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Effects of temperature and salinity on the production of cell biomass, chlorophyll-a and intra- and extracellular nodularins (NOD) and nodulopeptin 901 produced by Nodularia spumigena KAC 66

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Abstract

Nodularia spumigena is one of the dominant toxic cyanobacteria which produce blooms in the Baltic Sea, a brackish water body, particularly in late summer. Nodularia spp. are known to produce hepatotoxic nodularins (NODs) and other bioactive peptides such as spumigins and nodulopeptins. In a recent study, three new nodulopeptins with a molecular weight of 899, 901 and 917 Da were characterized from N. spumigena KAC66. To gain further insight into the effects of environmental stress on growth and production of bioactive metabolites in N. spumigena KAC66, two parameters were investigated: temperature and salinity. It was found that growth conditions have a considerable effect on biomass and toxin levels of N. spumigena KAC66. Increasing temperature had a profound effect on NOD production with an increase from 22 to 25 °C resulting in a 50% decrease in intracellular NOD levels. At 30 °C, little or no NOD was detected. In contrast, while concentrations of nodulopeptin 901 decreased with increasing temperature, it was still detectable throughout the growth cycle at elevated temperatures. The light intensity of 13 μmol photons m−2 s−1, 22 °C and 11–20‰ salinity were optimal growth conditions to obtain maximum biomass, intra- and extracellular peptide productions. This is the first report to evaluate the effects of selected environmental parameters on NOD/nodulopeptin 901 productions which ultimately may be helpful to explain the distribution, control of natural blooms and toxin levels of N. spumigena in the Baltic Sea, as well as in laboratory based experiments.

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References

  • Allen MM, Stanier RY (1968) Growth and division of some unicellular blue green algae. J Gen Microbiol 51:199–202

    Article  CAS  PubMed  Google Scholar 

  • Blackburn SI, McCausland MA, Bolch CJS, Newman SJ, Jones GJ (1996) Effect of salinity on growth and toxin production in cultures of the bloom-forming cyanobacterium Nodularia spumigena from Australian waters. Phycologia 35:511–522

    Article  Google Scholar 

  • Carmichael WW, Escedor JT, Patterson GM, Moore RE (1988) Toxicity and partial structure of a hepatotoxic peptide produced by the cyanobacterium Nodularia spumigena Mertens emend. L575 from New Zealand. Appl Environ Microbiol 54:2257–2263

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dahlmann J, Rühl A, Hummert C, Liebezeit G, Carlsson P, Granéli E (2001) Different methods for toxin analysis in the cyanobacterium Nodularia spumigena (Cyanophyceae). Toxicon 39:1183–1190

  • Dailidienė I, Davulienė L (2008) Salinity trend and variation in the Baltic Sea near the Lithuanian coast and in the Curonian Lagoon in 1984-2005. J Mar Syst 74:S20–S29

    Article  Google Scholar 

  • Edler L, Fernö S, Lind NG, Lundberg R, Nilsson PO (1985) Mortality of dogs associated with a bloom of the cyanobacterium Nodularia spumigena in the Baltic Sea. Ophelia 24:103–109

    Article  Google Scholar 

  • Falconer IR (2001) Toxic cyanobacterial bloom problems in Australian waters: risks and impacts on human health. Phycologia 40:228–233

    Article  Google Scholar 

  • Fujii K, Sivonen K, Adachi K, Noguchi K, Sano H, Hirayama K, Suzuki M, Harada K-I (1997) Comparative study of toxic and non-toxic cyanobacterial products: novel peptides from toxic Nodularia spumigena AV1. Tetrahedron Lett 38:5525–5528

    Article  CAS  Google Scholar 

  • Gasiunaite ZR, Cardoso AC, Heiskanen A-S, Henriksen P, Kauppila P, Olenina I, Pilkaityt R, Purina I, Razinkovas A, Sagert S, Schubert H, Wasmund N (2005) Seasonality of coastal phytoplankton in the Baltic Sea: influence of salinity and eutrophication. Estuar Coast Shelf Sci 65:239–252

    Article  Google Scholar 

  • Graham DJL (2007) An investigation into factors influencing the production and degradation of microcystins. Dissertation, The Robert Gordon University, Aberdeen, pp 204

  • Gupta N, Bhaskar ASB, Lakshmana RPV (2002) Growth characteristics and toxin production in batch cultures of Anabaena flos-aquae: effects of culture media and duration. World J Microbiol Biotechnol 18:29–35

    Article  CAS  Google Scholar 

  • HELCOM (2007) Climate change in the Baltic Sea area–HELCOM thematic assessment in 2007. Balt Sea Environ Proc No 111(p):48

    Google Scholar 

  • Hobson P, Fallowfield H (2001) Effect of salinity on photosynthetic activity of Nodularia spumigena. J Appl Phycol 13:493–499

    Article  Google Scholar 

  • Hobson P, Fallowfield HJ (2003) Effect of irradiance temperature and salinity on growth and toxin production by Nodularia spumigena. Hydrobiologia 493:7–15

    Article  CAS  Google Scholar 

  • Hobson P, Burch M, Fallowfield HJ (1999) Effect of salinity on photosynthetic activity of Nodularia spumigena. J Appl Phycol 13:493–499

    Article  Google Scholar 

  • Horstmann U (1975) Eutrophication and mass occurrence of blue-green algae in the Baltic. Merentutkimuslaitoksen Julk Havsforskningsinst Skr 239:83–90

  • Ibelings BW, Chorus I (2007) Accumulation of cyanobacterial toxins in freshwater “seafood” and its consequences for public health: a review. Environ Pollut 150:177–192

    Article  CAS  PubMed  Google Scholar 

  • Kankaanpää H, Vuorinen PJ, Sipiä V, Keinänen M (2002) Acute effects and bioaccumulation of nodularin in sea trout (Salmo trutta m. trutta L) exposed orally to Nodularia spumigena under laboratory conditions. Aquat Toxicol 61:155–168

  • Karlsson K, Sipiä V, Kankaanpää H, Meriluto J (2003) Mass spectrometric detection of nodularin and desmethylnodularin in mussels and flounders. J Chromatogr B 784:243–253

  • Kawachi M, Noёl MH (2005) Sterilization and sterile technique. In: Andersen RA (ed) Algal culturing techniques. Elsevier Academic Press, Oxford, p 565

    Google Scholar 

  • Lawton AL (1999) Determination of cyanobacteria in the laboratory. In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water: a guide toxic cyanobacteria in water: a guide to their public health consequences monitoring and management. E & FN Spon, London, pp 347–366

    Google Scholar 

  • Lehtimäki J, Sivonen K, Luukkainen R, Niemela SI (1994) The effects of incubation time temperature light salinity and phosphorus on growth and hepatotoxin production by Nodularia strains. Arch Hydrobiol 13:269–282

    Google Scholar 

  • Lehtimäki J, Moisander P, Sivonen K, Kononen K (1997) Growth nitrogen fixation and nodularin production by two Baltic Sea cyanobacteria. Appl Environ Microbiol 63:1647–1656

    PubMed  PubMed Central  Google Scholar 

  • Lilover MJ, Stips A (2008) The variability of parameters controlling the cyanobacteria bloom biomass in the Baltic Sea. J Mar Syst 74:S108–S115

    Article  Google Scholar 

  • Mazur-Marzec H, Żeglińska L, Pliński M (2005) The effect of salinity on the growth toxin production and morphology of Nodularia spumigena isolated from the Gulf of Gdańsk southern Baltic Sea. J Appl Phycol 17:171–179

    Article  CAS  Google Scholar 

  • Mazur-Marzec H, Kaczkowska MJ, Blaszczyk A, Akcaalan R, Spoof L, Meriluoto J (2013) Diversity of peptides produced by Nodularia spumigena from various geographical regions. Mar Drugs 11:1–19

    Article  CAS  Google Scholar 

  • Moisander PH, McClinton E, Paerl H (2002) Salinity effects on growth photosynthetic parameters and nitrogenase activity in estuarine planktonic cyanobacteria. Microb Ecol 43:432–442

    Article  CAS  PubMed  Google Scholar 

  • Murphy RJ, Underwood AJ, Pinkerton MH, Range P (2005) Field spectrometry: new methods to investigate epilithic micro-algae on rocky shores. J Exp Mar Biol Ecol 325:111–124

    Article  Google Scholar 

  • Murphy RJ, Tolhurst TJ, Chapman MG, Underwood AJ (2009) Seasonal distribution of chlorophyll on mudflats in New South Wales Australia measured by field spectrometry and PAM fluorometry. Estuar Coast Shelf Sci 84:108–118

    Article  CAS  Google Scholar 

  • MURSYS (2003) North Sea and Baltic Sea-report 2. (http://www.bsh.de/en/Marine_data/Observations/MURSYS_reporting_system/mursys1203.jsp)

  • MURSYS 2005- North Sea and Baltic Sea-report 2. (http://www.bsh.de/Vorlagen/ressources/Druckversion.jsp?_PRINTPAGE_=yes&_PRINTOID_=51997&)

  • MURSYS 2006- North Sea and Baltic Sea-report 2. (http://www.bsh.de/en/Marine_data/Observations/MURSYS_reporting_system/mursys0207.jsp)

  • Musial A, Plinski M (2003) Influence of salinity on the growth of Nodularia spumigena Mertens. Oceanol Hydrobiol St 2:45–52

    Google Scholar 

  • Persson P-E, Sivonen K, Keto J, Kononen K, Niemi M, Viljamaa H (1984) Potentially toxic blue-green algae (cyanobacteria) in Finnish natural waters. Aqua Fennica 14:147–154

    Google Scholar 

  • Report of Estonia on the implementation of nitrate directive 2000-2003. Tallinn (2005). pp 21

  • Rinehart KL, Harada K, Namikoshi M, Chen C, Harvis CA, Munro MHG, Blunt JW, Mulligan PE, Beasley VR, Dahlem AM, Carmichael WW (1988) Nodularin, microcystin, and the configuration of ADDA. J Am Chem Soc 110:8557–8558

    Article  CAS  Google Scholar 

  • Schumacher M, Wilson N, Tabudravu J, Edwards C, Lawton L, Mottid C, Wright T, Diederich M, Jaspars M (2012) Novel polypeptides from Nodularia spumigena KAC66. Tetrahedron 68:1622–1628

    Article  CAS  Google Scholar 

  • Sivonen K (1990) Effects of light temperature nitrate orthophosphate and bacteria on the growth of the hepatotoxin by Oscillatoria agardhii strains. Appl Environ Microbiol 56:2658–2666

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sivonen K (1996) Cyanobacterial toxins and toxin production. Phycologia 35:12–24

    Article  Google Scholar 

  • Sivonen K, Jones G (1999) Cyanobacterial toxins. In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water a guide to their public health consequences monitoring and management. E & FN Spon, London, pp 41–111

  • Sivonen K, Kononen K, Carmichael WW, Dahlem AM, Rinehart KL, Kiviranta J, Niemelä SI (1989a) Occurrence of the hepatotoxic cyanobacterium Nodularia spumigena in the Baltic Sea and the structure of the toxin. Appl Environ Microbiol 55:1990–1995

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sivonen K, Kononen K, Esala AE, Niemelä SI (1989b) Toxicity and isolation of the cyanobacterium Nodularia spumigena from the Southern Baltic Sea. Hydrobiologia 185:3–8

    Article  CAS  Google Scholar 

  • Stal LJ, Staal M, Villbrandt M (1999) Nutrient control of cyanobacteria blooms in the Baltic Sea. Aquat Microb Ecol 18:165–173

    Article  Google Scholar 

  • Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular bluegreen algae (order Chroococcales). Bacteriol Rev 35:171205

    Google Scholar 

  • Stolte W, Karlsson C, Carlsson P, Graneli E (2002) Modelling the increase of nodularin content in Baltic Sea Nodularia spumigena during stationary phase in phosphorus-limited batch cultures. FEMS Microb Ecol 41:211–220

    Article  CAS  Google Scholar 

  • Suikkanen S, Kaartokallio H, Hällfors S, Huttunen M, Laamanen M (2010) Life cycle strategies of bloom-forming filamentous cyanobacteria in the Baltic Sea. Deep Sea Res II 57:199–209

    Article  CAS  Google Scholar 

  • Van der Westhuizen AJ, Eloff JN (1985) Effect of temperature and light on the toxicity and growth of the blue-green alga Microcystis aeruginosa (UV-006). Planta 163:55–59

    Article  CAS  PubMed  Google Scholar 

  • Van der Westhuizen AJ, Eloff JN, Krüger GH (1986) Effect of temperature and light (fluence rate) on the composition of the toxin of the cyanobacterium Microcystis aeruginosa (UV-006). Arch Hydrobiol 108:145–154

    CAS  Google Scholar 

  • Vezie C, Rapala J, Vaitomaa J, Seitsonen J, Sivonen K (2002) Effect of nitrogen and phosphorus on growth of toxic and nontoxic Microcystis strains and on intracellular microcystin concentrations. Microb Ecol 4:443–454

    Article  Google Scholar 

  • Wasmund N (1997) Occurrence of cyanobacterial blooms in the Baltic Sea in relation to environmental conditions. Intern Revue Hydrobiol Hydrogr 82:169–184

    Article  Google Scholar 

  • Watanabe MF, Oishi S (1985) Effects of environmental factors on toxicity of a cyanobacterium (Microcystis aeruginosa) under culture conditions. Appl Environ Microbiol 49:1342–1344

    CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Shaista Hameed, Linda A. Lawton or Ajmal Khan.

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Hameed, S., Lawton, L.A., Edwards, C. et al. Effects of temperature and salinity on the production of cell biomass, chlorophyll-a and intra- and extracellular nodularins (NOD) and nodulopeptin 901 produced by Nodularia spumigena KAC 66. J Appl Phycol 29, 1801–1810 (2017). https://doi.org/10.1007/s10811-017-1115-5

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  • DOI: https://doi.org/10.1007/s10811-017-1115-5

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