Skip to main content
SpringerLink
Log in

Temporal dynamics of microcystins in two reservoirs with different trophic status during the early growth stage of cyanobacteria

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

Abstract

Harmful cyanobacterial blooms are increasing in frequency and severity, which makes their toxic secondary metabolites of microcystins (MCs) have been widely studied, especially in their distribution and influence factors in different habitats. However, the distribution of MCs on the early growth stage of harmful cyanobacteria and its influence factors and risks are still largely unknown. Thus, in the present study, two reservoirs (Lutian Reservoir and Lake Haitang) with different trophic status in China have been studied weekly from March to May in 2018, when the cyanobacteria communities were just in the early growth stage, to investigate the variation of MCs concentration and the relationships between MCs and environmental parameters. During the investigation, Lutian Reservoir and Lake Haitang were found to be mesotrophic and light eutrophic, respectively. In Lutian Reservoir, the concentration of EMCs (extracellular MCs) was obviously higher than that of IMCs (intracellular MCs) with a mean value of 0.323 and 0.264 μg/L, respectively. Meanwhile, the concentration of EMCs also fluctuated more sharply than that of IMCs. Congeners of IMC-YR and EMC-LR were respectively dominant in total concentrations of IMCs and EMCs. Unsurprisingly, in Lake Haitang, the concentrations of IMC and EMC were both significantly higher than that in Lutian Reservoir with a mean concentration of 0.482 and 0.472 μg/L, respectively. Differently, the concentration of MC-YR was dominant in both IMCs and EMCs, followed by MC-LR. In correlation analysis, the IMCs were significantly and positively correlated with the density and biomass of phytoplankton phyla and potential MCs-producing cyanobacteria and the parameters of water temperature (WT), nutrients, and organic matters. Similar results were also observed for EMCs. While the different variations of MCs in the two reservoirs might be primarily caused by the differences in WT, nutrients (especially phosphorus), organic matters, and the composition of MCs-producing cyanobacteria. In addition, the coexistence of the dominant species of Pseudoanabaena sp., which can produce a taste-and-odor compound of 2-methylisoborneol (2-MIB), might have a significant impact on the concentration and toxicity of MCs. Our results suggested that the risks posed by MCs at the early growth stage of cyanobacteria should also deserve our attention, especially in mesotrophic water bodies.

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

Data availability

The datasets used during the current study are available from the corresponding author on reasonable request.

References

  • Bakker ES, Hilt S (2016) Impact of water-level fluctuations on cyanobacterial blooms: options for management. Aquat Ecol 50(3):485–498

    Article  CAS  Google Scholar 

  • Benegas GRS, Bernal SPF, de Oliveira VM, Passarini MRZ (2021) Antimicrobial activity against Microcystis aeruginosa and degradation of microcystin-LR by bacteria isolated from Antarctica. Environ Sci Pollut R 28:52381–52391

    Article  CAS  Google Scholar 

  • Brêda-Alves F, de Oliveira Fernandes V, Cordeiro-Araújo MK, Chia MA (2021) The combined effect of clethodim (herbicide) and nitrogen variation on allelopathic interactions between Microcystis aeruginosa and Raphidiopsis raciborskii. Environ Sci Pollut R 28:11528–11539

    Article  Google Scholar 

  • Buratti FM, Manganelli M, Vichi S, Stefanelli M, Scardala S, Testai E, Funari E (2017) Cyanotoxins: producing organisms, occurrence, toxicity, mechanism of action and human health toxicological risk evaluation. Arch Toxicol 91(3):1049–1130

    Article  CAS  Google Scholar 

  • Chaffin JD, Davis TW, Smith DJ, Baer MM, Dick GJ (2018) Interactions between nitrogen form, loading rate, and light intensity on Microcystis and Planktothrix growth and microcystin production. Harmful Algae 73:84–97

    Article  Google Scholar 

  • Chen L, Chen J, Zhang X, Xie P (2016) A review of reproductive toxicity of microcystins. J Hazard Mater 301:381–399

    Article  CAS  Google Scholar 

  • Cordeiro-Araújo MK, Bittencourt-Oliveira, M.d.C. (2013) Active release of microcystins controlled by an endogenous rhythm in the cyanobacterium Microcystis aeruginosa. Phycol Res 61(1):1–6

    Article  Google Scholar 

  • Cunha DGF, Dodds WK, Loiselle SA (2018) Factors related to water quality and thresholds for microcystin concentrations in subtropical Brazilian reservoirs. Inland Waters 8(3):368–380

    Article  CAS  Google Scholar 

  • Díez-Quijada L, Prieto AI, Guzmán-Guillén R, Jos A, Cameán AM (2019) Occurrence and toxicity of microcystin congeners other than MC-LR and MC-RR: a review. Food Chem Toxicol 125:106–132

    Article  Google Scholar 

  • Downing TG, Meyer C, Gehringer MM, van de Venter M (2005) Microcystin content of Microcystis aeruginosa is modulated by nitrogen uptake rate relative to specific growth rate or carbon fixation rate. Environ Toxicol 20(3):257–262

    Article  CAS  Google Scholar 

  • Feng L-J, Sun X-D, Zhu F-P, Feng Y, Duan J-L, Xiao F, Li X-Y, Shi Y, Wang Q, Sun J-W, Liu X-Y, Liu J-Q, Zhou L-L, Wang S-G, Ding Z, Tian H, Galloway TS, Yuan X-Z (2020) Nanoplastics promote microcystin synthesis and release from cyanobacterial Microcystis aeruginosa. Environ Sci Technol 54(6):3386–3394

    Article  CAS  Google Scholar 

  • Ford DE (1990) Reservoir transport processes. In: Reservoir Limnology: Ecological Perspectives. John Wiley & Sons, New York

  • Gan N, Xiao Y, Zhu L, Wu Z, Liu J, Hu C, Song L (2012) The role of microcystins in maintaining colonies of bloom-forming Microcystis spp. Environ Microbiol 14(3):730–742

    Article  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(19):7361–7368

    Article  CAS  Google Scholar 

  • Gurbuz F, Uzunmehmetoğlu OY, Diler Ö, Metcalf JS, Codd GA (2016) Occurrence of microcystins in water, bloom, sediment and fish from a public water supply. Sci Total Environ 562:860–868

    Article  CAS  Google Scholar 

  • Harke MJ, Gobler CJ (2013) Global transcriptional responses of the toxic cyanobacterium, Microcystis aeruginosa, to nitrogen stress, phosphorus stress, and growth on organic matter. PLoS ONE 8(7):e69834

    Article  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

    Article  Google Scholar 

  • Hu C, Rzymski P (2019) Programmed cell death-like and accompanying release of microcystin in freshwater bloom-forming cyanobacterium Microcystis: From identification to ecological relevance. Toxins 11(12):706

    Article  CAS  Google Scholar 

  • Huisman J, Codd GA, Paerl HW, Ibelings BW, Verspagen JMH, Visser PM (2018) Cyanobacterial blooms. Nat Rev Microbiol 16(8):471–483

    Article  CAS  Google Scholar 

  • Jacoby JM, Collier DC, Welch EB, Hardy FJ, Crayton M (2000) Environmental factors associated with a toxic bloom of Microcystis aeruginosa. Can J Fish Aquat Sci 57(1):231–240

    Article  Google Scholar 

  • Jin X, Tu Q (1990) The standard methods for observation and analysis in lake eutrophication. Chinese Environmental Science Press, Beijing

    Google Scholar 

  • Jin X, Liu S, Zhang Z (1995) Lake environment in China. Oceanography press, Beijing

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Khomutovska N, Sandzewicz M, Łach Ł, Suska-Malawska M, Chmielewska M, Mazur-Marzec H, Cegłowska M, Niyatbekov T, Wood SA, Puddick J, Kwiatowski J, Jasser I (2020) Limited microcystin, anatoxin and cylindrospermopsin production by cyanobacteria from microbial mats in cold deserts. Toxins 12(4):244

    Article  CAS  Google Scholar 

  • Li Z, Yu J, Yang M, Zhang J, Burch MD, Han W (2010) Cyanobacterial population and harmful metabolites dynamics during a bloom in Yanghe Reservoir. North China Harmful Algae 9(5):481–488

    Article  CAS  Google Scholar 

  • Li L, Zhu C, Xie C, Shao C, Yu S, Zhao L, Gao N (2018) Kinetics and mechanism of Pseudoanabaena cell inactivation, 2-MIB release and degradation under exposure of ozone, chlorine and permanganate. Water Res 147:422–428

    Article  CAS  Google Scholar 

  • Liu Y-L, Walker HW, Lenhart JJ (2019) The effect of natural organic matter on the adsorption of microcystin-LR onto clay minerals. Colloid Surface A 583:123964

    Article  CAS  Google Scholar 

  • Major Y, Kifle D, Spoof L, Meriluoto J (2018) Cyanobacteria and microcystins in Koka reservoir (Ethiopia). Environ Sci Pollut R 25(27):26861–26873

    Article  CAS  Google Scholar 

  • Massey IY, Al Osman M, Yang F (2020) An overview on cyanobacterial blooms and toxins production: Their occurrence and influencing factors. Toxin Rev 1–21

  • Monchamp ME, Pick FR, Beisner BE, Maranger R (2014) Nitrogen forms influence microcystin concentration and composition via changes in cyanobacterial community structure. PLoS One 9(1):e85573

    Article  Google Scholar 

  • Niu Y, Shen H, Chen J, Xie P, Yang X, Tao M, Ma Z, Qi M (2011) Phytoplankton community succession shaping bacterioplankton community composition in Lake Taihu. China Water Res 45(14):4169–4182

    Article  CAS  Google Scholar 

  • Noori R, Berndtsson R, Franklin Adamowski J, Rabiee Abyaneh M (2018) Temporal and depth variation of water quality due to thermal stratification in Karkheh Reservoir. Iran J Hydrol-Reg Stud 19:279–286

    Google Scholar 

  • Nowlin WH, Davies J-M, Nordin RN, Mazumder A (2004) Effects of water level fluctuation and short-term climate variation on thermal and stratification regimes of a British Columbia reservoir and lake. Lake Reserv Manage 20(2):91–109

    Article  Google Scholar 

  • Okello W, Ostermaier V, Portmann C, Gademann K, Kurmayer R (2010a) Spatial isolation favours the divergence in microcystin net production by Microcystis in Ugandan freshwater lakes. Water Res 44(9):2803–2814

    Article  CAS  Google Scholar 

  • Okello W, Portmann C, Erhard M, Gademann K, Kurmayer R (2010b) Occurrence of microcystin-producing cyanobacteria in Ugandan freshwater habitats. Environ Toxicol 25(4):367–380

    Article  CAS  Google Scholar 

  • Orr PT, Jones GJ (1998) Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures. Limnol Oceanogr 43(7):1604–1614

    Article  CAS  Google Scholar 

  • Pang Z, Cai Y, Xiong W, Xiao J, Zou J (2021) A spectrophotometric method for measuring permanganate index (CODMn) by N, N-diethyl-p-phenylenediamine (DPD). Chemosphere 266:128936

    Article  CAS  Google Scholar 

  • Rohrlack T, Hyenstrand P (2007) Fate of intracellular microcystins in the cyanobacterium Microcystis aeruginosa (Chroococcales, Cyanophyceae). Phycologia 46(3):277–283

    Article  Google Scholar 

  • Rzymski P, Klimaszyk P, Jurczak T, Poniedziałek B (2020) Oxidative stress, programmed cell death and microcystin release in Microcystis aeruginosa in response to Daphnia Grazers. Front Microbiol 11(1201)

  • Shang L, Feng M, Xu X, Liu F, Ke F, Li W (2018) Co-occurrence of microcystins and taste-and-odor compounds in drinking water source and their removal in a full-scale drinking water treatment plant. Toxins 10(1):26

    Article  Google Scholar 

  • Shishido TK, Jokela J, Humisto A, Suurnäkki S, Wahlsten M, Alvarenga DO, Sivonen K, Fewer DP (2019) The biosynthesis of rare homo-amino acid containing variants of microcystin by a benthic cyanobacterium. Mar Drugs 17(5):271

    Article  CAS  Google Scholar 

  • Simiyu BM, Oduor SO, Rohrlack T, Sitoki L, Kurmayer R (2018) Microcystin content in phytoplankton and in small fish from eutrophic Nyanza Gulf, Lake Victoria. Kenya Toxins 10(7):275

    Article  Google Scholar 

  • Sivonen K, Jones G (1999) Cyanobacterial toxins, In: Toxic Cyanobacteria in Water: a Guide to Public Health Significance, Monitoring and Management. I. Chorus & J. Bertram (Eds.). p. 41–91. The World Health Organization. ISBN 0–419–23930–8. E & FN Spon, London, UK

  • Su X, Xue Q, Steinman A, Zhao Y, Xie L (2015) Spatiotemporal dynamics of microcystin variants and relationships with environmental parameters in Lake Taihu. China Toxins 7(8):3224

    Article  CAS  Google Scholar 

  • Tilahun S, Kifle D, Zewde TW, Johansen JA, Demissie TB, Hansen JH (2019) Temporal dynamics of intra-and extra-cellular microcystins concentrations in Koka reservoir (Ethiopia): Implications for public health risk. Toxicon 168:83–92

    Article  CAS  Google Scholar 

  • Vasconcelos VM, Sivonen K, Evans WR, Carmichael WW, Namikoshi M (1996) Hepatotoxic microcystin diversity in cyanobacterial blooms collected in portuguese freshwaters. Water Res 30(10):2377–2384

    Article  CAS  Google Scholar 

  • Wagner ND, Quach E, Buscho S, Ricciardelli A, Kannan A, Naung SW, Phillip G, Sheppard B, Ferguson L, Allen A, Sharon C, Duke JR, Taylor RB, Austin BJ, Stovall JK, Haggard BE, Chambliss CK, Brooks BW, Scott JT (2021) Nitrogen form, concentration, and micronutrient availability affect microcystin production in cyanobacterial blooms. Harmful Algae 103:102002

    Article  CAS  Google Scholar 

  • Walls JT, Wyatt KH, Doll JC, Rubenstein EM, Rober AR (2018) Hot and toxic: temperature regulates microcystin release from cyanobacteria. Sci Total Environ 610–611:786–795

    Article  Google Scholar 

  • Wan L, Wu Y, Zhang B, Yang W, Ding H, Zhang W (2021a) Effects of moxifloxacin and gatifloxacin stress on growth, photosynthesis, antioxidant responses, and microcystin release in Microcystis aeruginosa. J Hazard Mater 409:124518

    Article  CAS  Google Scholar 

  • Wan X, Cheng C, Gu Y, Shu X, Xie L, Zhao Y (2021b) Acute and chronic toxicity of microcystin-LR and phenanthrene alone or in combination to the cladoceran (Daphnia magna). Ecotox Environ Safe 220:112405

    Article  CAS  Google Scholar 

  • Wang M, Shi W, Chen Q, Zhang J, Yi Q, Hu L (2018) Effects of nutrient temporal variations on toxic genotype and microcystin concentration in two eutrophic lakes. Ecotox Environ Safe 166:192–199

    Article  CAS  Google Scholar 

  • Wang H, Xu C, Liu Y, Jeppesen E, Svenning JC, Wu J, Zhang W, Zhou T, Wang P, Nangombe S, Ma J, Duan H, Fang J, Xie P (2021) From unusual suspect to serial killer: cyanotoxins boosted by climate change may jeopardize African megafauna. The Innov 100092

  • Wood SA, Holland PT, Stirling DJ, Briggs LR, Sprosen J, Ruck JG, Wear RG (2006) Survey of cyanotoxins in New Zealand water bodies between 2001 and 2004. New Zeal J Mar Fresh 40(4):585–597

    Article  CAS  Google Scholar 

  • Wu SK, XIE, P., LIANG, G.D., WANG, S.B., LIANG, X.M. (2006) Relationships between microcystins and environmental parameters in 30 subtropical shallow lakes along the Yangtze River. China Freshwater Biol 51(12):2309–2319

    Article  CAS  Google Scholar 

  • Xue Q, Steinman AD, Su X, Zhao Y, Xie L (2016) Temporal dynamics of microcystins in Limnodrilus hoffmeisteri, a dominant oligochaete of hypereutrophic Lake Taihu. China Environ Pollut 213:585–593

    Article  CAS  Google Scholar 

  • Xue Q, Rediske RR, Gong Z, 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(2):253–262

    Article  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

    Article  CAS  Google Scholar 

  • Zastepa A, Pick FR, Blais JM (2014) Fate and persistence of particulate and dissolved microcystin-LA from Microcystis blooms. Hum Ecol Risk Assess 20(6):1670–1686

    Article  CAS  Google Scholar 

  • Zhang Q-X, Yu M-J, Li S-H, Carmichael WW (1991) Cyclic peptide hepatotoxins from freshwater cyanobacterial (blue-green algae) waterblooms collected in Central China. Environ Toxicol Chem 10(3):313–321

    Article  CAS  Google Scholar 

  • Zhang L, Liu J, Zhang D, Luo L, Liao Q, Yuan L, Wu N (2018) Seasonal and spatial variations of microcystins in Poyang Lake, the largest freshwater lake in China. Environ Sci Pollut R 25(7):6300–6307

    Article  CAS  Google Scholar 

  • Zhao M, Qu D, Shen W, Li M (2019) Effects of dissolved organic matter from different sources on Microcystis aeruginosa growth and physiological characteristics. Ecotox Environ Safe 176:125–131

    Article  CAS  Google Scholar 

Download references

Funding

This research was supported by the National Natural Science Foundation of China (Grant No. 41907326, 41877486, 41877502), Natural Science Foundation of Jiangsu Province (Grant No. BK20170109), and the Youth Innovation Promotion Association CAS (2018352).

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

    Qingju Xue, Liqiang Xie, Tong Li & Yanyan Zhao

  2. University of Chinese Academy of Sciences, 19 Yuquan Road, Beijing, 100049, China

    Qingju Xue, Liqiang Xie & Yanyan Zhao

  3. Ministry of Ecology and Environment, Nanjing Institute of Environmental Sciences, 8 Jiangwangmiao, 10 Street, Nanjing, 210042, China

    Ming Kong

  4. College of Chemistry and Life Sciences, Zhejiang Normal University, 688 Yingbin Road, Jinhua, 321004, China

    Mengna Liao & Zebin Yan

Authors
  1. Qingju Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ming Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liqiang Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mengna Liao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zebin Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yanyan Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Qingju Xue: formal analysis, writing, and original draft preparation. Ming Kong: sample analysis and manuscript review. Liqiang Xie: methodology and manuscript review. Tong Li, Mengna Liao, and Zebin Yan: sample sampling, data acquisition, and analysis. Yanyan Zhao: methodology, manuscript review, and editing. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Yanyan Zhao.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Vitor Vasconcelos

Publisher's note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xue, Q., Kong, M., Xie, L. et al. Temporal dynamics of microcystins in two reservoirs with different trophic status during the early growth stage of cyanobacteria. Environ Sci Pollut Res 29, 87132–87143 (2022). https://doi.org/10.1007/s11356-022-21665-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-022-21665-1

Keywords

Search

Navigation