Skip to main content
Log in

Variation of Microcystis and microcystins coupling nitrogen and phosphorus nutrients in Lake Erhai, a drinking-water source in Southwest Plateau, China

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Lake Erhai is the second largest lake of Southwest China and an important drinking water source. The lake is currently defined as the preliminary stage of eutrophic states, but facing a serious threat with transfer into intensive eutrophication. The present study examined the dynamics of Microcystis blooms and toxic Microcystis in Lake Erhai during 2010, based on quantitative real-time PCR method using 16S rRNA gene specific for Microcystis and microcystin systhesis gene (mcy), and chemical analysis on microcystin (MC) concentrations. Total Microcystis cell abundance at 16 sampling sites were shown as an average of 1.7 × 107 cells l−1 (1.3 × 102–3.8 × 109 cells l−1). Microcystin LR (MC-LR) and microcystin RR (MC-RR) were the main variants. The strong southwesterly winds, anticlockwise circular flows and geographical characteristics of lake and phytoplankton community succession impacted the distribution patterns of Chl a and MC in the lake. The concentration of Chl a and MC and abundances of total Microsytis and MC-producing Microsystis (MCM) were shown to be positively correlated with pH, DO and TP, negatively correlated with SD, NO3-N, TN/Chl a and TN/TP, and not correlated with NH4-N, TN, dissolved total nitrogen (DTN) and water temperatures. When TN/TP decrease, Microcystis tended to dominate and MC concentrations tended to increase, suggesting that the “TN/TP rule” can be partially applied to explain the correlation between the cyanobacterial blooms and nutrients N and P only within a certain nutrient level. It is speculated that N and P nutrients and the associated genes (e.g., mcy) may jointly drive MC concentration and toxigenicity of Microcystis in Lake Erhai.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bourke ATC, Hawes RB, Neilson A, Stallman ND (1983) An outbreak of hepato-enteritis (the Palm Island mystery disease) possibly caused by algal intoxication. Toxicon Suppl 3:45–48

    Article  Google Scholar 

  • Carmichael WW (2001) Health effects of toxin-producing cyanobacteria: “the CyanoHABs”. Hum Ecol Risk Assess 7(5):1393–1407

    Article  Google Scholar 

  • Chorus I, Niesel V, Fastner J, Wiedner C, Nixdorf B, Lindenschmidt KE (2001) Environmental factors of MClevels in waterbodies. In: Chorus I (ed) Cyanotoxins: occurrence, causes, consequences. Springer, Berlin, pp 159–177

    Chapter  Google Scholar 

  • Dong YX (2003) The relationship between distribution of algae and eutrophication of Erhai Lake. In: Bai JK, Sang YM, Kui LX (eds) Dali Erhai Lake scientific research. Ethnic Publishing House, Beijing, pp 398–401 (in Chinese)

    Google Scholar 

  • Du BH (1992) Study on eutrophication of Erhai Lake. J Lake Sci 4(2):86–92 (in Chinese)

    Google Scholar 

  • Falconer IR, Beresford AM, Runnegar MT (1983) Evidence of liver damage by toxin from a bloom of the blue-green alga, Microcystis aeruginosa. Med J Aust 1:511–514

    CAS  Google Scholar 

  • Forsberg C, Ryding SO (1980) Eutrophication parameters and trophic state indices in 30 Swedish wastereceiving lakes. Arch Hydrobiol 89:189–207

  • Ginn HP, Pearson LA, Neilan BA (2010) NtcA from Microcystis aeruginosa PCC 7806 is autoregulatory and binds to the microcystin promoter. Appl Environ Microbiol 76:4362–4368

    Article  CAS  Google Scholar 

  • Gobler CJ, Davis TW, Coyne KJ, Boyer GL (2007) Interactive influences of nutrient loading, zooplankton grazing, and microcystin synthetase gene expression on cyanobacterial bloom dynamics in a eutrophic New York lake. Harmful Algae 6(1):119–133

    Article  CAS  Google Scholar 

  • Gupta S, Giddings M, Sheffer M (2001) Cyanobacterial toxins in drinking water: a Canadian perspective. In: Chorus I (ed) Cyanotoxins: occurrence, causes, consequences. Springer, Berlin, pp 208–212

    Google Scholar 

  • Hilborn ED, Carmichael WW, Soares RM, Yuan M, Servaites JC, Barton HA, Azevedo SMFO (2007) Serologic evaluation of human microcystin exposure. Environ Toxicol 22(5):459–463

    Article  CAS  Google Scholar 

  • Honkanen RE, Dukelow M, Zwiller J, Moore RE, Khatra BS, Boynton AL (1991) Cyanobacterial nodularin is a potent inhibitor of type 1 and type 2A protein phosphatases. Mol Pharmacol 40:577–583

    CAS  Google Scholar 

  • Hu MM, Li YH, Wang YC, Zhou HD, Liu YD, Zhao GF (2013) Phytoplankton and bacterioplankton abundances and community dynamics in Lake Erhai. Water Sci Technol 68(2):348–356

    Article  CAS  Google Scholar 

  • Jiang Y, Ji B, Wong RNS, Wong MH (2008) Statistical study on the effects of environmental factors on the growth and microcystins production of bloom-forming cyanobacteriums Microcystis aeruginosa. Harmful Algae 7(2):127–136

    Article  CAS  Google Scholar 

  • Jiang YG, Yu GL, Chai WB, Song GF, Li RH (2013) Congruence between mcy based genetic type and microcystin composition within the populations of toxic Microcystis in a plateau lake, China. Environ Microbiol Rep 5(5):637–647

    CAS  Google Scholar 

  • Jochimsen EM, Carmichael WW, An J, Cardo DM, Cookson ST, Holmes CEM, Antunes CMB, Melo FDA, Lyra TM, Barreto VST, Azevedo SMFO, Jarvis WR (1998) Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. New Engl J Med 338(13):873–878

    Article  CAS  Google Scholar 

  • Joo HH, Taira H, Hiroshi T (2009) Quantification of toxic Microcystis and evaluation of its dominance ratio in blooms using real-time PCR. Environ Sci Technol 43(3):812–818

    Article  Google Scholar 

  • Kameyama K, Sugiura N, Isoda H, Maekawa T (2002) Effects of nitrate and phosphate concentration on production of microcystins by Microcystis viridis NIES-102. Aquat Econ Health Manag 5(4):443–449

    Article  CAS  Google Scholar 

  • Kasai F, Kawachi M, Erata M, Mori F, Yumoto K, Sato M, Ishimoto M (2009) NIES-collection, list of strains, 8th edn. Jpn J Phycol Suppl 57(1):216–217

    Google Scholar 

  • Kotak BG, Lam AKY, Prepas EE, Hrudey SE (2000) Role of chemical and physical variables in regulating microcystin-LR concentration in phytoplankton of eutrophic lakes. Can J Fish Aquat Sci 57:1584–1593

    Article  CAS  Google Scholar 

  • Kurmayer R, Kutzenberger T (2003) Application of real-time PCR for quantification of microcystin genotypes in a population of the toxic cyanobacterium Microcystis sp. Appl Environ Microbiol 69:6723–6730

    Article  CAS  Google Scholar 

  • Kurmayer R, Dittmann E, Fastner J, Chorus I (2002) Diversity of Microcystin gene within a population of the toxic cyanobacterium Microcystis spp. in Lake Wannsee (Berlin, Germany). Microb Ecol 43:107–118

    Article  CAS  Google Scholar 

  • Li YH, Wang Z, Hu MM, Chang FY, Liu YD, Li GB, Li DH, Shen YW (2011) Diversity and successional dynamics of picocyanobacterial community in lake Erhai (China) as inferred from 16s r RNA gene sequences. Fresenius Environ Bull 20(9):2284–2294

    CAS  Google Scholar 

  • Lin S, Shen J, Liu Y, Liu Q, Li R (2011) Molecular evaluation on the distribution, diversity and toxicity of Microcystis (Cyanobacteria) species from Lake Ulungur—a mesotrophic and brackish desert lake in Xinjiang, China. Environ Monit Assess 175:139–150

    Article  CAS  Google Scholar 

  • Lv XJ, Zhu J, Meng L (2010) Pilot study on diversity of cyanobacteria bloom in Lake Erhai. Environ Sci Surv 29(3):32–35 (in Chinese)

    Google Scholar 

  • MacKintosh C, Beattie KA, Klumpp S, Cohen P, Codd GA (1990) Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Lett 264(2):187–192

    Article  CAS  Google Scholar 

  • Meissner S, Fastner J, Dittmann E (2013) Microcystin production revisited: conjugate formation makes a major contribution. Environ Microbiol 15(6):1810–1820

    Article  CAS  Google Scholar 

  • Neilan B, Jacobs D, Deldot T, Blackall LL, Hawkins PR, Cox PT, Goodman AE (1997) rRNA sequences and evolutionary relationships among toxic and non-toxic cyanobacteria of the genus Microcystis. Int J Syst Bacteriol 47(3):693–697

    Article  CAS  Google Scholar 

  • Neilan BA, Pearson LA, Muenchhoff J, Moffitt MC, Dittmann E (2012) Environmental conditions that influence toxin biosynthesis in cyanobacteria. Environ Microbiol 15(5):1239–1253

    Article  Google Scholar 

  • Otten TG, Xu H, Qin B, Zhu G, Paerl HW (2012) Spatiotemporal patterns and ecophysiology of toxigenic microcystis blooms in Lake Taihu, China: implications for water quality management. Environ Sci Technol 46(6):3480–3488

    Article  CAS  Google Scholar 

  • Paerl HW, Fulton RS, Moisander PH, Dyble J (2001) Harmful freshwater algal blooms, with an emphasis on cyanobacterial. Sci World J 1:76–113

    Article  CAS  Google Scholar 

  • Runnegar MT, Kong S, Berndt N (1993) Protein phosphatase inhibition and in vivo hepatotoxicity of microcystins. Am J Physiol 265:G224–G230

    CAS  Google Scholar 

  • Scott JT, McCarthy MJ, Otten TG, Steffen MM, Baker BC, Grantz EM, Wilhelm SW, Paerl HW (2013) Comment: an alternative interpretation of the relationship between TN:TP and microcystins in Canadian lakes. Can J Fish Aquat Sci 70(8):1265–1268

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Sivonen K (1996) Cyanobacterial toxins and toxin production. Phycologia Suppl 35(6):12–24

    Article  Google Scholar 

  • Smith VH (1983) Low nitrogen to phosphorus ratios favour dominance by blue-green algae in lake phytoplankton. Science 22:669–671

    Article  Google Scholar 

  • Smith VH, Tilman GD, Nekola JC (1999) Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ Pollut 100:179–196

    Article  CAS  Google Scholar 

  • Song LR, Sano T, Li RH, Watanabe MH, Liu YD, Kaya K (1998) Microcystin production of Microcystis viridis (cyanobacteria) under different culture conditions. Phycol Res Suppl 46:19–23

    Article  CAS  Google Scholar 

  • Tillett D, Dittmann E, Erhard M, von Döhren H, Börner T, Neilan BA (2000) Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide–polyketide synthetase system. Chem Biol 7:753–764

    Article  CAS  Google Scholar 

  • Vaitomaa J, Rantala A, Halinen K, Rouhiainen L, Tallberg P, Mokelke L, Sivonen K (2003) Quantitative real-time PCR for determination of microcystin synthetase E copy numbers for Microcystis and Anabaena in lakes. Appl Environ Microbiol 69(12):7289–7297

    Article  CAS  Google Scholar 

  • Via-Ordorika L, Fastner J, Kurmayer R, Hisbergues M, Dittmann E, Komarek J, Erhard M, Chorus I (2004) Distribution of microcystin producing and non-microcystin-producing Microcystis sp. in European freshwater bodies: detection of microcystins and microcystin genes in individual colonies. Syst Appl Microbiol 27:592–602

    Article  CAS  Google Scholar 

  • Wang SM, Dou HS (1998) A directory of lakes in China. Science Press, Beijing (in Chinese)

    Google Scholar 

  • Wang SY, Liu XB, Liu C (2010) Analysis on spatial variation of nitrogen in top layer water of Erhai Lake. Water Resour Prot 26(6):37–41

    CAS  Google Scholar 

  • Wang Z, Wang YC, Hu MM, Li YH, Liu YD, Shen YW, Li GB, Wang GH (2011) Succession of the phytoplankton community in response to environmental factors in north Lake Erhai during 2009–2010. Fresenius Environ Bull 20(9):2221–2231

    CAS  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  Google Scholar 

  • WHO (World Health Organization) (2006) Guidelines for drinking water quality. First adendum to 3rd ed. Recommendations, vol. 1, Geneva, Switzerland, pp 195

  • Wu SK, Xie P, Liang GD, Wang SB, Liang XM (2006) Relationships between microcystins and environmental parameters in 30 subtropical shallow lakes along the Yangtze River, China. Freshw Biol 51:2309–2319

    Article  CAS  Google Scholar 

  • Xie LQ, Xie P, Li SX, Tang HJ, Liu H (2003) The low TN/TP ratio, a cause or a result of Microcystis blooms? Water Res 37:2073–2080

    Article  CAS  Google Scholar 

  • Xu Y, Wang GX, Yang WB, Li RH (2010) Dynamics of the water bloom-forming Microcystis and its relationship with physicochemical factors in Lake Xuanwu (China). Environ Sci Pollut Res 17:1581–1590

    Article  CAS  Google Scholar 

  • Yoshida M, Yoshida T, Yukari T, Hosoda N, Hiroishi S (2007) Dynamics of microcystin-producing and non-microcystin-producing Microcystis populations is correlated with nitrate concentration in a Japanese lake. FEMS Microbiol Lett 266(1):49–53

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Water Science and Technology Projects (2012ZX07105-004, 2008ZX07105-006), also by JSPS RONPAKU (Dissertation PhD) Program. We thank the anonymous reviewers whose comments improved a previous version of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Renhui Li.

Additional information

Responsible editor: Hailong Wang

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, G., Jiang, Y., Song, G. et al. Variation of Microcystis and microcystins coupling nitrogen and phosphorus nutrients in Lake Erhai, a drinking-water source in Southwest Plateau, China. Environ Sci Pollut Res 21, 9887–9898 (2014). https://doi.org/10.1007/s11356-014-2937-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-2937-1

Keywords

Navigation