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Multiple Strategies of Bloom-Forming Microcystis to Minimize Damage by Solar Ultraviolet Radiation in Surface Waters

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Abstract

The occurrence of bloom-forming cyanobacteria is one of the most obvious sign of eutrophication in freshwaters. Although in eutrophic lakes water transparency in the ultraviolet (UV) region is strongly reduced, bloom-forming cyanobacteria are exposed to high solar UV radiation at the surface. Here, we show that, in a natural phytoplankton community from a very eutrophic lake, Microcystis synthesizes UV sunscreen compounds identified as mycosporine-like amino acids (MAAs). The biomass-specific MAA concentration was significantly correlated with the occurrence of Microcystis but not with other algal groups, even though they were dominant in terms of biomass. Based on a photo-optical model, we estimated that the maximum MAA concentration per cell observed (2.5% dry weight) will confer only ~40% of internal screening to a single layer of Microcystis cells. Thus, the formation of a colony with several layers of cells is important to afford an efficient UV screening by internal self-shading. Overall, we propose that Microcystis uses a combination of photoprotective strategies (MAAs, carotenoids) to cope with high solar UV radiation at the water surface. These strategies include also the screening of UV radiation by d-galacturonic acid, one of the main chemical components of the slime layer in Microcystis.

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References

  1. Banaszak AT (2003) Photoprotective physiological and biochemical responses of aquatic organisms. In: Helbling EW, Zagarese H (eds) UV effects in aquatic organisms and ecosystems, Comprehensive Series in Photochemical and Photobiological Sciences. Royal Society of Chemistry, London, pp 329–358

    Google Scholar 

  2. Canini A, Leonardi D, Caiola MG (2001) Superoxide dismutase activity in the cyanobacterium Microcystis aeruginosa after surface bloom formation. New Phytol 152:107–116

    Article  CAS  Google Scholar 

  3. Castenholz RW (1997) Multiple strategies for UV tolerance in cyanobacteria. Spectrum 10:10–16

    Google Scholar 

  4. Chen Y, Qin B, Teubner K, Dokulil MT (2003) Long-term dynamics of phytoplankton assemblages: Microcystis domination in Lake Taihu, a large shallow lake in China. J Plankton Res 25:445–453

    Article  Google Scholar 

  5. Fastner J, Erhard M, von Döhren H (2001) Determination of oligopeptide diversity within a natural population of Microcystis spp. (Cyanobacteria) by typing single colonies by matrix-assisted laser desorption ionization–time of flight mass spectrometry. Appl Environ Microbiol 67:5069–5076

    Article  PubMed  CAS  Google Scholar 

  6. Garcia-Pichel F (1994) A model for internal self-shading in planktonic organisms and its implication for the usefulness of ultraviolet sunscreens. Limnol Oceanogr 39:1704–1717

    Google Scholar 

  7. Garcia-Pichel F (1998) Solar ultraviolet and the evolutionary history of cyanobacteria. Orig Life Evol Biosph 28:321–347

    Article  PubMed  CAS  Google Scholar 

  8. Garcia-Pichel F, Castenholz RW (1993) Occurrence of UV-absorbing mycosporine-like amino compounds among cyanobacterial isolates and an estimate of their screening capacity. Appl Environ Microbiol 59:163–169

    PubMed  CAS  Google Scholar 

  9. Guo L (2007) Doing battle with the green monster of Taihu Lake. Science 317:1166

    Article  PubMed  CAS  Google Scholar 

  10. He YY, Häder DP (2002) UV-B-induced formation of reactive oxygen species and oxidative damage of the cyanobacterium Anabaena sp.: protective effects of ascorbic acid and N-acetyl-l-cysteine. J Phtotochem Photobiol B Biol 66:115–124

    Article  CAS  Google Scholar 

  11. Hu H, Li Y, Wei Y, Zhu H, Chen J, Shi Z (eds) (1980) Freshwater algae in China. Shanghai Science and Technology Press, Shanghai (in Chinese)

  12. Jeffrey SW, MacTavish HS, Dunlap WC, Vesk M, Groenewoud K (1999) Occurrence of UVA- and UVB-absorbing compounds in 152 species (206 strains) of marine microalgae. Mar Ecol Prog Ser 189:35–51

    Article  CAS  Google Scholar 

  13. Jiang H, Qiu B (2005) Photosynthetic adaptation of a bloom-forming cyanobacterium Microcystis aeruginosa to prolonged UV-B exposure. J Phycol 41:983–992

    Article  Google Scholar 

  14. Jöhnk KD, Huisman J, Sharples J, Sommeijer B, Visser PM, Stroom JM (2008) Summer heatwaves promote blooms of harmful cyanobacteria. Glob Chang Biol 14:495–512

    Article  Google Scholar 

  15. Kinzie RA III, Banaszak AT, Lesser MP (1998) Effects of ultraviolet radiation on primary productivity in a high altitude tropical lake. Hydrobiologia 385:23–32

    Article  CAS  Google Scholar 

  16. Klemer AR, Cullen JJ, Mageau MT, Hanson KM, Sundell RA (1996) Cyanobacterial buoyancy regulation: the paradoxical roles of carbon. J Phycol 32:47–53

    Article  CAS  Google Scholar 

  17. Larson RA (1997) Naturally occurring antioxidants. Lewis, Boca Raton

    Google Scholar 

  18. Laurion I, Lami A, Sommaruga R (2002) Distribution of mycosporine-like amino acids and photoprotective carotenoids among freshwater phytoplankton assemblages. Aquat Microb Ecol 26:283–294

    Article  Google Scholar 

  19. Liu Z, Häder DP, Sommaruga R (2004) Occurrence of mycosporine-like amino acids (MAAs) in the bloom-forming cyanobacterium Microcystis aeruginosa. J Plankton Res 26:963–966

    Article  CAS  Google Scholar 

  20. Lorenzen CJ (1967) Determination of chlorophyll and phaeopigments: spectrophotometric equations. Limnol Oceanogr 12:343–346

    Article  CAS  Google Scholar 

  21. Morris DP, Zagarese H, Williamson CE, Balseiro E, Hargreaves BR, Modenutti B, Moeller R, Queimalinos C (1995) The attenuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnol Oceanogr 40:1381–1391

    CAS  Google Scholar 

  22. Neale PJ, Banaszak AT, Jarriel CR (1998) Ultraviolet sunscreens in Gymnodinium sanguineum (Dinophyceae): mycosporine-like amino acids protect against inhibition of photosynthesis. J Phycol 34:928–938

    Article  CAS  Google Scholar 

  23. Oren A, Gunde-Cimerman N (2007) Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiol Lett 269:1–10

    Article  PubMed  CAS  Google Scholar 

  24. Paerl HW, Kellar PE (1979) N2-fixing Anabaena: physiological adaptations instrumental in maintaining surface blooms. Science 204:620–622

    Article  PubMed  CAS  Google Scholar 

  25. Paerl HW, Ustach JF (1982) Blue-green algal scums: an explanation for their occurrence during freshwater blooms. Limnol Oceanogr 27:212–217

    CAS  Google Scholar 

  26. Paerl HW, Tucker J, Bland PT (1983) Carotenoid enhancement and its role in maintaining blue-green algal (Microcystis aeruginosa) surface blooms. Limnol Oceanogr 28:847–857

    CAS  Google Scholar 

  27. Plude JL, Parker DL, Schommer OJ, Timmerman RJ, Hagstrom SA, Joers JM, Hnasko R (1991) Chemical characterization of polysaccharide from the slime layer of the cyanobacterium Microcystis flos-aquae C3–40. Appl Environ Microbiol 57:1696–1700

    PubMed  CAS  Google Scholar 

  28. Reynolds CS (1984) The ecology of freshwater phytoplankton. Cambridge University Press, Cambridge, 384 pp

  29. Reynolds CS, Walsby AE (1975) Water-blooms. Biol Rev Camb Philos Soc 50:473–481

    Google Scholar 

  30. Roy S (2000) Strategies for the minimization of UV-induced damage. In: de Mora S, Demers S, Vernet M (eds) The effects of UV radiation in the marine environment, Cambridge Environmental Chemistry Series no. 10. Cambridge University Press, New York, pp 177–205

    Google Scholar 

  31. Shick JM, Dunlap WC (2002) Mycosporine-like amino acids and related gadusols biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu Rev Physiol 64:223–262

    Article  PubMed  CAS  Google Scholar 

  32. Sinha RP, Häder DP (2008) UV-protectants in cyanobacteria. Plant Sci 174:278–289

    CAS  Google Scholar 

  33. Sinha RP, Klisch M, Groniger A, Häder DP (1998) Ultraviolet-absorbing/screening substances in cyanobacteria, phytoplankton and macroalgae. J Photochem Photobiol B Biol 47:83–94

    Article  CAS  Google Scholar 

  34. Sinha RP, Klisch M, Häder DP (1999) Induction of a mycosporine-like amino acid (MAA) in the rice-field cyanobacterium Anabaena sp. by UV irradiation. J Photochem Photobiol B Biol 52:59–64

    Article  CAS  Google Scholar 

  35. 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: Biol 71:51–58

    Article  CAS  Google Scholar 

  36. Sommaruga R, Garcia-Pichel F (1999) UV-absorbing mycosporine-like compounds in planktonic and benthic organisms from a high-mountain lake. Arch Hydrobiol 144:255–269

    CAS  Google Scholar 

  37. Tartarotti B, Sommaruga R (2002) The effect of different methanol concentrations and temperatures on the extraction of mycosporine-like amino acids (MAAs) in algae and zooplankton. Arch Hydrobiol 154:691–703

    CAS  Google Scholar 

  38. Tartarotti B, Laurion I, Sommaruga R (2001) Large variability in the concentration of mycosporine-like amino acids among zooplankton from lakes located across an altitude gradient. Limnol Oceanogr 46:1546–1552

    CAS  Google Scholar 

  39. Vernet M, Neori A, Haxo FT (1989) Spectral properties and photosynthetic action in red-tide populations of Prorocentrum micans and Gonyaulax polyedra. Mar Biol 103:365–371

    Article  CAS  Google Scholar 

  40. Visser P, Ibelings B, Mur L, Walsby A (2005) The ecophysiology of the harmful cyanobacterium Microcystis. Features explaining its success and measures for its control. In: Huisman J, Matthijs HCP, Visser PM (eds) Harmful cyanobacteria, Aquatic Ecology Series. vol. 3. Springer, Dordrecht, pp 109–142

    Chapter  Google Scholar 

  41. Walsby AE (1991) The mechanical properties of the Microcystis gas vesicle. J Gen Microbiol 137:2401–2408

    Google Scholar 

  42. Zohary T (1985) Hyperscums of the cyanobacterium Microcystis aeruginosa in a hypertrophic lake (Hartbeespoort Dam, South Africa). J Plankton Res 7:399–409

    Article  Google Scholar 

Download references

Acknowledgment

We thank Hans Paerl for useful comments on a previous version. This study was supported by the Austrian Science Foundation (P14153-BIO to R.S.), by the Natural Science Foundation of Jiangsu (project BK2001193), and by the cooperation program between Austria and China (ÖAD, project V.C. 2).

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Authors and Affiliations

  1. Laboratory of Aquatic Photobiology and Plankton Ecology, Institute of Ecology, University of Innsbruck, 6020, Innsbruck, Austria

    Ruben Sommaruga

  2. Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, China

    Yuwei Chen & Zhengwen Liu

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  1. Ruben Sommaruga
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  2. Yuwei Chen
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  3. Zhengwen Liu
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Correspondence to Ruben Sommaruga.

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Sommaruga, R., Chen, Y. & Liu, Z. Multiple Strategies of Bloom-Forming Microcystis to Minimize Damage by Solar Ultraviolet Radiation in Surface Waters. Microb Ecol 57, 667–674 (2009). https://doi.org/10.1007/s00248-008-9425-4

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  • DOI: https://doi.org/10.1007/s00248-008-9425-4

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