Production of Dormant Stages and Stress Resistance of Polar Cyanobacteria

  • Daria Tashyreva
  • Josef Elster
Part of the Cellular Origin, Life in Extreme Habitats and Astrobiology book series (COLE, volume 24)


Cyanobacteria represent the major component of the autotrophic community in many different types of habitats in both the Arctic and Antarctic. Their dominance is attributed mainly because of their high tolerance to the extreme polar environments. Low temperatures and desiccation are the main forms of physical environmental stressors. During freezing-melting and desiccation periods, the cells are exposed to radical dehydration effects which can be quite damaging. Polar cyanobacteria have evolved a diverse range of protective strategies in order to avoid, or tolerate, the various stresses. The most widespread adaptation to environmental stress is dormancy. Dormancy can be subdivided into diapause and quiescence. Diapause (the cyanobacterial akinete) is endogenously controlled: it is connected to external stressors but is not directly induced by them. Akinetes are more resistant to various insults and commonly considered as overwintering stages. However, the majority of cyanobacteria in the polar regions survive winters without the production of akinetes. This suggests that other alternative mechanisms contribute to survival during stressful conditions. Quiescence (the decrease of metabolic activity under exogenous control) is the transformation into a resistant state, with hardly visible morphological differentiation of the cell. It has been suggested that starvation and entrance into the stationary phase can induce changes in the ultrastructure (e.g., thickening of cell walls) and biochemistry (e.g.,sucrose and trehalose accumulation, changes in composition of fatty acids, secretion of extracellular polysaccharides) of the stressed cells. We accept that the stationary-phase and/or starvation-induced cells can represent alternative dormant stages of polar cyanobacteria which do not produce akinetes. This overview summarizes the present knowledge about production of dormant stages and stress resistance of polar cyanobacteria. It is clear that we still have paucity of information on this topic and that further research is necessary.


Desiccation Tolerance Filamentous Cyanobacterium Dormant Stage Cyanobacterial Community Enhance Freezing Tolerance 
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.



The study was made possible with the support of grants from the Ministry of Education of the Czech Republic (Kontakt ME 934, and INGO – LA 341).


  1. Acker JP, McGann LE (2003) Protective effect of intracellular ice during freezing? Cryobiology 46:197–2002Google Scholar
  2. Agrawal SC (2009) Factors affecting spore germination in algae – review. Folia Microbiol 54(4):273–302Google Scholar
  3. Agrawal SC, Singh V (1999) Viability of dried vegetative trichomes, formation of akinetes and heterocysts and akinete germination in some blue-green algae under water stress. Folia Microbiol 44(4):411–418Google Scholar
  4. Alekseev VR, Hwang J, Tseng M (2006) Diapause in aquatic invertebrates: what’s known and what’s next in research and medical application? J Mar Sci Technol 14(4):269–286Google Scholar
  5. Alpert P (2005) The limits and frontiers of desiccation-tolerant life. Integr Comp Biol 45:685–695Google Scholar
  6. Alpert P (2006) Constrains of tolerance: why are desiccation-tolerant organisms so small or rare? J Exp Biol 209:1575–1584Google Scholar
  7. Argüelles JC (2000) Physiological role of trehalose in bacteria and yeasts: a comparative analysis. Arch Microbiol 174:217–224Google Scholar
  8. Billi D, Grilli Caiola M (1996) Effects of nitrogen limitation and starvation on Chroococcidiopsissp. (Chroococcales). New Phytol 133:563–571Google Scholar
  9. Billi D, Potts M (2000) Life without water: responses of prokaryotes to desiccation. In: Storey KB, Storey J (eds) Environmental stressors and gene responses. Elsevier Science, Amsterdam, pp 181–192Google Scholar
  10. Broady PA (1996) Diversity, distribution and dispersal of Antarctic algae. Biodivers Conserv 5:1307–1335Google Scholar
  11. Casamatta DA, Johansen JR, Vis ML, Broadwater ST (2005) Molecular and morphological characterization of ten polar and near-polar strains within the Oscillatoriales (cyanobacteria). J Phycol 41:421–438Google Scholar
  12. Castenholz RW, Jørgensen BB, D’Amelio E, Bauld J (1991) Photosynthetic and behavioral versatility of the cyanobacterium Oscillatoria boryanain a sulfide-rich microbial mat. FEMS Microbiol Ecol 86:43–58Google Scholar
  13. Cavacini P (2001) Soil algae from northern Victoria Land (Antarctica). Polar Biosci 14:45–60Google Scholar
  14. Colwell RR (2009) Viable but not cultivable bacteria. Microbiol Monogr 10:121–129Google Scholar
  15. Colwell RR, Grimes DJ (2000) Semantics and strategies. In: Colwell RR, Grimes DJ (eds) Nonculturable microorganisms in the environment. ASM Press, Washington, DC, pp 1–6Google Scholar
  16. Cronan JR (1968) Phospholipid alterations during growth of Escherichia coli. J Bacteriol 95(6):2054–2061Google Scholar
  17. Crowe JH, Oliver AE, Tablin F (2002) Is there a single biochemical adaptation to anhydrobiosis? Integr Comp Biol 42:497–503Google Scholar
  18. Crowe JH, Crowe LM, Tablin F, Wolkers W, Oliver AE, Tsvetkova NM (2004) Stabilization of cells during freeze-drying: the trehalose myth. In: Fuller BJ, Lane N, Benson EE (eds) Life in frozen state. CRC Press, London, pp 581–602Google Scholar
  19. Damerval T, Guglielmi G, Houmard J, Tandeau de Marsac N (1991) Hormogonium differentiation in the cyanobacterium Calothrix: a photoregulated developmental process. Plant Cell 3:191–201Google Scholar
  20. Davey MC (1989) The effects of freezing and desiccation on photosynthesis and survival of terrestrial Antarctic algae and cyanobacteria. Polar Biol 10:29–36ADSGoogle Scholar
  21. Davey MC, Clarke KJ (1991) The spatial distribution of microalgae on Antarctic fellfield soils. Antarct Sci 3(3):257–263Google Scholar
  22. Davies PL, Baardsnes J, Kuiper MJ, Walker VK (2002) Structure and function of antifreeze proteins. Phil Trans R Soc Lond 357:927–935Google Scholar
  23. De los Ríos A, Ascaso C, Wierzchos J, Fernández-Valiente E, Quesada A (2004) Microstructural characterization of cyanobacterial mats from the McMurdo Ice Shelf. Antarct Appl Environ Microbiol 70(1):569–580Google Scholar
  24. Dillon JG, Castenholz RW (1999) Scytonemin, a cyanobacterial sheath pigment, protects against UVC radiation: implications for early photosynthetic life? J Phycol 35:673–681Google Scholar
  25. Ehling-Schulz M, Scherer S (1999) UV protection in cyanobacteria. Eur J Phycol 34:329–338Google Scholar
  26. El’-Registan GI, Mulyukin AL, Nikolaev YA, Suzina NE, Gal’chenko VF, Duda VI (2006) Adaptogenic functions of extracellular autoregulators of microorganisms. Microbiology 75(4):380–389Google Scholar
  27. Elster J (1999) Algal versatility in various extreme environments. In: Seckbach J (ed) Enigmatic microorganisms and life in extreme environments. Kluwer Academic Publishers, Dordrecht, pp 215–227Google Scholar
  28. Elster J (2002) Ecological classification of terrestrial algal communities in polar environments. In: Beyer L, Bölter M (eds) Ecological studies, vol 154: Geoecology of Antarctic ice-free coastal landscapes. Springer, Berlin/Heidelberg, pp 303–326Google Scholar
  29. Elster J, Benson EE (2004) Life in the Polar terrestrial environment with a focus on algae and cyanobacteria. In: Fuller BJ, Lane N, Benson EE (eds) Life in frozen state. CRC Press, London, pp 111–150Google Scholar
  30. Elster J, Svoboda J, Komárek J, Marvan P (1997) Algal and cyanoprocaryote communities in a glacial stream, Sverdrup Pass, 79oN, Central Ellesmere Island, Canada. Arch Hydrobiol/Algolog Stud 85:57–93Google Scholar
  31. Fuller BJ (2004) Cryoprotectants: the essential antifreezes to protect life in the frozen state. CryoLetters 25(6):375–388Google Scholar
  32. Gao K, Qiu B, Xia J, Yu A, Li Y (1998) Effect of wind speed on loss of water from Nostoc flagelliformecolonies. J Appl Phycol 10:55–58Google Scholar
  33. Gilichinsky DA, Vorobyova EA, Erokhina LG, Fyodorov-Davydov DG, Chaikovskaya NR (1992) Long-term preservation of microbial ecosystems in permafrost. Adv Space Res 12(4):255–263ADSGoogle Scholar
  34. Gorshkov VY, Petrova OE, Mukhametshina NE, Ageeva MV, Mulyukin AL, Gogolev YV (2009) Formation of “nonculturable” dormant forms of the phytopathogenic enterobacterium Erwinia carotovora. Microbiology 78(5):585–592Google Scholar
  35. Grilli Caiola M, Billi D, Friedmann EI (1996) Effect of desiccation on envelopes of the cyanobacterium Chroococcidiopsissp. (Chroococcales). Eur J Phycol 31:97–105Google Scholar
  36. Hawes I, Howard-Williams C, Vincent WF (1992) Desiccation and recovery of Antarctic cyanobacterial mats. Polar Biol 12:587–594Google Scholar
  37. Helm RF, Huang Z, Edwards D, Leeson H, Peery W, Potts M (2000) Structural characterization of the released polysaccharide of desiccation-tolerant Nostoc communeDRH-1. J Bacteriol 182(4):974–982Google Scholar
  38. Hengge-Aronis R, Klein W, Langen R, Rimmele M, Boos W (1991) Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance in Escherichia coli. J Bacteriol 173(24):7918–7924Google Scholar
  39. Hershkovitz N, Oren A, Cohen Y (1991) Accumulation of trehalose and sucrose in cyanobacteria exposed to matric water stress. Appl Environ Microbiol 57(3):645–648Google Scholar
  40. Hill DR, Hladun SL, Schrerer S, Potts M (1994) 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(10):7726–7734Google Scholar
  41. Hill DR, Keenan TW, Helm RF, Potts M, Crowe LM, Crowe JH (1997) Extracellular polysaccharide of Nostoc commune (Cyanobacteria) inhibits fusion of membrane vesicles during desiccation. J Appl Phycol 9:237–248Google Scholar
  42. Hori K, Okamoto J, Tanji Y, Unno H (2003) Formation, sedimentation and germination properties of Anabaenaakinetes. Biochem Eng J 14:67–73Google Scholar
  43. Jenkins DE, Chaisson SA, Matin A (1990) Starvation-induced cross protection against osmotic challenge in Escherichia coli. J Bacteriol 172(5):2779–2781Google Scholar
  44. Jungblut A, Hawes I, Mounfort D, Hitzfield B, Ditrich DR, Burns BP, Neilan BA (2005) Diversity within cyanobacterial mat communities in variable salinity meltwater ponds of McMurdo Ice Shelf. Antarct Environ Microbiol 7(4):519–529Google Scholar
  45. Kaprelyants AS, Kell DB (1993) Dormancy in stationary-phase cultures of Micrococcus luteus: flow cytometric analysis of starvation and resuscitation. Appl Environ Microbiol 59(10):3187–3196Google Scholar
  46. Kaprelyants A, Gottschal J, Kell D (1993) Dormancy in non-sporulating bacteria. FEMS Microbiol Rev 104:271–286Google Scholar
  47. Keilin D (1959) The problem of anabiosis or latent life: history and current concepts. Proc Roy Soc 150B:149–191ADSGoogle Scholar
  48. Kell DB, Young M (2000) Bacterial dormancy and culturability: the role of autocrine growth factors. Curr Opin Microbiol 3(3):238–243Google Scholar
  49. Kell DB, Ryder HM, Kaprelyants AS, Westerhoff HV (1991) Quantifying heterogeneity: flow cytometry of bacterial cultures. Anton Leeuw 60:145–158Google Scholar
  50. Komárek J, Elster J, Komárek O (2008) Diversity of the cyanobacterial microflora on the northern part of James Ross Iceland, NW Weddell Sea, Antarctica. Polar Biol 31:853–865Google Scholar
  51. Leslie SB, Israeli E, Lighthart B, Crowe JH, Crowe LM (1995) Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying. Appl Environ Microbiol 61(10):3592–3597Google Scholar
  52. Li C, Zhao J, Wang Y, Han X, Liu N (2009) Synthesis of cyclopropane fatty acid and its effect on freeze-drying survival of Lactobacillus bulgaricusL2 at different growth conditions. World J Microbiol Biotechnol 25:1659–1665Google Scholar
  53. Lin Y, Hirai M, Kashino Y, Koike H, Tuzi S, Satoh K (2004) Tolerance to freezing in cyanobacteria with various tolerances to drying stress. Polar Biosci 17:56–68Google Scholar
  54. Livingstone D, Jaworski GHM (1980) The viability of akinetes of blue-green algae recovered from the sediments of Rostherne mere. Eur J Phycol 15:357–364Google Scholar
  55. Lizotte MP (2008) Phytoplankton and primary production. In: Vincent WF, Laybourn-Parry J (eds) Polar lakes and rivers: limnology of Arctic and Antarctic aquatic ecosystems. Oxford University Press, New York, pp 157–178Google Scholar
  56. Lundheim R (2002) Physiological and ecological significance of biological ice-nucleators. Phil Trans R Soc Lond 357:937–943Google Scholar
  57. MacKay MA, Norton RS, Borowitzka LJ (1984) Organic osmoregulatory solutes in cyanobacteria. J Gen Microbiol 130:2177–2191Google Scholar
  58. Mazur P (1984) Freezing of living cells: mechanisms and implications. Am J Physiol Cell Physiol 247:125–142Google Scholar
  59. Meeks JC, Campbell EL, Summers ML, Wong FC (2002) Cellular differentiation in the cyanobacterium Nostoc punctiforme. Arch Microbiol 178:395–403Google Scholar
  60. Morris GJ (1981) Cryopreservation: an introduction to cryopreservation in culture collections. Institute of Terrestrial Ecology, Cambridge, 27 ppGoogle Scholar
  61. Mueller DR, Vincent WF, Bonilla S, Laurion I (2005) Extremotrophs, extremophiles and broadband pigmentation strategies in a high arctic ice shelf ecosystem. FEMS Microbiol Ecol 53:73–87Google Scholar
  62. Mukamolova GV, Yanopolskaya ND, Votyakova TV, Popov VI, Kaprelyants AS, Kell DB (1995) Biochemical changes accompanying the long-term starvation of Micrococcus luteuscells in spent growth medium. Arch Microbiol 163:373–379Google Scholar
  63. Mulyukin AL, Lusta KA, Gryaznova MN, Kozlova AN, Duzha MV, Duda VI, El’-Registan GI (1996) Formation of resting cells by Bacillus cereusand Micrococcus luteus. Microbiology 65(6):683–689Google Scholar
  64. Mulyukin AL, Lusta KA, Gryaznova MN, Babushenko ES, Kozlova AN, Duzha MV, Mityushina LA, Duda VI, El’-Registan GI (1997) Formation of resting cells in microbial suspensions undergoing autolysis. Microbiology 66(1):32–38Google Scholar
  65. Muñoz-Rojas J, Bernal P, Duque E, Godoy P, Segura A, Ramos J (2006) Involvement of cyclopropane fatty acids in the response of Pseudomonas putidaKT2440 to freeze-drying. Appl Environ Microbiol 72(1):472–477Google Scholar
  66. Nadeau T, Castenholz RW (2000) Characterizations of psychrophilic oscillatorians (cyanobacteria) from Antarctic meltwater ponds. J Phycol 36:914–923Google Scholar
  67. Nichols JM, Adams DG (1982) Akinetes. In: Carr NG, Whitton BA (eds) The biology of cyanobacteria. Blackwell Scientific Publications, Oxford, pp 387–412Google Scholar
  68. Notley L, Ferenci T (1996) Induction of RpoS-dependent functions in glucose-limited continuous culture: what level of nutrient limitation induces the stationary phase of Escherichia coli. J Bacteriol 178(5):1465–1468Google Scholar
  69. Oliver JD (2005) The viable but nonculturable state in bacteria. J Microbiol 43:93–100Google Scholar
  70. Ophir T, Gutnick DL (1994) A role of exopolysaccharides in the protection of microorganisms from desiccation. Appl Environ Microbiol 60(2):740–745Google Scholar
  71. Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Mol Biol Rev 58:755–805Google Scholar
  72. Potts M (1999) Mechanisms of desiccation tolerance in cyanobacteria. Eur J Phycol 34:319–328Google Scholar
  73. Potts M, Slaughter SM, Hunneke F, Garst JF, Helm RF (2005) Desiccation tolerance of prokaryotes: application to human cells. Integr Comp Biol 45:800–809Google Scholar
  74. Quesada A, Vincent WF, Lean DRS (1999) Community and pigment structure of Arctic cyano­bacterial assemblages: the occurrence and distribution of UV-absorbing compounds. FEMS Microbiol Ecol 28:315–323Google Scholar
  75. Raymond JA, Fritsen CH (2000) Ice-active substances associate with Antarctic freshwater and terrestrial photosynthetic organisms. Antarct Sci 12(4):418–424Google Scholar
  76. Rebecchi L, Altiero T, Guidetti R (2007) Anhydrobiosis: the extreme limit of desiccation tolerance. Invertebr Surv J 4(2):65–81Google Scholar
  77. Reed RH, Richardson DL, Warr SRC, Stewart WDP (1984) Carbohydrate accumulation and osmotic stress in cyanobacteria. J Gen Microbiol 130:1–4Google Scholar
  78. Roszak DB, Colwell RR (1987) Survival strategies of bacteria in the natural environment. Microbiol Rev 51(3):365–379Google Scholar
  79. Sakamoto T, Yoshida T, Arima H, Hatanaka Y, Takani Y, Tamaru Y (2009) Accumulation of trehalose in response to desiccation and salt stress in the terrestrial cyanobacterium Nostoc commume. Physiol Res 57:66–73Google Scholar
  80. Schwarz R, Forchhammer K (2005) Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses. Microbiology 151:2503–2514Google Scholar
  81. Shaw E, Hill DR, Brittain N, Wright DJ, Täuber U, Marand H, Helm RF, Potts M (2003) Unusual water flux in the extracellular polysaccharide of the cyanobacterium Nostoc commune. Appl Environ Microbiol 69(9):5679–5684Google Scholar
  82. Siegele DA, Kolter R (1992) Life after log. J Bacteriol 174(2):345–348Google Scholar
  83. Singh SC, Sinha RP, Häder D (2002) Role of lipids and fatty acids in stress tolerance in cyanobacteria. Acta Protozool 41:297–308Google Scholar
  84. Smith JJ, Tow LA, Stafford W, Cary C, Cowan DA (2006) Bacterial diversity in three different Antarctic cold desert mineral soils. Microb Ecol 51:413–421Google Scholar
  85. Steponkus PL, Lynch DV (1989) Freeze/thaw-induced destabilization of the plasma membrane and the effects of cold acclimation. J Bioenerg Biomembr 21(1):21–41Google Scholar
  86. Strauss G, Hauser H (1986) Stabilization of lipid bilayer vesicles by sucrose during freezing. Proc Natl Acad Sci USA 83:2422–2426ADSGoogle Scholar
  87. Sudo SZ, Dworkin M (1973) Comparative biology of prokaryotic resting cells. Adv Microb Physiol 9:153–224Google Scholar
  88. Sukenik A, Beardall J, Hadas O (2007) Photosynthetic characterization of developing and mature akinetes of Aphanizomenon ovalisporum(cyanoprokaryota). J Phycol 43:780–788Google Scholar
  89. Sutherland JM, Herdman M, Stewart WDP (1979) Akinetes of the cyanobacterium NostocPCC 7524: macromolecular composition, structure and control of differentiation. J Gen Microbiol 115:273–287Google Scholar
  90. Sutherland JM, Reaston J, Stewart WDP, Herdman M (1985) Akinetes of the cyanobacterium NostocPCC 7524: macromolecular and biochemical changes during synchronous germination. J Gen Microbiol 131:2855–2863Google Scholar
  91. Suzina NE, Mulyukin AL, Kozlova AN, Shorokhova AP, Dmitriev VV, Barinova ES, Mokhova ON, El’-Registan GI, Duda VI (2004) Ultrastructure of resting cells of some non-spore-forming bacteria. Microbiology 73(4):435–447Google Scholar
  92. Tamaru Y, Takani Y, Yoshida T, Sakamoto T (2005) Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium Nostoc commune. Appl Environ Microbiol 71(11):7327–7333Google Scholar
  93. Tang EPY, Tremblay R, Vincent WF (1997) Cyanobacterial dominance of polar freshwater ecosystems: are high-latitude mat-formers adapted to low temperature? J Phycol 33:171–181Google Scholar
  94. Tanghe A, van Dijck P, Thevelein JM (2003) Determinants of freeze tolerance in microorganisms, physiological importance, and biotechnological applications. Adv Appl Microbiol 53:129–176Google Scholar
  95. Thiel T, Wolk CP (1983) Metabolic activities of isolated akinetes of the cyanobacterium Nostoc spongiaeforme. J Bacteriol 156(1):369–374Google Scholar
  96. Thomas DN, Fogg GE, Convey P, Fritsen CH, Gili J-M, Gradinger R, Laybourn-Parry J, Reid K, Walton DWH (2008) The biology of Polar Regions. Oxford University Press, New YorkGoogle Scholar
  97. Thomashow MF (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118:1–7Google Scholar
  98. Turner MA, Arellano F, Kozloff LM (1990) Three separate classes of bacterial ice nucleation structures. J Bacteriol 172(5):2521–2526Google Scholar
  99. Vézina S, Vincent WF (1997) Arctic cyanobacteria and limnological properties of their environment: Bylot Island, Northwest Territories, Canada (73°N, 80°W). Polar Biol 17:523–534Google Scholar
  100. Vincent WF (1988) Microbial ecosystems of Antarctica. Cambridge University Press, Cambridge, 304 ppGoogle Scholar
  101. Vincent WF (2000) Cyanobacterial dominance in the Polar Regions. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria: their diversity in time and space. Kluwer Academic Publishers, Dordrecht, pp 321–340Google Scholar
  102. Vincent WF (2007) Cold tolerance in cyanobacteria and life in the cryosphere. In: Seckbach J (ed) Algae and cyanobacteria in extreme environments. Springer, Dordrecht, pp 289–301Google Scholar
  103. Votyakova TV, Kaprelyants AS, Kell DB (1994) Influence of viable cells on the resuscitation of dormant cells in Micrococcus luteuscultures held in an extended stationary phase: the population effect. Appl Environ Microbiol 60(9):3284–3291Google Scholar
  104. Wharton DA, Ferns DJ (1995) Survival of intracellular freezing by the Antarctic nematode Panagrolaimus davidi. J Exp Biol 198:1381–1387Google Scholar
  105. Wharton DA, Goodall G, Marshall CJ (2003) Freezing survival and cryoprotective dehydration as cold tolerance mechanisms in the Antarctic nematode Panagrolaimus davidi. J Exp Biol 206:215–221Google Scholar
  106. Worland MR, Lukešová A (2001) The application of differential scanning calorimetry and ice nucleation spectrometry to ecophysiological studies of algae. Nova Hedwigia, Beiheft 123:571–583Google Scholar
  107. Yamamoto Y (1972) The fatty acid composition of akinetes, heterocysts and vegetative cells in Anabaena cylindrica. Plant Cell Physiol 13:913–915Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  1. 1.Faculty of ScienceUniversity of South BohemiaČeské BudějoviceCzech Republic
  2. 2.Institute of BotanyAcademy of Science of the Czech RepublicTřeboňCzech Republic

Personalised recommendations