia, G., Salamini, F. & Bartels, D. (1996). Plant Physiology 111, 1043–1050.CrossRefGoogle Scholar
Bertolani, R., Guidetti, R., Jonsson, K.I., Altiero, T., Boschiini, D. & Rebecchi, L. (2004). J. Limnol. 63 (Suppl. 1), 16–25.CrossRefGoogle Scholar
Bewley, J.D. (1979). Ann. Rev. Plant Physiology 30, 195–238.CrossRefGoogle Scholar
Bhatt, B. & Rohde, R. (1970). J. Nematol. 2, 277–285.Google Scholar
Block, W. (1990). Phil. Trans. R. Soc. London. B 326, 613–633.Google Scholar
Bottiger, B.W. & Martin, E. (2001). Curr. Opin. Crit. Care 7, 176–183.CrossRefGoogle Scholar
Bowler, K. & Fuller, B.J. (1987). Temperature and Animal Cells. CUP, Cambridge, UK.Google Scholar
Boyer, B.B., Barnes, B.M., Lowell, B.B. & Grujic, D. (1998). Am. J. Physiol. Regul. Integrat. Comp. Physiol. 275, R1232–R1238.CrossRefGoogle Scholar
Boyle, R. (1665). An Account of Freezing: New Experiments and Observations Touching Cold. John Crook, London.Google Scholar
Brisa, N.L., Zbindenb, M. & Gaillb, F. (2005). Deep-Sea Research I 52, 1071–1083.CrossRefGoogle Scholar
Browne, J., Tunnacliffe, A. & Burnell, A. (2002). Nature 416, 38.CrossRefGoogle Scholar
Browne, J.A., Dolan, K.M., Tyson, T., Goyal, K., Tunnacliffe, A. & Burnell, A.M. (2004). Eukaryot. Cell 3, 966–975.CrossRefGoogle Scholar
Browne, R.A. & MacDonald, G.H. (1982). J. Biogeography 9, 331–338.CrossRefGoogle Scholar
Buck, M.J., Squire, T.L. & Andrews, M.T. (2002). Physiol. Genomics 8, 5–13.CrossRefGoogle Scholar
Carlberg, U., Nilsson, A. & Nygaard, O. (1990). Eur. J. Biochem. 191(3), 639–645.CrossRefGoogle Scholar
Chapman, L.J., Kaufman, L.S., Chapman, C.A. & McKengie, F.E. (1995). Conservation Biol. 9, 1274–1288.CrossRefGoogle Scholar
Chen, S., Gollop, N. & Glazer, I. (2005). Parasitology 131, 1–9.CrossRefGoogle Scholar
Chen, T., Amons, R., Clegg, J.S., Warner, A.H. & MacRae, T.H. (2003). Eur. J. Biochem. 270, 137–145.CrossRefGoogle Scholar
Chen, Y., Matsushita, M., Nairn, A.C., Damuni, Z., Cai, D., Frerichs, K.U. & Hallenbeck, J.M. (2001). Biochemistry 40(38), 11 565–11 570.CrossRefGoogle Scholar
Cheng, C.C., Cziko, P.A. & Evans, C.W. (2006). Proc. Natl Acad. Sci. USA 103(27), 10 491–10 496.CrossRefGoogle Scholar
Chevaldonne, P., Desbruye′res, D. & Childress, J.J. (1992). Nature. 359, 593–594.CrossRefGoogle Scholar
Christman, M., Morgan, R., Jacobson, F. & Ames, B. (1985). Cell 41, 753–762.CrossRefGoogle Scholar
Clegg, J.S. (2001). Comp. Biochem. Physiol. 128 (Part B), 613–624.CrossRefGoogle Scholar
Clegg, J.S. & Trotman, C.N.A. (2002). Artemia: Basic and Applied Biology, eds Abatzopoulos, Th. J., Beardmore, J.A., Clegg, J.S. & Sorgeloos, P., pp. 129–170. Kluwer Academic, Dordrecht.CrossRefGoogle Scholar
Coates, C.W. (1937). Bull. N.Y. Zool. Soc. 40, 25–34.Google Scholar
Cocca, E., Ratnayake-Lecamwasam, M., Parker, S.K., Camardella, L., Ciaramella, M., di Prisco, G. & Detrich, H.W. III, (1995). Proc. Natl Acad. Sci. USA 92, 1817–1821.CrossRefGoogle Scholar
Collins, C.H. & Clegg, J.S. (2004). Cell. Biol. Intern. 28, 449–455.CrossRefGoogle Scholar
Convey, P. (2000). Cryo Lett. 21, 73–82.Google Scholar
Cuming, A.C. (1999). Seed Proteins, ed. Shewry, P.R. & Casey, R., pp. 753–780. Kluwer Academic, Dordrecht.CrossRefGoogle Scholar
Dalhoff, E., O'Brien, J., Somero, G.H. & Vetter, R.D. (1991). Physiol. Zool. 64, 1490–1508.CrossRefGoogle Scholar
Danks, H.V. (1978). Can. Ent. 110, 1167–1205.CrossRefGoogle Scholar
Danks, H.V. (1987). Biological Survey of Canada (terrestrial arthropods), p. 513. Canadian Museum of Nature, Ottawa, Canada.Google Scholar
Danks, H.V. (1991). Insects at Low Temperatures, eds Lee, R.E. Jr & Denlinger, D.L., pp. 231–239. Chapman and Hall, London.CrossRefGoogle Scholar
Danks, H.V. (2000). J. Insect Physiol. 46, 837–852.CrossRefGoogle Scholar
Denlinger, D.L. (1985). Comparative Insect Physiology, Biochemistry and Pharmacology, eds Kerkut, G.A. & Gilbert, L., pp. 353–412. Pergamon, Oxford.Google Scholar
Desbruye′res, D., Gaill, F., Laubier, L. & Fouquet, Y. (1985). Bull. Biol. Soc. Wash. 6, 103–116.Google Scholar
Desbruye′res, D.P. et al. (1998). Deep-Sea Res. PII 45, 383–422.Google Scholar
Desbruye′res, D. & Laubier, L. (1980). Oceanol. Acta 3, 267–274.Google Scholar
DeVries, A.L. (1988). Comp. Biochem. Physiol. B 90, 611–621.Google Scholar
di-Prisco, G., Condo, S.G., Tamburrini, M. & Giardina, B. (1991). Trends Biochem. Sci. 16, 471–474.CrossRefGoogle Scholar
Doyère, P.L.N. (1842). Ann. Sci. Nat. (Ser. 2) 18, 5.Google Scholar
Drinkwater, L.E. & Crowe, J.H. (1991). Bio. Bull. 180, 432–439.CrossRefGoogle Scholar
Dumeril, M.A. (1849). Ann. Sci. Nat. Zool. 12, 346.Google Scholar
Dure, L. (2001). Protein Peptide Lett. 8, 115–122.CrossRefGoogle Scholar
Eleutherio, E.C.A., Araujo, P. & Panek, A. (1993). Cryobiology 30, 591–596.CrossRefGoogle Scholar
Ellis, R.J. & Hartl, F.U. (1999). Curr. Opin. Struct. Biol. 9(1), 102–110.CrossRefGoogle Scholar
Ellis, R.J. & Hartl, F.-U. (2003). Nature Encyclopedia of the Human Genome, ed. Cooper, D.N., pp. 806–810. Nature Publishing Group, London.Google Scholar
Epperson, L.E. & Martin, S.L. (2002). Physiol. Genomics 10, 93–102.CrossRefGoogle Scholar
Fahlman, A., Storey, J.M. & Storey, K.B. (2000). Cryobiology 40, 332–342.CrossRefGoogle Scholar
Farrell, A.H., Hohenstein, K.A. & Shain, D.H. (2004). J. Mol. Evol. 59, 666–673.CrossRefGoogle Scholar
Franceschi, T. (1948). Boll. Mus. Ist. Biol. Univ. Geneva 22, 47–49.Google Scholar
Frank, F. (1985). Biophysics and Biochemistry at Low Temperatures. Cambridge University Press, Cambridge.Google Scholar
Freckman, D.W., Whitford, W.G. & Steinberger, Y. (1987). Biol. Fertility Soils 3, 3–10.Google Scholar
Frerichs, K.U., Smith, C.B., Brenner, M., DeGracia, D.J., Krause, G.S., Marrone, L., Dever, T.E. & Hallenbeck, J.M. (1998). Proc. Natl Acad. Sci. USA 95(24), 14 511–14 516.CrossRefGoogle Scholar
Gaff, D.F. (1971). Science 174, 1033–1034.CrossRefGoogle Scholar
Gaff, D.F. (1977). Oecologia 31, 95–104.CrossRefGoogle Scholar
Gaff, D.F. (1987). Oecologia 74, 133–136.CrossRefGoogle Scholar
Gaff, D.F. (1989). Structural and Functional Responses to Environmental Stresses: Water Shortage, eds Kreeb, K.H., Richter, H. & Hinckley, T.M., pp. 255–268. Academic Press, Amsterdam.Google Scholar
Gaff, D.F. & Giess, W. (1986). Dinternia 18, 17–36.Google Scholar
Gaff, D.F. & Wood, J.N. (1988). Proceedings Int. Congress Plant Physiology, pp. 984–988. New Delhi, India.Google Scholar
Gaill, F. (1993). FASEB J. 7, 558–565.CrossRefGoogle Scholar
Gaill, F., Mann, K., Wiedemann, H., Engel, J. & Timpl, R. (1995). J. Mol. Biol. 246, 284–294.CrossRefGoogle Scholar
Gaill, F., Wiedemann, H., Mann, Kuhn K.K., Timpl, R. & Engel, J. (1991). J. Mol. Biol. 221, 157–163.CrossRefGoogle Scholar
Garay-Arroyo, A., Colmenero-Flores, J.M., Garciarrubio, A. & Covarrubias, A.A. (2000). J. Biol. Chem. 275, 5668–5674.CrossRefGoogle Scholar
Garcia-de-Castro, A. & Tunnacliffe, A. (2000). FEBS Lett. 487, 199–202.CrossRefGoogle Scholar
Gavaret, J. (1859). Ann. Sci. Nat. (Ser. 4) 11, 315.Google Scholar
Gaubin, Y., Planel, H., Gasset, G., Pianezzi, B., Delpoux, M., Clegg, J., Kovalev, E.E., Nevzgodina, L.V., Maximova, E.N. & Miller, A.T. (1983). Adv. Space Res. 3, 135–140.CrossRefGoogle Scholar
Geiser, F. & Ruf, T. (1995). Physiol. Zool. 68, 935–966.CrossRefGoogle Scholar
Goyal, K., Browne, J.A., Burnell, A.M. & Tunnacliffe, A. (2005a). Biochimie 87, 565–574.CrossRefGoogle Scholar
Goyal, K., Walton, L.J., Browne, J.A., Burnell, A.M. & Tunnacliffe, A. (2005b). Integr. Comp. Biol. 45, 702–709.CrossRefGoogle Scholar
Goyal, K., Walton, L.J. & Tunnacliffe, A. (2005c). Biochem. J. 388, 151–157.CrossRefGoogle Scholar
Greenwood, P.H. (1986). J. Morphol. (Suppl. 1), 163–179.CrossRefGoogle Scholar
Guo, N., Puhlev, I., Brown, D.R., Mansbridge, J. & Levine, F. (2000). Nat. Biotech. 18, 168–171.CrossRefGoogle Scholar
Haddad, A., Camacho, F., Durand, P. & Cary, C. (1995). Appl. Environ. Microbiol. 61(5), 1679–1687.CrossRefGoogle Scholar
Hairston, N.G., Robert, A., Brunt, V., Kearns, C.M. & Engstrom, D.R. (1995). Ecology 76, 1706–1711.CrossRefGoogle Scholar
Hand, S.C. (1991). Adv. Comp. Environ. Physiol. 8, 1–50.Google Scholar
Hand, S.C. (1998). J. Exp. Biol. 201, 1233–1242.CrossRefGoogle Scholar
Hand, S.C. & Podrabsky, J.E. (2000). Thermochim. Acta 349, 31–42.CrossRefGoogle Scholar
Hartung, W., Schiller, P. & Karl-Josef, D. (1998). Progress Botany 59, 299–327.CrossRefGoogle Scholar
Haslbeck, M., Walke, S., Stromer, T., Ehrnsperger, M., White, H.E., Chen, S., Saibil, H.R. & Buchner, J. (1999). EMBO J. 18, 6744–6751.CrossRefGoogle Scholar
Hennequin, C., Collignon, A. & Karjalainen, T. (2001). Microbial Pathogenesis 31, 255–260.CrossRefGoogle Scholar
Higa, L.M. & Womersley, C.Z. (1993a). J. Exp. Zool. 267, 120–129.CrossRefGoogle Scholar
Higa, L.M. & Womersley, C.Z. (1993b). J. Exp. Zool. 267, 120–129.CrossRefGoogle Scholar
Hinton, H.E. (1960). J. Insect Physiol. 5, 286–300.CrossRefGoogle Scholar
Hittel, D. & Storey, K.B. (2001). Biochim. Biophys. Acta 1522, 238–243.CrossRefGoogle Scholar
Hochachka, P.W. & Somero, G.N. (1984). Biochemical Adaptation. Princeton University Press, Princeton, NJ.CrossRefGoogle Scholar
Hochachka, P.W. & Somero, G.N. (2002). Biochemical Adaptation. Oxford University Press, Oxford.CrossRefGoogle Scholar
Holopainen, I.J. & Hyvarinen, H. (1985). Verh. Int. Verein. Limnol. 22, 2566–2570.Google Scholar
Horwath, K.L. & Duman, J.G. (1983). J. Comp. Physiol. 151, 225–232.CrossRefGoogle Scholar
Horwath, K.L. & Duman, J.G. (1984). Physiol. Zool. 57, 40–45.CrossRefGoogle Scholar
Hovland, R., Eikhom, T.S. & Proud, C.G. (1999). FEBS Lett. 444(1), 97–101.CrossRefGoogle Scholar
Hylland, P. & Nilsson, G.E. (1999). Brain Research 823, R49–58.CrossRefGoogle Scholar
Imai, R.L., Chang, A., Ohta, E., Bray, A. & Takagi, M. (1996). Gene 170, 243–248.CrossRefGoogle ScholarPubMed
Inagaki, N., Yamatodani, A., Ando-Yamamoto, M., Tohyama, M., Watanabe, T. & Wada, H. (1988). J. Comp. Neurol. 273, 283–300.CrossRefGoogle Scholar
Ingram, J. & Bartels, D. (1996). Ann. Rev. Plant Physiol. Plant Mol. Biol. 47, 377–403.CrossRefGoogle Scholar
Jackson, D.C., Crocker, C.E. & Ultsch, G.R. (2000). Am. J. Physiol. Regul. Integrat. Comp. Physiol. 278, R1564–1571.CrossRefGoogle Scholar
Jackson, S.A. & Clegg, J.S. (1996a). Develop. Growth Diff. 38, 153–160.CrossRefGoogle Scholar
Jönsson, K.I. (2003). Physiol. Biochem. Zool. 76(4), 429–435.CrossRefGoogle Scholar
Kamekura, M., Seno, Y., Holmes, M.L. & Dyall-Smith, M.L. (1992). J. Bacteriol. 174, 736–742.CrossRefGoogle Scholar
Kaule, G., Timpl, R., Gaill, F. & Gunzler, V. (1998). Matrix Biol. 17, 205–212.CrossRefGoogle Scholar
Keilin, D. (1959). Proc. R. Soc. B 150, 149–191.Google Scholar
Kelley, D., Baross, J. & Delaney, J. (2002). Ann. Rev. Earth Planet. Sci. 30, 385–491.CrossRefGoogle Scholar
Knutson, R.M. (1974). Science 186, 746–747.CrossRefGoogle Scholar
Koag, M.-C., Fenton, R.D., Wilkens, S. & Close, T.J. (2003). Plant Physiol. 131, 309–316.CrossRefGoogle Scholar
Kojima, M., Shiba, T., Kondo, N. & Takamatsu, N. (2001). Eur. J. Biochem. 268, 5997–6002.CrossRefGoogle Scholar
Kojima, M., Takamatsu, N., Ishii, T., Kondo, N. & Shiba, T. (2000). Eur. J. Biochem. 267, 4635–4641.CrossRefGoogle Scholar
Kortner, G. & Geiser, F. (2000). Chronobiol. Int. 17, 103–128.CrossRefGoogle Scholar
Krembs, C., Deming, J., Junge, K. & Eicken, H. (2002). Deep-Sea Res. 49, 2163–2181.CrossRefGoogle Scholar
Kukal, O., Serianni, A.S. & Duman, J.G. (1988). J. Com. Physiol. B. 158, 175–183.CrossRefGoogle Scholar
Lee, R.E. Jr (1989). BioScience 39, 308–311.CrossRefGoogle Scholar
Lee, R.E. & Denlinger, D.L. (1991). Insects at Low Temperature. Chapman and Hall, London.CrossRefGoogle Scholar
Lee, T., Jordan, M.L. & Wang, L.C.H. (1996). Adaptations to the Cold, ed. Geiser, F., Hurlbert, A.J. & Nicol, S.C., pp. 197–201. University of New England Press, Armidale, Lebanon, NH.Google Scholar
Lees, A.D. (1955). Physiology of Diapause in Arthropods. Cambridge University Press, Cambridge.Google Scholar
Liang, P. & MacRae, T.H. (1999). Develop. Biol. 207, 445–456.CrossRefGoogle Scholar
Lutz, P.L. & Storey, K.B. (1997). Comparative physiology. In Handbook of Physiology, Section 13, ed. Danzler, W., pp. 1479–1522. Oxford University Press, Oxford.Google Scholar
Ma, X. et al. (2005). Cryobiology 51, 15–28.CrossRefGoogle Scholar
MacDonald, J.A. & Storey, K.B. (1999). Biochem. Biophys. Res. Commun. 254, 424–429.CrossRefGoogle Scholar
MacRae, T.H. (2000). Cell. Mol. Life Sci. 57, 899–913.CrossRefGoogle Scholar
Madin, K.A. & Crowe, J.H. (1975). J. Exp. Zool. 193, 335–342.CrossRefGoogle Scholar
Marcus, N.H. (1996). Hydrobiologia 320, 141–152.CrossRefGoogle Scholar
Marcus, N.H., Lutz, R., Burnett, W. & Cable, P. (1994). Limnol. Oceanograph. 39, 154–158.CrossRefGoogle Scholar
Mcnamara, J.M. (1994). J. Theoret. Biol. 168, 201–209.CrossRefGoogle Scholar
Moon, I., Fujikawa, S. & Shimada, K. (1996). Cryo Lett. 17, 105–110.Google Scholar
Nairn, A.C. & Palfrey, H.C. (1987). J. Biol. Chem. 262(36), 17 299–17 303.CrossRefGoogle Scholar
Ndima, T., Farrant, J., Thomson, J. & Mundree, S. (2001). Plant Growth Regulation 35, 137–145.CrossRefGoogle Scholar
Needham, J.T. (1743). Phil. Trans. 42, 634.Google Scholar
Nilsson, G.E. (2001). News Physiol. Sci. 16, 218–221.Google Scholar
Nilsson, G.E. & Lutz, P.L. (2004). J. Cerebral Blood Flow Metabolism 24, 475–486.CrossRefGoogle Scholar
O'Hara, B.F., Watson, F.L., Srere, H.K., Kumar, H., Wiler, S.W., Welch, S.K., Bitting, L., Heller, H.C. & Kilduff, T.S. (1999). J. Neurosci. 19, 3781–3790.CrossRefGoogle Scholar
Olsen, T.M. & Duman, J.G. (1997). J. Comp. Physiol. B 167, 105–113.CrossRefGoogle Scholar
Ono, M., Hosoe, Y., Azuma, S., Shoji, M., Nara, K., Kondo, N., Shiba, T. & Takamatsu, N. (2001). Gene 277, 121–127.CrossRefGoogle ScholarPubMed
Ono, M., Kojima-Kawagoe, M., Kondo, N., Shiba, T. & Takamatsu, N. (2003). Gene 302, 193–199.CrossRefGoogle ScholarPubMed
Pannewitz, S., Schlensog, M. & Green, T.G.A. (2003). Ecophysiology 135, 30–38.Google Scholar
Panula, P., Pirvola, U., Auvinen, S. & Airaksinen, M.S. (1989). Neuroscience 28, 585–610.CrossRefGoogle Scholar
Perry, R.N. (1998). Survival of Entomopathogenic Nematodes, ed. Glazer, I., Richardson, P., Boemare, N., Coudert, F. & Reiman, B.E., pp. 7–13. European Commission Press, Brussels, Belgium.Google Scholar
Pigòn, A. & Węglarska, B. (1953). Bull. Acad. Pol. Sci. 1, 69–72.Google Scholar
Pohlschröder, M., Prinz, W.A., Hartmann, E. & Beckwith, J. (1997). Cell 91, 563–566.CrossRefGoogle Scholar
Postnikova, G.B., Tselikova, S.V., Kolaeva, S.G. & Solomonov, N.G. (1999). Comp. Biochem. Physiol. A 124, 35–37.CrossRefGoogle Scholar
Prockop, D.J. & Kivirikko, K.I. (1995). Ann. Rev. Biochem. 64, 403–434.CrossRefGoogle Scholar
Proud, C.G. (1992). Current Topics Cellular Regulation 32, 243–369.CrossRefGoogle Scholar
Rahm, P.G. (1921). Zeitschr. Allg. Physiol. 20, 1–34.Google Scholar
Reamur, R.A.F. (1736). Paris: Imprimerie Royale 2, 141–147.Google Scholar
Redpath, N.T., Foulstone, E.J. & Proud, C.G. (1996). EMBO J. 15(9), 2291–2297.CrossRefGoogle Scholar
Redpath, N.T. & Proud, C.G. (1989). Biochem. J. 262(1), 69–75.CrossRefGoogle Scholar
Reiswig, H.M. & Miller, T.L. (1998). Invert. Biol. 117, 1–8.CrossRefGoogle Scholar
Ricci., C. (1998). Hydrobiologia 387/388, 321–326.CrossRefGoogle Scholar
Rothschild, L.J. (2006). Planetary Systems and the Origins of Life, ed. Pudritz, R.E., Higgs, P. & Stone, J.Cambridge University Press, Cambridge.Google Scholar
Rothschild, L.J. & Mancinelli, R.L. (2001). Nature 409, 1092–1101.CrossRefGoogle Scholar
Ruud, J.T. (1954). Nature 173, 848–850.CrossRefGoogle Scholar
Ryazanov, A.G. & Shestakova, E.A. (1988). Nature 334, 170–173.CrossRefGoogle Scholar
Saitongdee, P., Milner, P., Becker, D.L., Knigh, C.E. & Burnstock, G. (2000). Cardiovasc. Res. 47, 108–115.CrossRefGoogle Scholar
Sales, K., Brandt, W., Rumbak, E. & Lindsey, G. (2000). Biochim. Biophys. Acta. 1463, 267–278.CrossRefGoogle Scholar
Sandell, M. (1990). Q. Rev. Biol. 65, 23–42.CrossRefGoogle Scholar
Scandurra, R., Consalvi, V., Chiaraluce, R., Politi, L. & Engel, P.C. (2000). Front. Biosci. 5, D787–D795.CrossRefGoogle Scholar
Schmidt-Nielsen, K., Taylor, C.R. & Shkolnik, A. (1971). J. Exp. Biol. 55, 385–398.CrossRefGoogle Scholar
Schmidt-Rhaesa, A. (2001). Zoologischer Anzeiger 240(3–4), 549–555.CrossRefGoogle Scholar
Schneider, H., Wistuba, N., Wagner, H.-J., Thurmer, F. & Zimmermann, U. (2000). New Phytol. 148, 221–238.CrossRefGoogle Scholar
Schulze-Makuch, D. & Irwin, L.N. (2004). Life in the Universe: Expectations and Constraints, p. 172. Springer, Berlin.Google Scholar
Schwartz, J.-C., Arrang, J.-M., Garbarg, M., Pollard, H. & Ruat, M. (1991). Physiol. Rev. 71, 1–51.CrossRefGoogle Scholar
Scott, P. (2000). Annals Botany 85, 159–166.CrossRefGoogle Scholar
Seki, K. & Toyoshima, M. (1998). Nature 395, 853–854.CrossRefGoogle Scholar
Shen-Miller, J., Mudgett, M.B., Schopf, J.W., Clarke, S. & Berger, R. (1995). Am. J. Botany 82, 1367–1380.CrossRefGoogle Scholar
Sherwin, H.W. & Farrant, J.M. (1996). Annals Botany 78, 703–710.CrossRefGoogle Scholar
Shimada, K. (1995). Proc. NIPR Symp. Polar Biol. 8, 200.Google Scholar
Shivatcheva, T.M. (1989). Living in the Cold, ed. Malan, A. & Canguilhem, B., pp. 87–95. John Libbey Eurotext Ltd., Paris.Google Scholar
Sick, T.J., Rosenthal, M., LaManna, J.C. & Lutz, P.L. (1982). Am. J. Physiol. Regul. Integrat. Comp. Physiol. 243, R281–R288.CrossRefGoogle Scholar
Sicot, F.-X., Mesnage, M., Masselot, M., Exposito, J.-Y., Garrone, R., Deutsch, J. & Gaill, F. (2000). J. Mol. Biol. 302, 811–820.CrossRefGoogle Scholar
Sicot, F.X., Exposito, J.Y., Masselot, M., Garrone, R., Deutsch, J. & Gaill, F. (1997). Eur. J. Biochem. 590, 1–9.Google Scholar
Sidell, B.D., Vayda, M.E., Small, D.J., Moylan, T.J., Londraville, R.L., Yuan, M.-L., Rodnick, K.J., Eppley, Z.A. & Costello, L. (1997). Proc. Natl Acad. Sci. USA 94, 3420–3424.CrossRefGoogle Scholar
Sinclair, B.J. & Sjursen, H. (2001). Antarctic Sci. 13(3), 271–279.CrossRefGoogle Scholar
Sivamani, E. et al. (2000). Plant Sci. 155, 1–9.CrossRefGoogle Scholar
Snell, T.W. (2005). Small-scale Freshwater Environment Toxicity Test Methods, eds Blaise, C. & Ferard, J.F.Kluwer, Dordrecht.Google Scholar
Somero, G.N. & DeVries, A.L. (1967). Science 156, 257–258.CrossRefGoogle Scholar
Somero, G.N. & Yancey, P.H. (1997). Handbook of Physiology, pp. 441–484. Oxford University Press, Oxford.Google Scholar
Sømme, L. (1999). Eur. J. Entomol. 96, 1–10.Google Scholar
Song, X., Kortner, G. & Geiser, F. (1997). Am. J. Physiol. Regul. Integr. Comp. Physiol. 273, R2097–R2104.CrossRefGoogle Scholar
Soukri, A., Valverde, F., Hafid, N., Elkebbaj, M.S. & Serrano, A. (1996). Gene 181, 139–145.CrossRefGoogle ScholarPubMed
Spallanzani, L. (1776). Societa Tipografica. (Modena) 2, 203–285.Google Scholar
Steiner, G. & Albin, F.E. (1946). J. Wash. Acad. Sci. 36, 97–99.Google Scholar
Stocco, D.M., Beers, P.C. & Warner, A.H. (1972). Develop. Biol. 27, 479–489.CrossRefGoogle Scholar
Storey, K.B., Baust, J.G. & Beuscher, P. (1981). Cryobiology 18(3), 315–321.CrossRefGoogle Scholar
Sturla, M., Masini, M.A., Prato, P., Grattarola, C. & Uva, B. (2001). Cell Tissue Res. 303, 351–358.CrossRefGoogle Scholar
Takamatsu, N. et al. (1997). Gene 204, 127–132.CrossRefGoogle Scholar
Takamatsu, N., Ohba, K., Kondo, J., Kondo, N. & Shiba, T. (1993). Mol. Cell. Biol. 13, 1516–1521.Google Scholar
Tauber, M.J.C.A. & Masaki, S. (1968). Seasonal anhydrobiosis in invertebrates. In Adaptations of Insects, p. 411. Oxford University Press, Oxford.Google Scholar
Townshend, J.L. (1984). J. Nematology 16, 282–289.Google Scholar
Treece, G.D. (2000). Southern Regional Aquaculture Center (Texas A & M University), Pub. No. 702, pp. 1–8.Google Scholar
Treonis, A.M., Wall, D.H. & Virginia, R.A. (2000). Functional Ecol. 14, 460–467.CrossRefGoogle Scholar
Tunnacliffe, A. & Lapinski, J. (2003). Phil. Trans. R. Soc. London B 358, 1755–1771.CrossRefGoogle Scholar
Turner, L.M. (1886). Second Arctic Serial Publication, Signal Services U.S. Army, p. 226.Google Scholar
Ultsch, G.R. (1989). Bio. Rev. 64, 435–516.CrossRefGoogle Scholar
Ultsch, G.R. & Jackson, D.C. (1982). J. Exp. Biol. 96, 11–28.CrossRefGoogle Scholar
van Breukelen, F., Maier, R. & Hand, S.C. (2000). J. Exp. Biol. 203, 1123–1130.CrossRefGoogle Scholar
vander-Rest, M. & Bruckner, P. (1993). Curr. Opin. Struct. Biol. 3, 430–436.CrossRefGoogle Scholar
vander-Rest, M. & Garrone, R. (1991). FASEB J. 5, 2814–2823.CrossRefGoogle Scholar
Viner, R.I. & Clegg, J.S. (2001). Cell Stress Chaperones 6(2), 126–135.2.0.CO;2>CrossRefGoogle Scholar
Vornanen, M. & Paajanen, V. (2006). Am. J. Physiol. Regul. Integrat. Comp. Physiol. June 1, R1482–R1489.Google Scholar
Wada, H., Inagaki, N., Yamatodani, A. & Watanabe, T. (1991). Trends Neurosci. 14, 415–418.CrossRefGoogle Scholar
Wang, L.C.H. (1978). Strategies in the Cold: Natural Torpidity and Thermogenesis, eds Wang, L.C.H. & Hudson, J.W., pp. 105–145. Academic Press, New York.Google Scholar
Wang, L.C.H. (1982). Hibernation and Torpor in Mammals and Birds, eds Lyman, C.P., Willis, J.S., Malan, A. & Wang, L.C.H., pp. 206–236. Academic Press, New York.Google Scholar
Wang, L.C.H. (ed.) (1989). Animal Adaptation to Cold, pp. 361–401. Springer, Heidelberg.CrossRefGoogle Scholar
Warner, A.H. & Clegg, J.S. (2001). Eur. J. Biochem. 268, 1568–1576.CrossRefGoogle Scholar
Warner, A.H. (1992). Ap4A and other Dinucleoside Polyphosphates, ed. McLennan, A.G., pp. 276–393. CRC Press, Boca Raton, FL.Google Scholar
Warner, A.H., Brunet, R.T, MacRae, T.H. & Clegg, J.S. (2004). Arch. Biochem. Biophys. 424, 189–200.CrossRefGoogle Scholar
Warner, A.H., Jackson, S.A. & Clegg, J.S. (1997). J. Exp. Biol. 200, 897–908.CrossRefGoogle Scholar
Weinstein, R.B. & Somero, G.N. (1998). J. Comp. Physiol. B: Biochem. Systemic Environ. Physiol. 168(3), 190–196.CrossRefGoogle Scholar
Wehner, R., Marsh, A.C. & Wehner, S. (1992). Desert ants on a thermal tightrope. Nature 357, 586–587.CrossRefGoogle Scholar
Westh, P. & Ramlùv, H. (1991). J. Exp. Zool. 258, 303–311.CrossRefGoogle Scholar
Wharton, D.A. (2002). Life at the Limits—Organisms in Extreme Environments, p. 300. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Wharton, D.A. & Brown, I.M. (1991). J. Exp. Biol. 155, 629–641.CrossRefGoogle Scholar
Willsie, J.K. & Clegg, J.S. (2002). J. Cell. Biochem. 84, 601–614.CrossRefGoogle Scholar
Wise, M.J. & Tunnacliffe, A. (2004). Trends Plant Sci. 9, 13–17.CrossRefGoogle Scholar
Wolkers, W.F., Tablin, F. & Crowe, J.H. (2002). Comp. Biochem. Physiol. A 131, 535–543.CrossRefGoogle Scholar
Wolkers, W.F., Walkers, N.J., Tablin, F. & Crowe, J.H. (2001). Cryobiology 42, 79–87.CrossRefGoogle Scholar
Womersley, C.Z., Wharton, D.A. & Higa, L.M. (1998). The Physiology and Biochemistry of Free-living and Plant-parasitic Nematodes, eds Perry, R.N. & Wright, D.J., pp. 271–302. CABI Publishing, Wallingford.Google Scholar
Wright, J.C. (1989). Tissue Cell 21, 263–279.CrossRefGoogle Scholar
Wright, J.C. (2001). Zool. Anz. 240, 563–582.CrossRefGoogle Scholar
Wright, J.C., Westh, P. & Ramløv, H. (1992). Biol. Rev. 67, 1–29.CrossRefGoogle Scholar
Xu, D., Duan, X., Wang, B., Hong, B., Ho, T. & Wu, R. (1996). Plant Physiol. 110, 249–257.CrossRefGoogle Scholar
Yamashita, O. & Hasegawa, K. (1985). Comprehensive Insect Physiology, Biochemistry and Pharmacology, eds Kerkut, G.A. & Gilbert, L.I., pp. 407–434. Pergamon Press, Oxford.Google Scholar
Yancey, P.H., Clark, M.E., Hand, S.C., Bowlus, R.D. & Somero, G. (1982). Science 217, 1214–1222.CrossRefGoogle Scholar
Zettler, L., Gomez, F., Zettler, E., Keenan, B., Amils, R. & Sogin, M. (2002). Nature 417, 137.CrossRefGoogle Scholar
Zhang, L., Ohta, A., Takagi, M. & Imai, R. (2000). J. Biochem. 127, 611–616.CrossRefGoogle Scholar