Microbial Ecology

, Volume 57, Issue 4, pp 675–686 | Cite as

Interaction Effects of Ambient UV Radiation and Nutrient Limitation on the Toxic Cyanobacterium Nodularia spumigena

  • Malin Mohlin
  • Angela Wulff
Original Article


Nodularia spumigena is one of the dominating species during the extensive cyanobacterial blooms in the Baltic Sea. The blooms coincide with strong light, stable stratification, low ratios of dissolved inorganic nitrogen, and dissolved inorganic phosphorus. The ability of nitrogen fixation, a high tolerance to phosphorus starvation, and different photo-protective strategies (production of mycosporine-like amino acids, MAAs) may give N. spumigena a competitive advantage over other phytoplankton during the blooms. To elucidate the interactive effects of ambient UV radiation and nutrient limitation on the performance of N. spumigena, an outdoor experiment was designed. Two radiation treatments photosynthetic active radiation (PAR) and PAR +UV-A + UV-B (PAB) and three nutrient treatments were established: nutrient replete (NP), nitrogen limited (−N), and phosphorus limited (−P). Variables measured were specific growth rate, heterocyst frequency, cell volume, cell concentrations of MAAs, photosynthetic pigments, particulate carbon (POC), particulate nitrogen (PON), and particulate phosphorus (POP). Ratios of particulate organic matter were calculated: POC/PON, POC/POP, and PON/POP. There was no interactive effect between radiation and nutrient limitation on the specific growth rate of N. spumigena, but there was an overall effect of phosphorus limitation on the variables measured. Interaction effects were observed for some variables; cell size (larger cells in −P PAB compared to other treatments) and the carotenoid canthaxanthin (highest concentration in −N PAR). In addition, significantly less POC and PON (mol cell−1) were found in −P PAR compared to −P PAB, and the opposite radiation effect was observed in −N. Our study shows that despite interactive effects on some of the variables studied, N. spumigena tolerate high ambient UVR also under nutrient limiting conditions and maintain positive growth rate even under severe phosphorus limitation.


Specific Growth Rate Photosynthetic Active Radiation Nutrient Limitation Dissolve Inorganic Phosphorus Phosphorus Limitation 
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.



We thank V. Lindberg, H. Olofsdotter-Mossfeldt, and M. Appelgren for assistance with experimental work, and Dr P. Moksnes and Prof. P. Jonsson for advice on the statistical analyses. We are grateful to Prof. P. Jonsson for valuable comments on the manuscript. STRÅNG data used here are from the Swedish Meteorological and Hydrological Institute and were produced with support from the Swedish Radiation Protection Authority and the Swedish Environmental Agency. Financial support was provided by The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning; The Oscar and Lilli Lamm Foundation; The Carl Trygger Foundation; The Magnus Bergvall Foundation; The Lars Hierta Foundation; and The Research Fund of Martina Lundgren.


  1. 1.
    Aldhous P (2000) Global warming could be bad news for Arctic ozone layer. Nature 404:531–531PubMedCrossRefGoogle Scholar
  2. 2.
    Bianchi TS, Engelhaupt E, Westman P, Andren T, Rolff C, Elmgren R (2000) Cyanobacterial blooms in the Baltic Sea: natural or human-induced? Limnol Oceanogr 45:716–726Google Scholar
  3. 3.
    Carreto JI, Carignan MO, Montoya NG (2005) A high-resolution reverse-phase liquid chromatography method for the analysis of mycosporine-like amino acids (MAAs) in marine organisms. Mar Biol 146:237–252CrossRefGoogle Scholar
  4. 4.
    Degerholm J, Gundersen K, Bergman B, Soderback E (2006) Phosphorus-limited growth dynamics in two Baltic Sea cyanobacteria, Nodularia sp. and Aphanizomenon sp. FEMS Microbiol Ecol 58:323–332PubMedCrossRefGoogle Scholar
  5. 5.
    Dunlap WC, Yamamoto Y (1995) Small-molecule antioxidants in marine organisms: antioxidant activity of mycosporine–glycine. Comp Biochem Physiol 112:105–114CrossRefGoogle Scholar
  6. 6.
    Falkowski PG, Laroche J (1991) Acclimation to spectral irradiance in algae. J Phycol 27:8–14CrossRefGoogle Scholar
  7. 7.
    Finni T, Kononen K, Olsonen R, Wallstrom K (2001) The history of cyanobacterial blooms in the Baltic Sea. Ambio 30:172–178PubMedGoogle Scholar
  8. 8.
    Garcia-Pichel F, Castenholz RW (1993) Occurrence of UV-absorbing, mycosporine-like compounds among cyanobacterial isolates and an estimate of their screening capacity. Appl Environ Microbiol 59:163–169PubMedGoogle Scholar
  9. 9.
    Graneli E, Wallstrom K, Larsson U, Graneli W, Elmgren R (1990) Nutrient limitation of primary production in the Baltic Sea area. Ambio 19:142–151Google Scholar
  10. 10.
    Graneli E, Codd B, Dale B, Lipiautou E, Maestrini SY, Rosenthal H (eds) (1999) Harmful algal blooms in European marine and brackish waters. EC Commission Publication, Research in Enclosed Seas Series-5, EUR 18592, p 93Google Scholar
  11. 11.
    Grasshoff K, Kremling K, Ehrhardt M (1999) Methods of seawater analysis, 3rd edn. Wiley-VCH, WeinheimGoogle Scholar
  12. 12.
    Grönlund L, Kononen K, Lahdes E, Makela K (1996) Community development and modes of phosphorus utilization in a late summer ecosystem in the central Gulf of Finland, the Baltic Sea. Hydrobiologia 331:97–108CrossRefGoogle Scholar
  13. 13.
    Goldman JC, McCarthy JJ, Peavy DG (1979) Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature 279:210–215CrossRefGoogle Scholar
  14. 14.
    Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. New York, Plenum, pp 29–60Google Scholar
  15. 15.
    Healey FP (1973) Characteristics of phosphorus deficiency in Anabaena. J Phycol 9:383–394Google Scholar
  16. 16.
    Healey FP (1975) Physiological indicators of nutrient deficiency in algae. Fish Mar Serv Tech Rep 585:30Google Scholar
  17. 17.
    Hessen DO, Faerovig PJ, Andersen T (2002) Light, nutrients, and P:C ratios in algae: grazer performance related to food quality and quantity. Ecology 83:1886–1898CrossRefGoogle Scholar
  18. 18.
    Jezberova J, Komarkova J (2007) Morphometry and growth of three Synechococcus-like picoplanktonic cyanobacteria at different culture conditions. Hydrobiologia 578:17–27CrossRefGoogle Scholar
  19. 19.
    Karentz D (1994) Ultraviolet tolerance mechanisms in Antarctic marine organisms. Antarct Res Ser 62:93–110Google Scholar
  20. 20.
    Karentz D (2001) Chemical defenses of marine organisms against solar radiation exposure: UV-absorbing mycosporine-like amino acids and scytonemin. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, FL, pp 481–520Google Scholar
  21. 21.
    Karentz DK, Cleaver JE, Mitchell DL (1991) Cell survival characteristics and molecular responses of Antarctic phytoplankton to ultraviolet-B radiation. J Phycol 27:326–341CrossRefGoogle Scholar
  22. 22.
    Larsson U, Hajdu S, Walve J, Elmgren R (2001) Baltic Sea nitrogen fixation estimated from the summer increase in upper mixed layer total nitrogen. Limnol Oceanogr 46:811–820Google Scholar
  23. 23.
    Latasa M, Berdalet E (1994) Effect of nitrogen or phosphorus starvation on pigment composition of cultured Heterocapsa sp. J Plankton Res 16:83–94CrossRefGoogle Scholar
  24. 24.
    Layzell DB, Turpin DH, Elrifi IR (1985) Effect of N source on the steady state growth and N assimilation of P-limited Anabaena flos-aquae. Plant Physiol 78:739–745PubMedCrossRefGoogle Scholar
  25. 25.
    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 130:269–282Google Scholar
  26. 26.
    Lehtimäki J, Moisander P, Sivonen K, Kononen K (1997) Growth, nitrogen fixation, and nodularin production by two Baltic Sea cyanobacteria. Appl Environ Microbiol 63:1647–1656PubMedGoogle Scholar
  27. 27.
    Neale PJ, Davis RF, Cullen JJ (1998) Interactive effects of ozone depletion and vertical mixing on photosynthesis of Antarctic phytoplankton. Nature 392:585–589CrossRefGoogle Scholar
  28. 28.
    Nehring S (1993) Mortality of dogs associated with a mass development of Nodularia spumigena (Cyanophyceae) in a brackish lake at the German North Sea coast. J Plankton Res 15:867–872CrossRefGoogle Scholar
  29. 29.
    Niemi Å (1979) Blue-green algal blooms and N:P ratio in the Baltic Sea. Acta Bot Fenn 11:57–61Google Scholar
  30. 30.
    Oliver RL, Ganf GG (2000) Freshwater blooms. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Their diversity in time and space. Kluwer, Dordrecht, pp 149–194Google Scholar
  31. 31.
    Paasche E, Erga SR (1988) Phosphorus and nitrogen limitation of phytoplankton in the inner Oslofjord (Norway). Sarsia 73:229–243Google Scholar
  32. 32.
    Paerl HW (1988) Nuisance phytoplankton blooms in coastal, estuarine, and inland waters. Limnol Oceanogr 33:823–847Google Scholar
  33. 33.
    Paerl HW (2000) Marine plankton. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Their diversity in time and space. Kluwer, Dordrecht, pp 121–148Google Scholar
  34. 34.
    Panosso R, Graneli E (2000) Effects of dissolved organic matter on the growth of Nodularia spumigena (Cyanophyceae) cultivated under N or P deficiency. Mar Biol 136:331–336CrossRefGoogle Scholar
  35. 35.
    Portwich A, Garcia-Pichel F (1999) Ultraviolet and osmotic stresses induce and regulate the synthesis of mycosporines in the cyanobacterium Chlorogloeopsis PCC6912. Arch Microbiol 172:187–192PubMedCrossRefGoogle Scholar
  36. 36.
    Portwich A, Garcia-Pichel F (2000) A novel prokaryotic UVB photoreceptor in the cyanobacterium Chlorogloeopsis PCC 6912. J Photochem Photobiol B 71:493–498CrossRefGoogle Scholar
  37. 37.
    Rapala J, Sivonen K, Lyra C, Niemela SI (1997) Variation of microcystins, cyanobacterial hepatotoxins, in Anabaena spp. as a function of growth stimuli. Appl Environ Microbiol 63:2206–2212PubMedGoogle Scholar
  38. 38.
    Rosen BH Lowe RC (1984) Physiological and ultrastructural responses of Cyclotella meneghiniania (Bacillariophyta) to light intensity and nutrient limitation. J Phycol 20:173–180CrossRefGoogle Scholar
  39. 39.
    Rydin E, Hyenstrand P, Gunnerhed M, Blomqvist P (2002) Nutrient limitation of cyanobacterial blooms: an enclosure experiment from the coastal zone of the NW Baltic proper. Mar Ecol Prog Ser 239:31–36CrossRefGoogle Scholar
  40. 40.
    Sakshaug E, Andresen K, Myklestad S, Olsen Y (1983) Nutrient status of phytoplankton communities in Norwegian waters (marine, brackish, fresh) as revealed by their chemical composition. J Plankton Res 5:175–196CrossRefGoogle Scholar
  41. 41.
    Shick JM, Dunlap WC (2002) Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu Rev Physiol 64:223–262PubMedCrossRefGoogle Scholar
  42. 42.
    Shindell DT, Schmidt GA, Miller RL, Rind D (2001) Northern Hemisphere winter climate response to greenhouse gas, ozone, solar, and volcanic forcing. J Geophys Res D 106:7193–7210CrossRefGoogle Scholar
  43. 43.
    Sinha RP, Ambasht NK, Sinha JP, Klisch M, Häder DP (2003) UV-B-induced synthesis of mycosporine-like amino acids in three strains of Nodularia (cyanobacteria). J Photochem Photobiol B 71:51–58PubMedCrossRefGoogle Scholar
  44. 44.
    Sinha RP, Häder DP (2008) UV-protectants in cyanobacteria. Plant Sci 174:278–289Google Scholar
  45. 45.
    Sivonen K, Halinen K, Sihvonen LM, Koskenniemi K, Sinkko H, Rantasarkka K, Moisander PH, Lyra C (2007) Bacterial diversity and function in the Baltic Sea with an emphasis on cyanobacteria. Ambio 36:180–185PubMedCrossRefGoogle Scholar
  46. 46.
    Staehr PA, Henriksen P, Markager S (2002) Photoacclimation of four marine phytoplankton species to irradiance and nutrient availability. Mar Ecol Prog Ser 238:47–59CrossRefGoogle Scholar
  47. 47.
    Stal LJ, Staal M, Villbrandt M (1999) Nutrient control of cyanobacterial blooms in the Baltic Sea. Aquat Microb Ecol 18:165–173CrossRefGoogle Scholar
  48. 48.
    Summons RE, Jahnke LL, Hope JM, Logan GA (1999) 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400:554–557PubMedCrossRefGoogle Scholar
  49. 49.
    Turpin DH (1991) Effects of inorganic N availability on algal photosynthesis and carbon metabolism. J Phycol 27:14–20CrossRefGoogle Scholar
  50. 50.
    Underwood AJ (1997) Experiments in ecology. Cambridge, Cambridge University PressGoogle Scholar
  51. 51.
    Walve J, Larsson U (2007) Blooms of Baltic Sea Aphanizomenon sp. (Cyanobacteria) collapse after internal phosphorus depletion. Aquat Microb Ecol 49:57–69CrossRefGoogle Scholar
  52. 52.
    Vahtera E, Laamanen M, Rintala JM (2007) Use of different phosphorus sources by the bloom-forming cyanobacteria Aphanizomenon flos-aquae and Nodularia spumigena. Aquat Microb Ecol 46:225–237CrossRefGoogle Scholar
  53. 53.
    Villafañe VE, Sundbäck K, Figueroa FL, Helbling WE (2003) Photosynthesis in the aquatic environment as affected by ultraviolet radiation. In: Helbling WE, Zagarese H (eds) UV effects in aquatic organisms and ecosystems. Comprehensive Series in Photosciences. Royal Societyof Chemistry, Cambridge, UK, pp 357–398CrossRefGoogle Scholar
  54. 54.
    Wright S, Jeffrey S (1997) High-resolution HPLC system for chlorophylls and carotenoids of marine phytoplankton. In: Jeffrey S, Mantoura R, Wright S (eds) Phytoplankton pigments in oceanography. Paris, UNESCO, pp 327–341Google Scholar
  55. 55.
    Wright SW, Jeffrey SW, Mantoura RFC (1997) Evaluation of methods and solvents for pigment extraction. In: Jeffrey SW, Mantoura RFC, Wright SW (eds) Phytoplankton pigments in oceanography. Paris, UNESCO, pp 261–282Google Scholar
  56. 56.
    Wulff A, Wangberg SA, Sundback K, Nilsson C, Underwood GJC (2000) Effects of UVB radiation on a marine microphytobenthic community growing on a sand-substratum under different nutrient conditions. Limnol Oceanogr 45:1144–1152Google Scholar
  57. 57.
    Wulff A, Mohlin M, Sundback K (2007) Intraspecific variation in the response of the cyanobacterium Nodularia spumigena to moderate UV-B radiation. Harmful Algae 6:388–399CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Department of Marine Ecology, Marine BotanyUniversity of GothenburgGöteborgSweden

Personalised recommendations