Advertisement

Membrane Integrity in Anhydrobiotic Organisms: Toward a Mechanism for Stabilizing Dry Cells

  • J. H. Crowe
  • L. M. Crowe

Abstract

Water is normally thought to be required for maintenance of structure and function in biomolecules (reviewed in Tanford 1980; J.H. Crowe et al. 1987a; L.M. Crowe and J.H. Crowe 1988b). Nevertheless, numerous organisms are capable of surviving essentially complete dehydration, including some that are familiar in daily life, such as seeds of many plants, yeast cells, fungal spores, and the like (see Leopold 1986 for references), but also including some microscopic animals, such as certain nematodes, rotifers, tardigrades, and cysts of some crustacean embryos (for example, those of the brine shrimp, Artemia). The dry organisms may remain in this unique living state, which is known as “anhydrobiosis”, for decades or perhaps even centuries under favorable conditions. When water again becomes available they may rapidly swell and resume active life.

Keywords

Desiccation Tolerance Liquid Crystalline Phase Trehalose Content Trehalose Synthesis Lipid Phase Transition 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anchordoguy TJ, Rudolph AS, Carpenter JF, Crowe JH (1987) Modes of interaction of cryoprotectants with membrane phospholipids during freezing. Cryobiology 24: 324–331PubMedCrossRefGoogle Scholar
  2. Arakawa T, Carpenter JF, Kita YA, Crowe JH (1990) The basis for toxicity of certain cryoprotectants: an hypothesis. Cryobiology 27: 401–415CrossRefGoogle Scholar
  3. Araujo PS, Panek AC, Crowe JH, Crowe LM, Panek AD (1991) Trehalose transporting membrane vesicles prepared from yeasts. Biochem Int (in press)Google Scholar
  4. Attfield PV (1987) Trehalose accumulates in Saccharomyces cerevisiae during exposure to agents that induce heat shock response. FEBS Lett 225: 259–263PubMedCrossRefGoogle Scholar
  5. Beker MJ, Blumbergs JE, Ventina EJ, Rapoport AI (1984) Characteristics of cellular membranes at rehydration of dehydrated yeast Saccharomyces cerevisiae. Eur J Appl Microhiol Biotechnol 19: 347–352Google Scholar
  6. Bhandal IS, Hauptmann RM, Widholm JM (1985) Trehalose as cryoprotectant for the freeze preservation of carrot and tobacco cells. Plant Physiol 78: 430–432PubMedCrossRefGoogle Scholar
  7. Borelli MI, Semino MC, Hernandez RE (1987) Cryopreservation of islets of Langerhans: the use of trehalose as a cryoprotective agent. Med Sci Res 15: 299–300Google Scholar
  8. Brana AF, Mendez C, Diaz LA, Manzanal MB, Hardisson C (1986) Glycogen and trehalose accumulation during colony development in Streptomyces antibioticus. J Gen Microhiol 132: 1319–1326Google Scholar
  9. Caffrey M, Fonseca V, Leopold AC (1988) Sugar-lipid interactions. Relevance to anhydrous biology. Plant Physiol 86: 754–758PubMedCrossRefGoogle Scholar
  10. Carpenter JF, Crowe JH (1988a) Modes of stabilization of a protein by organic solutes during desiccation. Cryobiology 25: 459–470CrossRefGoogle Scholar
  11. Carpenter JF, Crowe JH (1988b) The mechanisms of cryoprotection of proteins by solutes. Cryobiology 25: 244–255PubMedCrossRefGoogle Scholar
  12. Carpenter JF, Crowe JH (1989) An infrared spectroscopic study of the interactions of carbohydrates with dried proteins. Biochemistry 28: 3916–3922PubMedCrossRefGoogle Scholar
  13. Carpenter JF, Crowe LM, Crowe JH (1987a) Stabilization of phosphofructokinase with sugars during freeze-drying: characterization of enhanced protection in the presence of divalent cations. Biochim Biophys Acta 923: 109–115PubMedCrossRefGoogle Scholar
  14. Carpenter JF, Martin B, Crowe LM, Crowe JH (1987b) Stabilization of phosphofructokinase during air-drying with sugars and sugar/transition metal mixtures. Cryobiology 24: 455–464PubMedCrossRefGoogle Scholar
  15. Chandrasekhar I, Gaber BP (1988) Stabilization of the bio-membrane by small molecules: interaction of trehalose with the phospholipid bilayer. J Biomol Str Dyn 5: 1163–1171Google Scholar
  16. Charlab R, Oliveira DE, Panek AD (1985) Investigation of the relationship between sstl and fdp mutations in yeast and their effect on trehalose synthesis. Braz J Med Biol Res 18: 447–454PubMedGoogle Scholar
  17. Clegg JS (1986) The physical properties and metabolic status of Artemia cysts at low water contents: the “water replacement” hypothesis. In: Leopold AC (ed) Membranes, Metabolism, and Dry Organisms. Cornell Univ Press, Ithaca, NY, pp 169–187Google Scholar
  18. Coutinho C, Bernardes E, Felix D, Panek AD (1988) Trehalose as cryoprotectant for preservation of yeast strains. J Biotechnol 7: 23–32CrossRefGoogle Scholar
  19. Crowe JH, Crowe LM (1986) Stabilization of membranes in anhydrobiotic organisms. In: Leopold AC (ed) Membranes, Metabolism, and Dry Organisms. Cornell Univ Press, Ithaca, NY, pp 188–209Google Scholar
  20. Crowe JH, Crowe LM (1988) Factors affecting the stability of dry liposomes. Biochim Biophys Acta 939: 327–334PubMedCrossRefGoogle Scholar
  21. Crowe JH, Crowe LM, Jackson SA (1983) Preservation of structural and functional activity in lyophilized sarcoplasmic reticulum. Arch Biochem Biophys 220: 447–484CrossRefGoogle Scholar
  22. Crowe JH, Crowe LM, Chapman D (1984) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223: 701–703PubMedCrossRefGoogle Scholar
  23. Crowe JH, Crowe LM, Carpenter JF, Aurell Wistrom C (1987a) Stabilization of dry phospholipid bilayers and proteins by sugars. Biochem J 242: 1–10PubMedGoogle Scholar
  24. Crowe JH, Spargo BJ, Crowe LM (1987b) Preservation of dry liposomes does not require retention of residual water. Proc Natl Acad Sci USA 84: 1537–1540PubMedCrossRefGoogle Scholar
  25. Crowe JH, Crowe LM, Carpenter JF, Rudolph AS, Aurell Wistrom C, Spargo BJ, Anchordoguy TJ (1988) Interactions of sugars with membranes. Biochim Biophys Acta 947: 367–384PubMedGoogle Scholar
  26. Crowe JH, Crowe LM, Hoekstra FA (1989a) Phase transitions and permeability changes in dry membranes during rehydration. J Bioenerg Biomembr 21: 77–91PubMedCrossRefGoogle Scholar
  27. Crowe JH, Hoekstra FA, Crowe LM (1989b) Membrane phase transitions are responsible for imbibitional damage in dry pollen. Proc Natl Acad Sci USA 86: 520–523PubMedCrossRefGoogle Scholar
  28. Crowe JH, Hoekstra FA, Crowe LM, Anchordoguy TJ, Drobnis E (1989e) Lipid phase transitions measured in intact cells with Fourier transform infrared spectroscopy. Cryobiology 26: 76–84PubMedCrossRefGoogle Scholar
  29. Crowe JH, Carpenter JF, Crowe LM, Anchordoguy TJ (1990) Are freezing and dehydration similar stress vectors? A comparison of modes of interaction stabilizing solutes with biomolecules. Cryobiology 27: 219–231CrossRefGoogle Scholar
  30. Crowe JH, Panek AD, Crowe LM, Panek AC, Araujo PS (1991) Trehalose transport in yeast cell. Biochem Int (in press)Google Scholar
  31. Crowe LM, Crowe JH (1988a) Lyotropic effects of water on phospholipids. In: Aloia RC (ed) Physiological Regulation of Membrane Fluidity. Alan R Liss Inc, New York, pp 75–99Google Scholar
  32. Crowe LM, Crowe JH (1988b) Trehalose and dry dipalmitoylphosphatidylcholine revisited. Biochim Biophys Acta 946: 193–201PubMedCrossRefGoogle Scholar
  33. Crowe LM, Crowe JH, Rudolph A, Womersley C, Appel L (1985) Preservation of freeze-dried liposomes by trehalose. Arch Biochem Biophys 242: 240–247PubMedCrossRefGoogle Scholar
  34. Crowe LM, Womersley C, Crowe JH, Reid D, Appel L, Rudolph A (1986) Prevention of fusion and leakage in freeze-dried liposomes by carbohydrates. Biochim Biophys Acta 861: 131–140Google Scholar
  35. de Oliveria DE, Arrese M, Kidane G, Panek AD, Matoon JR (1986) Trehalose and maltose metabolism in yeast transformed by a MAL4 regulatory gene cloned from a constitutive donor strain. Curr Genet 11: 97–106CrossRefGoogle Scholar
  36. Donnini C, Puglisi PP, Vecli A, Marmiroli N (1988) Germination of Saccharomyces cerevisiae ascospores without trehalose mobilization as revealed by in vivo. C-13 nuclear magnetic resonance spectroscopy. J Bacterio 1170:3789–3791Google Scholar
  37. Gadd GM, Chalmers K, Reed RH (1987) The role of trehalose in dehydration resistance of Saccharomyces cerevisiae. FEMS Microbiol Lett 48: 249–254CrossRefGoogle Scholar
  38. Greiner JV, Medcalf SK, Meneses P, Glonek T (1989) Trehalose maintenance of the metabolic health of the crystalline lens during severe temperature stress. Invest Opthalmol Visual Sci 27 (Suppl): 278–278Google Scholar
  39. Harding TS (1923) The sources of the rare sugars. IX-History of trehalose, its discovery and methods of preparation. Sugar 25: 476–478Google Scholar
  40. Hino A, Mihara K, Nakashima K, Takano H (1990) Trehalose levels and survival ratio of freeze-tolerant versus freeze-sensitive yeasts. Appl Environ Microbiol 56: 1386–1391PubMedGoogle Scholar
  41. Hoekstra FA, van Roekel T (1988) Desiccation tolerance of Papaver dubium during its development in the anther. Possible role of phospholipid composition and sucrose content. Plant Physiol 88: 626–632PubMedCrossRefGoogle Scholar
  42. Hoekstra FA, Crowe LM, Crowe JH (1989) Differential desiccation sensitivity of corn and Pennisetum pollen linked to their sucrose contents. Plant Cell Environ 23: 83–91CrossRefGoogle Scholar
  43. Honadel TE, Killian GJ (1988) Cryopreservation of murine embryos with trehalose and glycerol. Cryobiology 25: 331–337PubMedCrossRefGoogle Scholar
  44. Hottiger T, Boller T, Wiemken A (1987) Rapid changes of heat and desiccation tolerance correlated with changes of trehalose content in Saccharomyces cerevisiae cells subjected to temperature shifts. FEBS Lett 220: 113–115PubMedCrossRefGoogle Scholar
  45. Hottiger T, Boller T, Wiemken A (1989) Correlation of trehalose content and heat resistance in yeast mutants altered in the RAS/adenylate cyclase pathway: is trehalose a thermoprotectant’? FEBS Lett 255: 431–434PubMedCrossRefGoogle Scholar
  46. Katohda S, Ito M, Sadaki K, Takahashi M (1987) Carbohydrate composition during germination and outgrowth of ascospores of Saccharomyces cerevisiae. Agric Biol Chem 51: 2975–2981CrossRefGoogle Scholar
  47. Katohda S, Ito H, Takahashi H, Kikuchi H (1988) Carbohydrate metabolism during sporulation in spheroplasts of yeasts, Saccharomyces cerevisiae. Agric Biol Chem 52: 349–355CrossRefGoogle Scholar
  48. Koster KL, Leopold AC (1988) Sugars and desiccation tolerance in seeds. Plant Physiol 88:829–832 Kotyk A, Michaljanicova D (1979) Uptake of trehalose by Saccharomyces cerevisiae. J Gen Microbiol 110: 323–332Google Scholar
  49. Kotyk A, Michaljanicova D, Struzinsky R, Baryshnikova LM, Sychrova H (1985) Absence of glucose-stimulated transport in yeast protoplasts. Folia Microbiol 30: 110–116CrossRefGoogle Scholar
  50. Krag KT, Koehler I-M, Wright RW (1985) Trehalose — a nonpermeable cryoprotectant for direct freezing of early stage murine embryos. Cryobiology 22: 636–636CrossRefGoogle Scholar
  51. Lee CWB, Waugh JS, Griffin RG (1986) Solid-state NMR study of trehalose/1,2-dipalmitoyl-snphosphatidylcholine interactions. Biochemistry 25: 3737–3742PubMedCrossRefGoogle Scholar
  52. Lee CWB, Das Gupta SK, Mattai J, Shipley GG, Abdel-Mageed OH, Makriyannis A, Griffin RG (1989) Characterization of the Llambda phase in trehalose-stabilized dry membranes by solid-state NMR and X-ray diffraction. Biochemistry 28: 5000–5009PubMedCrossRefGoogle Scholar
  53. Leopold AC (1986) (ed) Membranes, Metabolism, and Dry Organisms. Cornell Univ Press, Ithaca, NY, 374 ppGoogle Scholar
  54. Leprince O, Bronchart R, Deltour R (1990) Changes in starch and soluble sugars in relation to the acquisition of desiccation tolerance during maturation of Brassica campestris seed. Plant Cell Environ 13: 539–546CrossRefGoogle Scholar
  55. Mackenzie KF, Singh KK, Brown AD (1988) Water stress plating hypersensitivity of yeasts: protective role of trehalose in Saccharomyces cerevisiae. J Gen Microbiol 134: 1661–1666PubMedGoogle Scholar
  56. Madden TD, Bailey MB, Hope MJ, Cullis PR, Schieren HP, Janoff AS (1985) Protection of large unilamellar vesicles by trehalose during dehydration: retention of vesicle contents. Biochim Biophys Acta 817: 67–74PubMedCrossRefGoogle Scholar
  57. Marechal LR (1984) Transport and metabolism of trehalose in Escherichia coli and Salmonella typhinutrium. Arch Microbiol 137: 70–73PubMedCrossRefGoogle Scholar
  58. Martin MC, Diaz LA, Manzanal MB, Hardisson C (1986) Role of trehalose in the spores of Streptomyces. FEMS Microbiol Lett 35: 49–54CrossRefGoogle Scholar
  59. McBride MJ, Ensign JC (1987) Effects of intracellular trehalose content on Streptomyces griseus spores. J Bacteriol 169: 4995–5001PubMedGoogle Scholar
  60. Mouradian R, Womersley C, Crowe LM, Crowe JH (1984) Preservation of functional integrity during long term storage of a biological membrane. Biochim Biophys Acta 778: 615–617PubMedCrossRefGoogle Scholar
  61. Murao S, Nagano H, Ogura S, Nishino T (1985) Enzymatic synthesis of trehalose from maltose. Agric Biol Chem 49: 2113–2118CrossRefGoogle Scholar
  62. Oda Y, Uno K, Ohta S (1986) Selection of yeasts for breadmaking by the frozen-dough method. Appl Environ Microbiol 52: 941–943PubMedGoogle Scholar
  63. Ozer Y, Talsma H, Crommelin DJA, Hincal AA (1988) Influence of freezing and freeze-drying on the stability of liposomes dispersed in aqueous media. Acta Pharmacol Technol 34: 129–139Google Scholar
  64. Panek AD (1985) Trehalose metabolism and its role in Saccharomyces cerevisiae. J Biotechnol 3: 121–130CrossRefGoogle Scholar
  65. Panek AD, Bemardes EJ (1983) Trehalose: its role in germination of Saccharomyces cerevisiae. Curr Genet 7: 393–397CrossRefGoogle Scholar
  66. Panek AD, de Araujo PS, Neto VM, Panek AD (1987) Regulation of the trehalose-6-phosphate synthase complex in Saccharomyces. Curr Genet 11: 459–465Google Scholar
  67. Paschoalin VMF, Costa-Carvalho VLA, Panek AD (1986) Further evidence for the alternative pathway of trehalose synthesis linked to maltose utilization in Saccharomyces. Curr Genet 10: 725–731PubMedCrossRefGoogle Scholar
  68. Paschoalin VMF, Panek AC, Panek AD (1987) Catabolite inactivation of trehalose synthesis during growth of yeast on maltose. Braz J Med Biol Res 20: 675–683PubMedGoogle Scholar
  69. Piper PW, Lockheart A (1988) A temperature-sensitive mutant of Saccharomyces cerevisiae defective in the specific phosphatase of trehalose biosynthesis. FEMS Microbiol Lett 49: 245–250CrossRefGoogle Scholar
  70. Postma PW, Keizer HG, Koolwijk P (1986) Transport of trehalose in Salmonella typhimurium. J Bacteriol 168: 1107–1111PubMedGoogle Scholar
  71. Poy F, Jacobson GR (1990) Evidence that a low-affinity sucrose phosphotransferase activity in Streptococcus mutans GS-5 is a high-affinity trehalose uptake system. Infect Immun 58: 1479–1480PubMedGoogle Scholar
  72. Quinn PJ (1989) Effect of sugars on the phase behaviour of phospholipid model membranes. Biochem Soc Trans 17: 953–957PubMedGoogle Scholar
  73. Rapoport AI, Beker ME (1983) Effect of sucrose and lactose on resistance of the yeast Saccharomyces cerevisiae to dehydration. Mikrobiologiya 52: 556–559Google Scholar
  74. Reshkin SJ, Cassano G, Womersley C, Ahearn GA (1990) Preservation of glucose transport and enzyme activity in fish intestinal brush border and basolateral membrane vesicles. J Exp Biol 140: 123–136Google Scholar
  75. Strauss G, Hauser H (1986) Stabilization of lipid bilayer vesicles by sucrose during freezing. Proc Natl Acad Sci USA 83: 2422–2426PubMedCrossRefGoogle Scholar
  76. Strauss G, Schurtenberger P, Hauser H (1986) The interaction of saccharides with lipid bilayer vesicles: stabilization during freeze-thawing and freeze-drying. Biochim Biophys Acta 858: 169–180PubMedCrossRefGoogle Scholar
  77. Streeter JG (1985) Accumulation of alpha, alpha-trehalose by Rhizobium bacteria and bacteroids. J Bacteriol 164: 78–84PubMedGoogle Scholar
  78. Tanford C (1980) The Hydrophobic Effect. Wiley, New YorkGoogle Scholar
  79. Tsvetkov TD, Tsonev LI, Tsvetkova NM, Koynova RD, Tenchov BG (1989) Effect of trehalose on the phase properties of hydrated and lyophilized dipalmitoylphosphatidylcholine multilayers. Cryobiology 26: 162–169PubMedCrossRefGoogle Scholar
  80. Tsvetkova N, Tsvetkov TS, Tenchov B, Tsonev L (1988) Dependence of trehalose protective action on the initial phase state of dipalmitoylphosphatidylcholine bilayers. Cryobiology 25: 256–263PubMedCrossRefGoogle Scholar
  81. Van Laere A, Siegers LK (1987) Trehalose breakdown in germinating spores of Mucor rouxii. FEMS Microbiol Lett 41: 247–252CrossRefGoogle Scholar
  82. Van Laere A, Francois A, Overloop K, Verbeke M, Van Gerven L (1987) Relation between germination, trehalose and the status of water in Phycomyces blakesleeanus spores as measured by proton-NMR. J Gen Microbiol 133: 239–245Google Scholar
  83. Van Steveninck J, Ledeboer AM (1974) Phase transitions in the yeast cell membrane. The influence of temperature on the reconstitution of active dry yeast. Biochim Biophys Acta 352: 64–70PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1992

Authors and Affiliations

  • J. H. Crowe
    • 1
  • L. M. Crowe
    • 1
  1. 1.Department of ZoologyUniversity of CaliforniaDavisUSA

Personalised recommendations