Mechanisms of desiccation tolerance in cyanobacteria

European Journal of Phycology

Volumn 34, Issue 4, 1999, Pages 319-328

  Potts, Malcolm ^a  

^a Fralin Life Science Institute   (United States)

Author keywords

Cyanobacteria; Desiccation; EPS; Membranes; Nostoc; Nucleic acids

Indexed keywords

CYANOBACTERIUM; DESICCATION; TOLERANCE;

CHROOCOCCIDIOPSIS; LYNGBYA; MICROCOLEUS; NOSTOC COMMUNE; TOLYPOTHRIX;

EID: 0032764530     PISSN: 09670262     EISSN: None     Source Type: Journal    
DOI: 10.1017/S0967026299002267     Document Type: Short Survey

References (115)

1. ADHIKARY, S.P. (1998). Polysaccharides from mucilaginous envelope layers of cyanobacteria and their ecological significance. J. Sci. Indust. Res., 57: 454-466.
2. ALLEN, M.M. (1984). Cyanobacterial cell inclusions. Annu. Rev. Microbiol., 38: 1-25.
3. AMARPALLI, R., TRIPATHY, P. & ADHIKARY, S.P. (1997). Epilithic blue-green algae/cyanobacteria from temples of India and Nepal. Presence of UV sunscreen pigments. Algol. Stud., 86: 147-161.
4. ANGELONI, S.V. & POTTS, M. (1986). Polysome turnover in immobilized cells of Nostoc commune (Cyanobacteria) exposed to water stress. J. Bacteriol., 168: 1036-1039.
5. BIEGER-DOSE, A., DOSE, K., MEFFERT, R., MEHLER, M. & RISI, S. (1992). Extreme dryness and DNA-protein cross-links. Adv. Space. Res., 12: 265-270.
6. BILLI, D. & POTTS, M. (1999). Life without water: responses of prokaryotes to desiccation. In Cell and Molecular Responses to Stress (Storey, K.B. & Storey, J.M., editors). JAI Press, Connecticut, in press.
7. BILLI, D., CAIOLA, M.G., PAOLOZZI, L. & GHELARDINI, P. (1998). A method for DNA extraction from the desert cyanobacterium Chroococcidiopsis and its application to identification of ftsZ. Appl. Environm. Microbiol., 64: 4053-4056.
8. BÖGER, P. and DURNER, J. (1995). Ubiquitin in the prokaryote Anabaena variabilis. J. Biol. Chem., 24: 3720-3725.
9. BÖHME, G.A., PFLIEDERER, W., BÖGER, P. & SCHERER, S. (1995). Structure of a novel oligosaccharide-mycosporine amino acid ultraviolet-A/B sunscreen pigment from the terrestrial cyanobacterium Nostoc commune. J. Biol. Chem., 270: 8536-8539.
10. CAMERON, R.E. (1962). Species of Nostoc Vaucher occurring in the Sonoran Desert in Arizona. Trans. Am. Microsc. Soc., 81: 379-384.
11. CAIOLA, M.G., BILLI, D. & FRIEDMANN, E.I. (1996). Effect of desiccation on envelopes of the cyanobacterium Chroococcidiopsis sp. (Chroococcales). Eur. J. Phycol., 31: 97-105.
12. CAIOLA, M.G., OCAMPO-FREIDMANN, R. & FRIEDMANN, E.I. (1993). Cytology of long-term desiccation in the desert cyanobacterium Chroococcidiopsis (Chroococcales). Phycologia, 32: 315-322.
13. CANO, R.J. & BORUCKI, M.K. (1995). Revival and identification of bacterial spores in 25-to 40-million-year-old Dominican amber. Science, 268: 1060-1064.
14. CARPENTER, J.F. & CROWE, J.H. (1989) An infrared spectroscopic study of the interactions of carbohydrates with dried proteins. Biochemistry, 28: 3916-3922.
15. CIFERRI, O. (1983). Spirulina, the edible microorganism. Microbiol. Rev., 47: 551-578.
16. CLEGG, J.S. (1978). Hydration-dependent metabolic transitions and the state of cellular water in Artemia cysts. In Dry Biological Systems (Crowe J.H. & Clegg J.S., editors), 117-153. Academic Press, London.
17. CROWE, J.H., & CROWE, L.M. (1986). Stabilization of membranes in anhydrobiotic organisms. In Membranes, metabolism and dry organisms. (Leopold A.C., editor), 188-209. Cornell University Press, Ithaca, NY.
18. CROWE, J.H. & CROWE, L.M. (1992a). Membrane integrity in anhydrobiotic organisms: toward a mechanism for stabilizing dry cells. In Water and life. (Somero, G.N., Osmond, CB & Bolis, C.L., editors), 87-103. Springer, Berlin.
19. CROWE, L.M. & CROWE, J.H. (1992b). Anhydrobiosis: a strategy for survival. Adv. Space Res., 12: 239-247.
20. CROWE, J.H., CROWE, L.M., CARPENTER, J.F. & AURELL WISTROM, C. (1987). Stabilization of dry phospholipid bilayers and proteins by sugars. Biochem. J., 242: 1-10.
21. CROWE, J.H., HOEKSTRA, F.A. & CROWE, L.M. (1992). Anydrobiosis. Annu. Rev. Physiol., 54: 579-599.
22. DE CHAZAL, N.M., SMAGLINSKY, S. & SMITH, G.D. (1992). Methods involving light variation for isolation of cyanobacteria: characterization of isolates from central Australia. Appl. Environm. Microbiol., 58: 3561-3566.
23. DOR, I. & PAZ, N. (1989). Temporal and spatial distribution of mat microalgae in the experimental solar ponds, Dead Sea area, Israel. In Microbial Mats: Physiological Ecology of Benthic Microbial Communities (Cohen, Y. & Rosenberg, E., editors), 114-122. American Society for Microbiology, Washington, DC.
24. DOSE, K., BIEGER-DOSE, A., LABUSCH, M. & GILL, M. (1992). Survival in extreme dryness and DNA-single-strand breaks. Adv. Space Res., 12: 221-229.
25. EHLING-SCHULZ, M., BILGER, W. & SCHERER, S. (1997). UV-B-induced synthesis of photoprotective pigments and extracellular polysaccharides in the terrestrial cyanobacterium Nostoc commune. J. Bacteriol., 179: 1940-1945.
26. EVERSHED, R.P., BLAND, H.A., VAN BERGEN, P.F., CARTER, J.F., HORTON, M.C. & ROWLEY-CONWY, P.A. (1997). Volatile compounds in archaeological plant remains and the Maillard reaction during decay of organic matter. Science, 278: 432-433.
27. FINNEY, J.L. (1977). The organization and function of water in protein crystals. Proc. R. Soc. Lond., Ser. B, 278: 3-32.
28. FOGG, G.E. (1982). Marine plankton. In The Biology of Cyanobacteria (Carr, N.G. & Whitton, B.A., editors), 491-513. Blackwell Scientific, Oxford.
29. FRANKS, F. (1977). Solvation interactions of proteins in solution. Proc. R. Soc. Lond. Ser. B, 278: 89-96.
30. FRANKS, F. (1988). Characterization of Proteins. Humana Press, Clifton, NJ.
31. FRIEDMANN, E.I. (1971). Light and scanning electron microscopy of the endolithic desert algal habitat. Phycologia, 10: 411-428.
32. FRIEDMANN, E.I. (1982). Endolithic microorganisms in the Antarctic cold desert. Science, 215: 1045-1053.
33. FRIEDMANN, E.I. & WEED. R. (1987). Microbial trace-fossil formation, biogenous, and abiotic weathering in the Antarctic Cold Desert. Science, 236: 703-705.
34. FRIEDMANN, E.I., HUA, M. & OCAMPO-FRIEDMANN, O. (1988). Cryptoendolithic lichen and cyanobacterial communities of the Ross Desert, Antarctica. Polarforschung, 58: 251-159.
35. FRIEDMANN, E.I., KAPPEN, L., MEYER, M.A. & NIENOW, J.A. (1993). Long-term productivity in the cryptoendolithic microbial community of the Ross Desert, Antarctica. Microb. Ecol., 25: 51-69.
36. GAO, K. (1998). Chinese studies on the edible blue-green alga, Nostoc flagelliforme: a review. J. Appl. Phycol., 10: 337-349.
37. GAO, K., QIU, B., XIA, J., YU, A. & LI, Y. (1998a). Effect of wind speed on loss of water from Nostoc flagelliforme colonies. J. Appl. Phycol., 10: 55-58.
38. GAO, K., QIU, B., XIA, J. & YU, A. (1998b). Light dependency of the photosynthetic recovery of Nostoc flagelliforme. J. Appl. Phycol., 10:51-53.
39. GARCIA-PICHEL, F. & CASTENHOLZ, R. (1999). Cyanobacterial responses to UV radiation. In The Ecology of Cyanobacteria; Their Success in Time and Space (Whitton, B.A. & Potts, M., editors). Kluwer Academic, Dordrecht, in press.
40. GERHARDT, P. (1998). Survival of ancient bacteria desiccated within amber: believe it or not? ASM News, 64: 68-69.
41. GILICHINSKY, D.A., VOROBYOVA, E.A., EROKHINA, L.G., FYODOROV-DAYVDOV, D.G. & CHAIKOVSKAYA, N.R. (1992). Long-term preservation of microbial ecosystems in permafrost. Adv. Space Res., 12: 255-263.
42. HERDMAN, M., JANVIER, M., RIPPKA, R. & STANIER, R.Y. (1979). Genome size of cyanobacteria. J. Gen. Microbiol., 111: 73-85.
43. HILL, D.R., HLADUN, S.L., SCHERER, S. & POTTS, M. (1994a). Water stress proteins of Nostoc commune (Cyanobacteria) are secreted with UV-A/B-absorbing pigments and associate with 1,4-β-D-xylanxylanohydrolase activity. J. Biol. Chem., 269: 7726-7734.
44. HILL, D.R., PEAT, A. & POTTS, M. (1994b). Biochemistry and structure of the glycan secreted by desiccation-tolerant Nostoc commune (Cyanobacteria). Protoplasma, 182: 126-148.
45. HILL, D.R., KEENAN, T.W., HELM, R.F., POTTS, M., CROWE, L.M. & CROWE, J.H. (1997). Extracellular polysaccharide of Nostoc commune (Cyanobacteria) inhibits fusion of membrane vesicles during desiccation. J. Appl. Phycol., 9: 237-248.
46. ITO, T. (1992). The effects of vacuum-UV radiation (20-190 nm) on microorganisms and DNA. Adv. Space Res., 12: 249-253.
47. JAENICKE, R. (1991). Protein stability and molecular adaptation to extreme conditions. Eur. J. Biochem., 202: 715-728.
48. JAENICKE, R. (1993). Molecular adaptation of proteins to extremes of physical conditions. Cryobiology, 30: 211-212.
49. JÄGER, K. & Potts, M. (1988a). In vitro translation of mRNA from Nostoc commune (Cyanobacteria). Arch. Microbiol., 149: 225-231.
50. JÄGER, K. & POTTS, M. (1988b). Distinct fractions of genomic DNA from cyanobacterium Nostoc commune that differ in the degree of methylation. Gene, 74: 197-201.
51. KENNEDY, M.J., READER, S.L. & SWIERCZYNSKI, L.M. (1994). Preservation records of micro-organisms : evidence of the tenacity of life. Microbiology, 140: 2513-2529.
52. KOGUT, M. & RUSSELL, N.J. (1987). Life at the limits: considerations on how bacteria can grow at extremes of temperature and pressure, or with high concentrations of ions and solutes. Sci. Progr., Oxf., 71: 381-399.
53. LAUDENBACH, D.E. & GROSSMAN, A. (1991). Characterization and mutagenesis of sulfur-regulated genes in a cyanobacterium: evidence for function in sulfate transport. J. Bacteriol., 173: 2739-2750.
54. LEE, C.W.B., WAUGH, J.S. & GRIFFIN, R.G. (1986). Solid-state NMR study of trehalose/1,2-dipalmitoyl-sn-phosphatidylcholine interactions. Biochemistry, 25: 3737-3742.
55. LEE, C.W.B., DASGUPTA, S.K., MATTAI, J., SHIPLEY, G.G., ABDEL-MAGEED, O.L., MAKRIYANNIS, A. & GRIFFIN, R.G. (1989). Characterization of the L-phase in trehalose-stabilized dry membranes by solid-state NMR and X-ray diffraction. Biochemistry, 28: 5000-5009.
56. LESLIE, S.B., TETER, S.B., CROWE, L.M. & CROWE, J.H. (1994). Trehalose lowers membrane phase transitions in dry yeast cells. Biochim. Biophys. Acta, 1192: 7-13.
57. LINDAHL, T. (1993). Instability and decay of the primary structure of DNA. Nature, 362: 709-715.
58. LINDAHL, T. & NYBERG, B. (1972). Rate of depurination of native deoxyribonucleic acid. Biochemistry, 11: 3610-3618.
59. LINDBERG, C. & HORNECK, G. (1992). Thymine photoproduct formation and inactivation of intact spores of Bacillus subtilis irradiated with short wavelength UV (200-300 nm) at atmospheric pressure and in vacuo. Adv. Space Res., 12: 275-279.
60. LINDSAY, J.A. & MURRELL, W.G. (1983). A comparison of UV-induced DNA photoproducts from isolated and non-isolated developing bacterial forespores. Biochem. Biophys. Res. Commun., 113: 618-625.
61. LOUNNAS, V., MONTGOMERY PETTITT, G. & PHILLIPS, G.N. JR (1994). A global model of the protein-solvent interface. Biophys. J., 66: 601-614.
62. MANCINELLI, R.L., WHITE, M.R. & ROTHSCHILD, L.J. (1998). Biopan-survival 1: exposure of the osmophiles Synechococcus sp. (Nägeli) and Haloarcula sp. to the space environment. Adv. Space Res., 22: 327-334.
63. MARSHALL, W.A. & CHALMERS, M.O. (1997). Airborne dispersal of antarctic terrestrial algae and cyanobacteria. Ecography, 20: 585-594.
64. MATTIMORE, V. & BATTISTA, J.R. (1996). Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation J. Bacteriol., 178: 633-637.
65. MEURY, J. & KOHIYAMA, M. (1992). Potassium ions and changes in bacterial DNA supercoiling under osmotic stress. FEMS Microbiol. Lett., 99: 159-164.
66. NIENOW, J.A. & FRIEDMANN, E.I. (1993). Terrestrial lithophytic (rock) communities. In Antarctic Microbiology (Friedmann, E. I. & Thistle, A.B., editors), 343-412. Wiley, New York.
67. OKSANEN, C.A. & ZOGRAFI, G. (1993). Molecular mobility in mixtures of absorbed water and solid poly(vinylpyrrolidone). Pharm. Res., 10: 791-799.
68. OLIE, J.J. & POTTS, M. (1986). Purification and biochemical analysis of the cytoplasmic membrane from the desiccation-tolerant cyanobacterium Nostoc commune UTEX 584. Appl. Environm. Microbiol., 52: 706-710.
69. OLIVER, A.E., CROWE, L.M. & CROWE, J.H. (1998). Methods for dehydration-tolerance: depression of the phase transition temperature in dry membranes and carbohydrate vitrification. Seed Sci. Res., 8: 211-221.
70. ORCUTT, D.M., PARKER, B.C. & LUSBY, W.R. (1986). Lipids in blue-green algal mats (modern stromatolites) from Antarctic oasis lakes. J. Phycol., 22: 523-530.
71. PALCHAUDHURI, S., TOMINNA, B. & LEAON, M.A. (1998). H-NS regulates DNA repair in Shigella. J. Bacteriol., 180: 5260-5262.
72. PALMER, R.J. & FRIEDMANN, E.I. (1990). Water relations and photosynthesis in the cryptoendolithic microbial habitat of hot and cold deserts. Microb. Ecol., 19: 111-118.
73. PEAT, A., POWELL, N. & POTTS, M. (1988). Ultrastructural analysis of the rehydration of desiccated Nostoc commune HUN (Cyanobacteria) with particular reference to the immunolabelling of NifH. Protoplasma, 146: 72-80.
74. PENTECOST, A. (1985). Relationships between light, temperature and photosynthesis in a temperate Microcoleus (cyanobacterium) mat. Microbios, 43: 141-148.
75. PHILIPPIS, R. DE & VINCENZINI, M. (1998). Exocellular polysaccharides from cyanobactyeria and their possible applications. FEMS Microbiol. Rev., 22: 151-175.
76. POSTGATE, J. & PRIEST, F.G. (1995). Putative oligocene spores. Microbiology, 14: 2763-2764.
77. POTTS, M. (1977). PhD. thesis, University of Durham, UK.
78. POTTS, M. (1985). Protein synthesis and proteolysis in immobilized cells of the cyanobacterium Nostoc commune UTEX 584 exposed to matric water stress. J. Bacteriol., 164: 1025-1031.
79. POTTS, M. (1986). The protein index of Nostoc commune UTEX 584 (cyanobacteria): changes induced in immobilized cells by water stress. Arch. Microbiol., 146: 87-95.
80. POTTS, M. (1994). Desiccation tolerance of prokaryotes. Microbiol. Rev., 58: 755-805.
81. POTTS, M. (1999). Nostoc. In: The Ecology of Cyanobacteria; Their Success in Time and Space, (Whitton, B.A. & Potts, M., editors). Kluwer Academic, Dordrecht, in press.
82. POTTS, M. & BOWMAN, M.A. (1985). Sensitivity of Nostoc commune UTEX 584 (Cyanobacteria) to water stress. Arch. Microbiol., 141: 51-56.
83. POTTS, M. & WHITTON, B.A. (1977). Nitrogen fixation by blue-green algal communities in the intertidal zone of the lagoon of Aldabra Atoll. Oecologia (Berl.), 27: 275-283.
84. POTTS, M. & WHITTON, B.A. (1980). Vegetation of the intertidal zone of the lagoon of Aldabra, with particular reference to the photosynthetic prokaryotic communities. Proc. R. Soc. Lond., Ser. B, 208: 13-55.
85. m) in immobilized cultures of cyanobacteria. FEMS Microbiol. Lett., 24: 193-196.
86. PRIEST, F.G. (1995). Age of bacteria from amber. Science, 270: 2015.
87. QUIOCHO, F.A., WILSON, D.K. & VYAS, N.K. (1989). Substrate specificity and affinity of a protein modulated by bound water molecules. Nature, 340: 404-407.
88. RECORD, M.T. JR, COURTENAY, E.S., CAYLEY, D.S. & GUTTMAN,. H.J. (1998). Responses of E. coli to osmotic stress; large changes in amounts of cytoplasmic solutes and water. Trends Biol. Sci., 23: 143-148.
89. RITTER, D. & YOPP, J.H. (1993). Plasma membrane lipid composition of the halophilic cyanobacterium Aphanothece halophytica. Arch. Microbiol., 159: 435-439.
90. RODGERS, G.A. (1977). Nitrogenase activity in Nostoc muscorum; recovery from desiccation. Plant Soil, 46: 671-674.
91. RUSSELL, N.J. (1990). Cold adaptation of microorganisms. Phil. Trans. R. Soc. Lond., Ser. B, 326: 595-611.
92. RUSSELL, N.J. & FUKUNAGA, N. (1990). A comparison of thermal adaptation of membrane lipids in psychrophilic and thermophilic bacteria. FEMS Microbiol. Rev., 75: 171-182.
93. SCHERER, S. (1991). Mikroorganismen in extremen Lebensräumen: cyanobakterien in Wüstengebieten. Biol. Zeit, 4: 220-222.
94. SCHERER, S. & POTTS, M. (1989). Novel water stress protein from a desiccation-tolerant cyanobacterium : purification and partial characterization. J. Biol. Chem., 264: 12546-12553.
95. SCHERER, S. & ZHONG, Z.-P. (1991). Desiccation independence of terrestrial Nostoc commune ecotypes (Cyanobacteria). Microb. Ecol., 22: 271-283.
96. SCHWARZ, R. & GROSSMAN, A.R. (1998). A response regulator of cyanobacteria integrates diverse environmental signals and is critical for survival under adverse extreme conditions. Proc. Natl. Acad. Sci. USA, 95: 11008-11013.
97. SIMON, P. (1980). DNA content of heterocysts and spores of the filamentous cyanobacterium Anabaena variabilis. FEMS Microbiol. Lett., 8: 241-245.
98. SLADE, L. & LEVINE, H. (1991). Beyond water activity: Recent advances based on an alternative approach to the assessment of food quality and safety. Crit. Rev. Food Sci. Nutrit., 30: 115-360.
99. STACEY, R.A.P. & AALEN, R.B. (1998). Identification of sequence homology between the internal hydrophilic repeated motifs of group 1 late-embryogenesis-abundant proteins in plants and hydrophilic repeats of the general stress protein GsiB of Bacillus subtilis. Planta, 206: 476-478.
100. STULP, B.K. & POTTS, M. (1987). Stability of nucleic acids in immobilized and desiccated Nostoc commune UTEX 584 (Cyanobacteria). FEMS Microbiol. Lett., 41: 241-245.
101. TARANTO, P.A., KEENAN, T.W. & POTTS, M. (1993). Rehydration induces rapid onset of lipid biosynthesis in desiccated Nostoc commune (Cyanobacteria). Biochim. Biophys. Acta, 1168: 228-237.
102. TIMASHEFF, S.N. (1993). Stabilization of proteins by cosolvents in aqueous media. Cryobiology, 30: 218-219.
103. TRIPATHY, P., AMARPALLI, R & ADHIKARY, S.P. (1997). Survey of epilithic blue-green algae (cyanobacteria) from temples of India and Nepal. Algol. Stud., 87: 43-57.
104. VASAN, S., ZHANG, X., ZHANG, X., KAPURNIOTU, A., BERNHAGEN, J., TEICHBERG, S., BASGEN, J., WAGLE, D., SHIH, D., TERLECKY, I., BUCALA, R., CERAMI, A., EGAN, J. & ULRICH, P. (1996). An agent cleaving glucose-derived protein crosslinks in vitro and in vivo. Nature, 382: 275-278.
105. WALSBY, A.E. (1982). Cell-water and cell-solute relations. In The Biology of Cyanobacteria (Carr, N.G. & Whitton, B.A., editors), 237-262. Blackwell Scientific, Oxford.
106. WANNER, B.L. (1987). Phosphate regulation of gene expression in Escherichia coli. In Escherichia coli and Salmonella typhimurium, Cellular and Molecular Biology (Neidhardt, F.C., Ingraham, J.L., Brooks Low, K., Magasanik, B., Shaechter, M. & Umbarger, H.E., editors), 1326-1333. American Society for Microbiology, Washington, DC.
107. WARD, D.M., WELLER, R., SHIEA, J., CASTENHOLZ, R.W. & COHEN, Y. (1989). Hot spring microbial mats: anoxygenic and oxygenic mats of possible evolutionary significance. In Microbial Mats: Physiological Ecology of Benthic Microbial Communities (Cohen Y. & Rosenberg, E., editors), 3-15. American Society for Microbiology, Washington DC.
108. WEBB, S.J. (1965). Bound Water in Biological Integrity. C.C. Thomas, Springfield, IL.
109. WEISSENBORN, D.L., WITTEKINDT, N. & LARSON, T.J. (1992). Structure and regulation of the glpFK operon encoding glycerol diffusion facilitator and glycerol kinase of Escherichia coli K-12. J. Biol. Chem., 267: 6122-6131.
110. WHITTON, B.A. (1992). Diversity, ecology, and taxonomy of the cyanobacteria. In Photosynthetic Prokaryotes (Mann, N.H. & Carr, N.G., editors), 1-51. Plenum Press, New York.
111. WHITTON, B.A. & POTTS, M., (eds.) (1999). The Ecology of Cyanobacteria; Their Success in Time and Space. Kluwer Academic, Dordrecht, in press.
112. WHITTON, B.A., DONALDSON, A. & POTTS, M. (1979). Nitrogen fixation by Nostoc colonies in terrestrial environments of Aldabra Atoll, Indian Ocean. Phycologia, 18: 278-287.
113. WYNN-WILLIAMS, D., ELLIS-EVANS, C. & LEAKEY, R. (1992). Microbial ecology in Antarctica. Soc. Gen. Microbiol. Quarterly, (Nov): 99-104.
114. XIE, W.-Q., TICE, D. & POTTS, M. (1995). Cell water deficit regulates expression of rpoC1C2 (RNA polymerase) at the level of mRNA in desiccation-tolerant Nostoc commune UTEX 584 (Cyanobacteria). FEMS Microbiol. Lett., 126: 159-164.
115. YASUI, A. & MCREADY, S.J. (1998). Alternative repair pathways for UV-induced DNA damage. BioEssays, 20: 291-297.