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Tolerance of the widespread cyanobacterium Nostoc commune to extreme temperature variations (−269 to 105°C), pH and salt stress

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Abstract

Nostoc commune is a widespread colonial cyanobacterium living on bare soils that alternate between frost and thaw, drought and inundation and very low and high temperatures. We collected N. commune from alternating wet and dry limestone pavements in Sweden and tested its photosynthesis and respiration at 20°C after exposure to variations in temperature (−269 to 105°C), pH (2–10) and NaCl (0.02–50 g NaCl kg−1). We found that dry field samples and rewetted specimens tolerated exposure beyond that experienced in natural environmental conditions: −269 to 70°C, pH 3–10 and 0–20 g NaCl kg−1, with only a modest reduction of respiration, photosynthesis and active carbon uptake at 20°C. 14CO2 uptake from air declined markedly below zero and above 55°C, but remained positive. Specimens maintained a high metabolism with daily exposure to 6 h of rehydration and 18 h of desiccation at −18 and 20°C, but died at 40°C. The field temperature never exceeded the critical 40°C threshold during the wet periods, but it frequently exceeded this temperature during dry periods when N. commune is already dry and unaffected. We conclude that N. commune has an excellent tolerance to low temperatures, long-term desiccation and recurring cycles of desiccation and rewetting. These traits explain why it is the pioneer species in extremely harsh, nutrient-poor and alternating wet and dry environments.

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References

  • Aboal M, Cristobal CJ, Marin-Murcia JP (2010) About the presence of N. commune var flagelliforme (Nostocaceae, Cyanophyceae) on clay soils from arid regions of south east Spain. Acta Bot Malacitana 35:156–161

    Google Scholar 

  • Alpert P (2006) Constraints on tolerance: why are desiccation-tolerant organisms so small or rare? J Exp Biol 9:1575–1584

    Article  Google Scholar 

  • Angeloni SV, Potts M (1986) Polysome turnover in immobilized cells of Nostoc commune (cyanobacteria) exposed to water stress. J Bacteriol 168:1036–1039

    PubMed  CAS  Google Scholar 

  • Büdel B, Bendix J, Bicker FR, Green TGA (2008) Dewfall as a water source frequently activates the endolithic cyanobacterial communities in the granites of Taylor Valley, Antarctica. J Phycol 44:1415–1424

    Article  Google Scholar 

  • Cameron RE (1962) Species of Nostoc voucher occurring in the Sonaran desert in Arizona. Trans Am Microsc Soc 81:379–384

    Article  Google Scholar 

  • Caiola MG, Billi D, Friedmann EI (1996) Effect of desiccation on envelopes of the cyanobacterium Chroococcidiopsis sp (Chroococcales). Eur J Phycol 31:97–105

    Article  Google Scholar 

  • Davey MC (1989) The effect of freezing and desiccation on photosynthesis and survival of terrestrial Antarctic algae and cyanobacteria. Polar Biol 10:29–36

    Article  Google Scholar 

  • Hill DL, 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 9:237–248

    Article  CAS  Google Scholar 

  • Holst J, Butterbach-Bahl K, Liy CY, Cheng XH, Kaiser AJ, Schnitzler JP, Zechmeister-Boltenstern S, Bryggemann N (2009) Dinitrogen fixation by biological soil crusts in Inner Mongolian steppe. Biol Fert Soils 45:679–690

    Article  CAS  Google Scholar 

  • Hu ZH, Xu YN, Gong YD, Kuong TY (2005) Effects of heat treatment on the protein secondary structure and pigment environment in photosystem I complex. Photosynthetica 43:529–534

    Article  CAS  Google Scholar 

  • Huang H, Bai KZ, Zhong ZP, Li LB, Li LB, Kuang TY (2005) Energy transfer from phycobilisomes to photosystems of N. flagelliforme Born. et Filah. During the rewetting course and its physiological significance. J Integr Plant Biol 47:703–708

    Article  Google Scholar 

  • Knowles EJ, Castenholz RW (2008) Effects of exogeneous extracellular polysaccharides on the desiccation and freezing tolerance of rock-inhabiting phototrophic microorganisms. FEMS Microbiol Ecol 66:261–270

    Article  PubMed  CAS  Google Scholar 

  • Li H, Xu J, Liu Y, Ai S, Li Z, Zhang H, Huang Z (2011) Antioxidant and moisture-retention activities of the polysaccharide from Nostoc commune. Carbohyd Polym 83:1821–1827

    Article  CAS  Google Scholar 

  • Mackay MA, Norton RS, Borowitzka LJ (1984) Organic osmoregulatory solutes in cyanobacteria. J Gen Microbiol 130:2177–2191

    CAS  Google Scholar 

  • Marsh J, Nouvet S, Sanborn P, Coxson D (2006) Composition and function of biological crust communities along topographic gradients in grasslands of central interior British Columbia (Chilcotin) and southwestern Yukon (Kluane). Can J Bot 84:713–731

    Article  Google Scholar 

  • Novis PM, Whitebread D, Gregorich EG, Hunt JE, Sparrow AD, Hopkins DW, Elberling B, Greenfield LG (2007) Annual carbon fixation in terrestrial populations of Nostoc commune (Cyanobacteria) from an Antarctic dry valley is driven by temperature regime. Glob Change Biol 13:1224–1237

    Article  Google Scholar 

  • Potts M (1999) Mechanisms of desiccation tolerance in cyanobacteria. Eur J Phycol 34:319–329

    Article  Google Scholar 

  • Price GD, Badger MR, Woodger FJ, Long BM (2008) Advances in understanding the cyanobacterial CO2-concentrating-mechanisms (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59:1441–1461

    Article  PubMed  CAS  Google Scholar 

  • Ramløv H, Westh P (1992) Survival of the cryptobiotic tardigrade Adorybiotus coronifer during cooling to–196 °C; effect of cooling rate, trehalose level, and short-term acclimation. Cryobiol 29:125–130

    Article  Google Scholar 

  • Ramirez M, Hernandez-marine M, Mateo P, Berrendero E, Roldan M (2011) Polyplasic approach and adaptive strategies of Nostoc cf commune (Nostocales, Nostocaceae) growing on Mayan monuments. Fottea 11:73–86

    Google Scholar 

  • Raun AL, Borum J, Sand-Jensen K (2009) Active accumulation of internal DIC pools reduces transport limitation in large colonies of Nostoc pruniforme. Aquat Biol 5:23–29

    Article  Google Scholar 

  • Rebsdorf A (1972) The carbon dioxide system of freshwater. A set of tables for easy computation of total carbon dioxide and other components of the carbon dioxide system. Freshwater Biological Laboratory, University of Copenhagen, Hillerød

    Google Scholar 

  • 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 commune. Phycol Res 57:66–73

    Article  CAS  Google Scholar 

  • Sand-Jensen K, Baastrup-Spohr L, Winkel A, Møller CL, Borum J, Brodersen K, Lindell T, Staehr PA (2010) Plant distribution patterns and adaptation in a limestone quarry on Øland. Sv Bot Tidsskr 104:23–31

    Google Scholar 

  • Sand-Jensen K, Raun AL, Borum J (2009) Metabolism and resources of spherical colonies of Nostoc zetterstedtii. Limnol Oceanogr 54:1282–1291

    Article  CAS  Google Scholar 

  • Satoh K, Hirai M, Nishio J, Yamaji T, Kashino Y, Koike H (2002) Recovery of photosynthetic systems during rewetting is quite rapid in a terrestrial cyanobacterium. Plant Cell Physiol 43:170–176

    Article  PubMed  CAS  Google Scholar 

  • Scherer WS, Ernst A, Chen T-W, Boger P (1984) Rewetting of drought-resistant blue-green algae: Time-course of water uptake and reappearance of respiration, photosynthesis, and nitrogen fixation. Oecologia 62:418–423

    Article  Google Scholar 

  • Ström L, Owen AG, Godbold DL, Jones DC (2005) Organic acid behaviour in a calcareous soil—implications for rhizospehre nutrient cycling. Soil Biol Biochem 37:2046–2054

    Article  Google Scholar 

  • Tamaru Y, Takani Y, Yoshida Y, Sakamoto T (2005) Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium, Nostoc commune. Appl Environ Microbiol 71:7327–7333

    Article  PubMed  CAS  Google Scholar 

  • Taranto PA, Keenan TW, Potts M (1993) Rehydration induces rapid onset of lipid biosynthesis in desiccated Nostoc commune (Cyanobacteria). Biochim Biophys Acta 1168:228–237

    PubMed  CAS  Google Scholar 

  • Vermaat JE, Sand-Jensen K (1987) Survival, metabolism and growth of Ulva lactuca under winter conditions: a laboratory study of bottlenecks in the life cycle. Mar Biol 95:55–61

    Article  CAS  Google Scholar 

  • Yong-Hong B, Zhong-Yang D, Zheng-Yu H, Min X (2005) Response of Nostoc flagelliforme to salt stress. Acta Hydrobiol Sin 29:125–129

    Google Scholar 

  • Yoshida T, Sakamoto T (2009) Water-stress induced trehalose accumulaton and control of trehalase in the cyanbacterium Nostoc punctiforme. J Gen Appl Microbiol 55:135–145

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Ayoe Lüchau for technical assistance, Claus Lindskov Møller for help with statistics and graphs, and Jesper Christensen for analysing field temperatures. The manuscript benefitted from constructive referee comments. This work was supported by grants from the Carlsberg foundation to KSJ and TSJ and from the Lundbeck Foundation to TSJ. We thank Colin Stedmon for improving the English of the text.

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Correspondence to Kaj Sand-Jensen.

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Communicated by Allan Green.

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Sand-Jensen, K., Jespersen, T.S. Tolerance of the widespread cyanobacterium Nostoc commune to extreme temperature variations (−269 to 105°C), pH and salt stress. Oecologia 169, 331–339 (2012). https://doi.org/10.1007/s00442-011-2200-0

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  • DOI: https://doi.org/10.1007/s00442-011-2200-0

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