Skip to main content
SpringerLink
Log in

Occurrence and risk assessment of microcystin and its relationship with environmental factors in lakes of the eastern plain ecoregion, China

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

Abstract

The frequent occurrence of microcystins (MCs) in freshwater poses serious threats to the drinking water safety and health of human beings. Although MCs have been detected in individual fresh waters in China, little is known about their occurrence over a large geographic scale. An investigation of 30 subtropical lakes in eastern China was performed during summer 2018 to determine the MCs concentrations in water and their possible risk via direct water consumption to humans, and to assess the associated environmental factors. MCs were detected in 28 of 30 lakes, and the highest mean MCs concentrations occurred in Lake Chaohu (26.7 μg/L), followed by Lake Taihu (3.11 μg/L). MC-LR was the primary variant observed in our study, and MCs were mainly produced by Microcystis, Anabaena (Dolicospermum), and Oscillatoria in these lakes. Replete nitrogen and phosphorus concentrations, irradiance, and stable water column conditions were critical for dominance of MC-producing cyanobacteria and high MCs production in our study. Hazard quotients indicated that human health risk of MCs in most lakes was at moderate or low levels except Lakes Chaohu and Taihu. Nutrient control management is recommended to decrease the likelihood of high MCs production. Finally, we recommend the regional scale thresholds of total nitrogen and total phosphorus concentrations of 1.19 mg/L and 7.14 × 10−2 mg/L, respectively, based on the drinking water guideline of MC-LR (1 μg/L) recommended by World Health Organization. These targets for nutrient control will aid water quality managers to reduce human health risks created by exposure to MCs.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • APHA (2012) Standard methods for examination of water and wastewater 22ed. Washington, American Public Health Association

  • Beaver JR, Tausz CE, Scotese KC, Pollard AI, Mitchell RM (2018) Environmental factors influencing the quantitative distribution of microcystin and common potentially toxigenic cyanobacteria in U.S. lakes and reservoirs. Harmful Algae 78:118–128

    CAS  Google Scholar 

  • Butterwick C, Heaney SI, Talling JF (2005) Diversity in the influence of temperature on the growth rates of freshwater algae, and its ecological relevance. Freshw Biol 50(2):291–300

    Google Scholar 

  • Cade BS, Noon BR (2003) A gentle introduction to quantile regression for ecologists. Front Ecol Environ 1(8):412–420

    Google Scholar 

  • Chorus I, Bartram J (1999) Toxic cyanobacteria in water-a guide to their public health consequences, monitoring and management. Spon Press, London

    Google Scholar 

  • Chorus I (2001) Cyanotoxins: occurrence, causes, consequences. Springer, Berlin

    Google Scholar 

  • Deng J, Qin B, Sarvala J, Salmaso N, Zhu G, Ventelä AM, Zhang Y, Gao G, Nurminen L, Kirkkala T, Tarvainen M, Vuorio K (2016) Phytoplankton assemblages respond differently to climate warming and eutrophication: a case study from Pyhäjärvi and Taihu. J Great Lakes Res 42:386–396

    CAS  Google Scholar 

  • Derbalah A, Chidya R, Jadoon W, Sakugawa H (2019) Temporal trends in organophosphorus pesticides use and concentrations in river water in Japan, and risk assessment. J Environ Sci-China 79:135–152

    Google Scholar 

  • Dittmann E, Wiegand C (2006) Cyanobacterial toxins–occurrence, biosynthesis and impact on human affairs. Mol Nutr Food Res 50:7–17

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Frank CAP (2002) Microcystin-producing cyanobacteria in recreational waters in southwestern Germany. Environ Toxicol 17:361–366

    CAS  Google Scholar 

  • Graham JL, Jones JR, Jones SB, Downing JA, Clevenger TE (2004) Environmental factors influencing microcystin distribution and concentration in the Midwestern United States. Water Res 38:4395–4404

    CAS  Google Scholar 

  • Graham JL, Loftin KA, Meyer MT, Ziegler AC (2010) Cyanotoxin mixtures and taste-and-odor compounds in cyanobacterial blooms from the midwestern United States. Environ Sci Technol 44:7361–7368

    CAS  Google Scholar 

  • Gupta N, Pant SC, Vijayaraghavan R, Rao PVL (2003) Comparative toxicity evaluation of cyanobacterial cyclic peptide toxin microcystin variants (LR, RR, YR) in mice. Toxicology 188(2–3):285–296

    CAS  Google Scholar 

  • Harke MJ, Steffen MM, Gobler CJ, Otten TG, Wilhelm SW, Wood SA, Paerl HW (2016) A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae 54:4–20

    Google Scholar 

  • Hu H, Wei Y (2006) The freshwater algae of China: systematics, taxonomy and ecology. Science Press, Beijing, China

    Google Scholar 

  • Hu Y, Qi S, Zhang J, Tan L, Zhang J, Wang Y, Yuan D (2011) Assessment of organochlorine pesticides contamination in underground rivers in Chongqing, Southwest China. J Geochem Explor 111(1–2):47–55

    CAS  Google Scholar 

  • Imai H, Chang KH, Kusaba M, Nakano SI (2009) Temperature-dependent dominance of Microcystis (Cyanophyceae) species: M. aeruginosa and M. wesenbergii. J Plankton Res 31:171–178

  • Jähnichen S, Long BM, Petzoldt T (2011) Microcystin production by Microcystis aeruginosa: direct regulation by multiple environmental factors. Harmful Algae 12:95–104

    Google Scholar 

  • Joung SH, Oh HM, Ko SR, Ahn CY (2011) Correlations between environmental factors and toxic and non-toxic Microcystis dynamics during bloom in Daechung Reservoir, Korea. Harmful Algae 10:188–193

    Google Scholar 

  • Kaebernick M, Neilan BA, Börner T, Dittmann E (2000) Light and the transcriptional response of the microcystin biosynthesis gene cluster. Appl Environ Microbiol 66(8):3387–3392

  • Koenker R, Bassett G Jr (1978) Regression quantiles. Econometrica 46:33–50

    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

    CAS  Google Scholar 

  • Lee TA, Rollwagen-Bollens G, Bollens SM, Faber-Hammond JJ (2014) Environmental influence on cyanobacteria abundance and microcystin toxin production in a shallow temperate lake. Ecotoxicol Environ Saf 114:318–325

  • Li J, Li R, Li J (2017a) Current research scenario for microcystins biodegradation-a review on fundamental knowledge, application prospects and challenges. Sci Total Environ 595(Suppl. C):615–632

    CAS  Google Scholar 

  • Li DM, Zheng HY, Pan JL, Zhang TQ, Tang SK, Lu JM, Zhong LQ, Liu YS, Liu XW (2017b) Seasonal dynamics of photosynthetic activity, Microcystis genotypes and microcystin production in Lake Taihu, China. J Great Lakes Res 43:710–716

  • Loftin KA, Graham JL, Hilborn ED, Lehmann SC, Meyer MT, Dietze JE, Griffith CB (2016) Cyanotoxins in inland lakes of the United States: occurrence and potential recreational health risks in the EPA National Lakes Assessment 2007. Harmful Algae 56:77–90

  • Mowe MAD, Porojan C, Abbas F, Mitrovic SM, Lim RP, Furey A, Yeo DCJ (2015) Rising temperatures may increase growth rates and microcystin production in tropical Microcystis species. Harmful Algae 50:88–98

    CAS  Google Scholar 

  • Neilan BA, Pearson LA, Muenchhoff J, Moffitt MC, Dittmann E (2013) Environmental conditions that influence toxin biosynthesis in cyanobacteria. Environ Microbiol 15(5):1239–1253

    CAS  Google Scholar 

  • Nürnberg GK (1996) Trophic state of clear and colored, soft and hardwater lakes with special consideration of nutrients, anoxia, phytoplankton and fish. Lake Reserv Manage 12(4):432–447

    Google Scholar 

  • Orihel DM, Bird DF, Brylinsky M, Chen H, Donald DB, Huang DY, Giani A, Kinniburgh D, Kling H, Kotak BG, Leavitt PR, Nielsen CC, Reedyk S, Rooney RC, Watson SB, Zurawell RW, Vinebrooke RD (2012) High microcystin concentrations occur only at low nitrogen-to-phosphorus ratios in nutrient-rich Canadian lakes. Can J Fish Aquat Sci 69:1457–1462

    CAS  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 46:3480–3488

  • Paerl H, Otten T (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65(4):995–1010

    CAS  Google Scholar 

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

  • Paerl HW, Hall NS, Calandrino ES (2011) Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Sci Total Environ 409(10):1739–1745

    CAS  Google Scholar 

  • Paerl HW, Xu H, Hall NS, Rossignol KL, Joyner AR, Zhu G, Qin B (2015) Nutrient limitation dynamics examined on a multi-annual scale in Lake Taihu, China: implications for controlling eutrophication and harmful algal blooms. J Freshw Ecol 30(1):5–24

    CAS  Google Scholar 

  • Papadakis EN, Vryzas Z, Kotopoulou A, Kintzikoglou K, Makris KC, Papadopoulou-Mourkidou E (2015) A pesticide monitoring survey in rivers and lakes of northern Greece and its human and ecotoxicological risk assessment. Ecotoxicol Environ Saf 116:1–9

    CAS  Google Scholar 

  • Pham TL, Utsumi M (2018) An overview of the accumulation of microcystins in aquatic ecosystems. J Environ Manag 213:520–529

  • Preece EP, Hardy FJ, Moore BC, Bryan M (2017) A review of microcystin detections in estuarine and marine waters: environmental implications and human health risk. Harmful Algae 61(Suppl. C):31–45

  • Rantala A, Rajaniemi-Wacklin P, Lyra C, Lepisto L, Rintala J, Mankiewicz-Boczek J, Sivonen K (2006) Detection of microcystin-producing cyanobacteria in Finnish Lakes with genus-specific microcystin synthetase gene E (mcyE) PCR and associations with environmental factors. Appl Environ Microbiol 72:6101–6110

  • Scherer PI, Raeder U, Geist J, Zwirglmaier K (2016) Influence of temperature, mixing, and addition of microcystin-LR on microcystin gene expression in Microcystis aeruginosa. Microbiol Open 6:e00393

  • Spears B, Steinman AD (2019) Synthesis, future avenues, and prospects. In: Steinman AD, Spears BM (eds) Internal phosphorus loading: causes, case studies, and management. J Ross Publishing, Plantation, FL, pp 445–457

  • Spoof L, Catherine A (2017) Appendix 3: tables of microcystins and nodularins. In: Meriluoto J, Spoof L, Codd GA (eds) Handbook of cyanobacterial monitoring and cyanotoxin analysis. John Wiley & Sons, Ltd, Chichester, pp 526–553

    Google Scholar 

  • Su XM, Xue QJ, Steinman AD, Zhao Y, Xie L (2015) Spatiotemporal dynamics of microcystin variants and relationships with environmental parameters in Lake Taihu, China. Toxins 7:3224–3244

    CAS  Google Scholar 

  • Su XM, Steinman AD, Xue QJ, Zhao Y, Xie L (2018) Evaluating the contamination of microcystins in Lake Taihu, China: the application of equivalent total MC-LR concentration. Ecol Indic 89:445–454

    CAS  Google Scholar 

  • Su XM, Steinman AD, Oudsema M, Hassett M, Xie L (2019) The influence of nutrients limitation on phytoplankton growth and microcystins production in Spring Lake, USA. Chemosphere 234:34–42

    CAS  Google Scholar 

  • Tonk L, Visser PM, Christiansen G, Dittmann E, Snelder EOFM, Wiedner C, Mur LR, Huisman J (2005) The microcystin composition of the cyanobacterium Planktothrix agardhii changes toward a more toxic variant with increasing light intensity. Appl Environ Microbiol 71(9):5177–5181

    CAS  Google Scholar 

  • Vézie 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 43(4):443–454

    Google Scholar 

  • Walsby AE, Hayes PK, Boje R, Stal LJ (1997) The selective advantage of buoyancy provided by gas vesicles for planktonic cyanobacteria in the Baltic Sea. New Phytol 136(3):407–417

  • Wang R, Xu M, Yang H, Yang X, Zhang K, Zhang E, Shen J (2019) Ordered diatom species loss along a total phosphorus gradient in eutrophic lakes of the lower Yangtze River basin, China. Sci Total Environ 650:1688–1695

    CAS  Google Scholar 

  • Wang SR (2015) Lake environment evolution and protection management. Science Press, Beijing

    Google Scholar 

  • Wang SMD, H S (1998) Lakes of China. Science Press, Beijing

    Google Scholar 

  • WHO (2011) Guidelines for drinking-water quality, 4th edn. World Health Organization, Geneva

  • Wu KS, 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

  • Wu XL, Xiang L, Yan QY, Jiang YN, Li YW, Huang XP, Li H, Cai QY, Mo CH (2014) Distribution and risk assessment of quinolone antibiotics in the soils from organic vegetable farms of a subtropical city, southern China. Sci Total Environ 487:399–406

    CAS  Google Scholar 

  • Xiang L, Li YW, Liu BL, Zhao HM, Li H, Cai QY, Mo CH, Wong MH, Li QX (2019) High ecological and human health risks from microcystins in vegetable fields in southern China. Environ Int 133:105142

    CAS  Google Scholar 

  • Xu H, Paerl HW, Qin B, Zhu G, Hall NS, Wu Y (2014) Determining critical nutrient thresholds needed to control harmful cyanobacterial blooms in eutrophic lake Taihu, China. Environ Sci Technol 49:1051–1059

  • Xu YY, Schroth AW, Isles PDF, Rizzo DM (2015) Quantile regression improves models of lake eutrophication with implications for ecosystem-specific management. Freshw Biol 60:1841–1853

    Google Scholar 

  • Xue QJ, Rediske RR, Gong ZJ, Su X, Xu H, Cai Y, Zhao Y, Xie L (2018) Spatio-temporal variation of microcystins and its relationship to biotic and abiotic factors in Hongze Lake, China. J Great Lakes Res 44:253–262

    CAS  Google Scholar 

  • Yu GL, Jiang YG, Song GF, Tan W, Zhu M, Li R (2014) 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

    CAS  Google Scholar 

  • Yuan LL, Pollard AI (2017) Using national-scale data to develop nutrient–microcystin relationships that guide management decisions. Environ Sci Technol 51(12):6972–6980

    CAS  Google Scholar 

  • Zamyadi A, MacLeod SL, Fan Y, McQuaid N, Dorner S, Sauvé S, Prévost M (2012) Toxic cyanobacterial breakthrough and accumulation in a drinking water plant: a monitoring and treatment challenge. Water Res 46(5):1511–1523

  • Zhao Y, Xue Q, Su X, Xie L, Yan Y, Steinman AD (2015) Microcystin-LR induced thyroid dysfunction and metabolic disorders in mice. Toxicology 328:135–141

    CAS  Google Scholar 

  • Zilliges Y, Kehr J, Meissner S, Ishida K, Mikkat S, Hagemann M, Kaplan A, Börner T, Dittman E (2011) The cyanobacteria hepatotoxin microcystin binds to proteins and increases the fitness of Microcystis under oxidative stress conditions. PLoS One 6(3):e17615

Download references

Acknowledgments

We thank Xiubo Shu, Qingju Xue, Wei Zou, Yurong Gu, and Yanhua Zhao for their helps in sample collection and MCs analysis. Xiang Wan wrote the main manuscript text; Professor Alan Steinman and Liqiang Xie modified the paper, checked English grammar, and improved English writing.

Funding

This research was supported by the National Natural Science Foundation of China (grant number 41877486), National Water Pollution Control and Management Technology Major Projects (grant no. 2018ZX07208008), and the Strategic Priority Research Program of Chinese Academy of Sciences (grant no. XDA23040201).

Author information

Authors and Affiliations

  1. State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 73 East Beijing Road, Nanjing, 210008, China

    Xiang Wan, Yurong Gu, Guangwei Zhu, Xiubo Shu, Qingju Xue, Wei Zou & Liqiang Xie

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Xiang Wan, Yurong Gu & Wei Zou

  3. Annis Water Resources Institute, Grand Valley State University, 740 West Shoreline Drive, Muskegon, MI, 49441, USA

    Alan D. Steinman

Authors
  1. Xiang Wan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alan D. Steinman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yurong Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guangwei Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiubo Shu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qingju Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wei Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Liqiang Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Liqiang Xie.

Additional information

Responsible Editor: Vitor Manuel Oliveira Vasconcelos

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 32 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wan, X., Steinman, A.D., Gu, Y. et al. Occurrence and risk assessment of microcystin and its relationship with environmental factors in lakes of the eastern plain ecoregion, China. Environ Sci Pollut Res 27, 45095–45107 (2020). https://doi.org/10.1007/s11356-020-10384-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-10384-0

Keywords

Search

Navigation