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Effects of glyphosate on microcystin-LR production and release from Microcystis aeruginosa at different temperatures

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Abstract

Cyanobacterial blooms and their associated toxins are growing issues for many aquatic ecosystems. Microcystin-LR (MC-LR) is a toxic and common cyanobacterial toxin, whereas glyphosate is a commonly used herbicide that is massively applied in agriculture. In this study, the effects of glyphosate on the growth of Microcystis aeruginosa and MC-LR synthesis and release from M. aeruginosa at different temperatures are investigated. In addition, the MC-LR pollution in the Huangpu River in Shanghai urban area is studied. Results indicated that the MC-LR concentration in the Huangpu River is related to water temperature. The laboratory experiments revealed that the growth of M. aeruginosa was slightly promoted at 15 °C and glyphosate concentrations of 1 and 5 mg/L and inhibited in the presence of glyphosate and high temperatures (20 °C, 25 °C, 30 °C, and 35 °C). The intracellular MC-LR contents were remarkably increased by glyphosate at 15 °C, 20 °C, 25 °C, and 30 °C and remarkably decreased at 35 °C. Meanwhile, the extracellular MC-LR contents were remarkably increased at all temperatures and all concentrations except when treated with 1 mg/L glyphosate at 35 °C. The highest extracellular MC-LR content, which was 143.9% higher compared with that of the control, was observed at 30 °C and treatment with 10 mg/L glyphosate. These results were consistent with those of MC-LR investigation in Huangpu River. Furthermore, in accordance with the intracellular MC-LR contents, the ability of a single cell to synthesize MC-LR was enhanced at 15 °C, 20 °C, 25 °C, and 30 °C and decreased at 35 °C. These results provide an understanding on the toxic effects of glyphosate on cyanobacteria and the effects of temperature on MC release. Moreover, these results will be helpful in protecting aquatic ecosystems and human health.

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References

  • Azevedo SM, Carmichael WW, Jochimsen EM, Rinehart KL, Lau S, Shaw GR, Eaglesham GK (2002) Human intoxication by microcystins during renal dialysis treatment in Caruaru-Brazil. Toxicology 181(24):441–446

    Google Scholar 

  • Benbrook CM (2016) Trends in glyphosate herbicide use in the United States and globally. Environ Sci Eur 28(1):1–15

    CAS  Google Scholar 

  • Brutemark A, Engström-Öst J, Vehmaa A, Gorokhova E (2015) Growth, toxicity and oxidative stress of a cultured cyanobacterium (Dolichospermum sp.) under different CO2/pH and temperature conditions. Phycol Res 63:56–63

    CAS  Google Scholar 

  • Chen SY, Zhang LJ, Chen H, Chen ZW, Wen YZ (2019) Enantioselective toxicity of chiral herbicide metolachlor to Microcystis aeruginosa. J Agric Food Chem 67(6):1631–1637

    CAS  Google Scholar 

  • Dziga D, Maksylewicz A, Maroszek M, Budzynska A, Napiorkowska-Krzebietke A, Toporowska M, Grabowska M, Kozak A, Rosińska J, Meriluoto J (2017) The biodegradation of microcystins in temperate freshwater bodies with previous cyanobacterial history. Ecotoxicol Environ Saf 145:420–430

    CAS  Google Scholar 

  • Flury M (1996) Experimental evidence of transport of pesticides through field soils - a review. J Environ Qual 25(1):25–45

    CAS  Google Scholar 

  • Jang MH, Ha K, Joo GJ, Takamura N (2003) Toxin production of cyanobacteria is increased by exposure to zooplankton. Freshw Biol 48:1540–1550

    Google Scholar 

  • Johal GS, Huber DM (2009) Glyphosate effects on diseases of plants. Eur J Agron 31(3):144–152

    CAS  Google Scholar 

  • Kumar Sinha A, Eggleton MA, Lochmann RT (2018) An environmentally friendly approach for mitigating cyanobacterial bloom and their toxins in hypereutrophic ponds: potentiality of a newly developed granular hydrogen peroxide-based compound. Sci Total Environ 637-638:524–537

    Google Scholar 

  • Li H, Joshi SR, Jaisi DP (2016) Degradation and isotope source tracking of glyphosate and aminomethylphosphonic acid. J Agric Food Chem 64:529–538

    CAS  Google Scholar 

  • Liu WH, Ming Y, Huang ZW, Li P (2012) Impacts of florfenicol on marine diatom Skeletonema costatum through photosynthesis inhibition and oxidative damages. Plant Physiol Biochem 60:165–170

    CAS  Google Scholar 

  • Ma ZL, Fang TX, Thring RW, Li YB, Yu HG, Zhou Q, Zhan M (2015) Toxic and non-toxic strains of Microcystis aeruginosa induce temperature dependent allelopathy toward growth and photosynthesis of Chlorella vulgaris. Harful Algae 48:21–29

    Article  CAS  Google Scholar 

  • Mahakhant A, Sano T, Ratanachot P, Taksawan T, Srivastava VC, Watanabe MM, Kaya K (2010) Detection of microcystins from cyanobacterial water blooms in Thailand fresh water. Phycol Res 46(s2):25–29

    Article  Google Scholar 

  • Malécot M, Guével B, Pineau C, Holbech BF, Bormans M, Wiegand C (2013) Specific proteomic response of Unio pictorum mussel to a mixture of glyphosate and microcystin-LR. J Proteome Res 12(11):5281–5292

    Article  Google Scholar 

  • Marc J, Belle R, Morales J, Cormier P, Mulner-Lorillon O (2004) Formulated glyphosate activates the DNA-response checkpoint of the cell cycle leading to the prevention of G2/M transition. Toxicol Sci 82:436–442

    Article  CAS  Google Scholar 

  • Martínez REB, Martínez JF (2018) Exposure to the herbicide 2,4-D produces different toxic effects in two different phytoplankters: a green microalga (Ankistrodesmus falcatus) and a toxigenic cyanobacterium (Microcystis aeruginosa). Sci Total Environ 619-620:1566–1578

    Article  Google Scholar 

  • Martínez HJ, Lópezrodas V, Costas E (2009) Microcystins from tap water could be a risk factor for liver and colorectal cancer: a risk intensified by global change. Med Hypotheses 72(5):539–540

    Article  Google Scholar 

  • OECD (2011) Freshwater alga and cyanobacteria, growth inhibition test (201). OECD Guidelines for the Testing of Chemicals

  • Paerl HW, Huisman J (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1(1):27–37

    Article  CAS  Google Scholar 

  • Park H, Kim B, Kim E, Okino T (1998) Hepatotoxin microcystins and neurotoxicanatoxin-a in cyanobacterial bloom from Korean lakes. Environ Toxicol Water Qual 13(3):225–234

    CAS  Google Scholar 

  • Peuthert A, Chakrabarti S, Pflugmacher S (2007) Uptake of microcystins–LR and –LF (cyanobacterial toxins) in seedlings of several important agricultural plant species and the correlation with cellular damage (lipid peroxidation). Environ Toxicol 22(4):436–442

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Posch T, Kӧster O, Salcher MM, Pernthaler J (2012) Harmful filamentous cyanobacteria favoured by reduced water turnover with lake warming. Nat Clim Change 2:809–813

  • Qian H, Pan X, Chen J, Zhou D, Chen Z, Zhang L, Fu Z (2012) Analyses of gene expression and physiological changes in Microcystis aeruginosa rebeal the phytotoxicities of three environmental pollutants. Ecotoxicology 21:847–859

    CAS  Google Scholar 

  • Ross T, V’azquez LS, Paul V (2006) Toxin release in response to oxidative stress and programmed cell death in the cyanobacterium Microcystis aeruginosa. Aquat Toxicol 78:66–73

    CAS  Google Scholar 

  • Rubin B, Kleinman Z, Ben-Ami G, Sibony M (2011) Response of Conyza spp. to glyphosate is temperature and plant age dependent. Weed science Society of America 51st annual meeting. Weed Science Society of America, Portland, OR. Abstract 364

  • Smith RD, Wilson JE, Walker JC, Baskin TI (1994) Protein-phosphatase inhibitors block root hair growth and alter cortical cell shape of Arabidopsis roots. Planta 194(4):516–524

    CAS  Google Scholar 

  • Thacker RW, Mcleod AM, Mcleod SW (2005) Herbivore-induced saxitoxin production in the freshwater cyanobacterium Lyngbya wollei. Algol Stud 117(1):415–425

    Google Scholar 

  • Thongprakaisang S, Thiantanawat A, Rangkadilok N, Suriyo T, Satayavivad J (2013) Glyphosate induces human breast cancer cells growth via estrogen receptors. Food Chem Toxicol 59:129–136

    CAS  Google Scholar 

  • Ueno Y, Nagata S, Tsutsumi T, Hasegawa A, Watanabe MF, Park HD, Chen GC, Chen G, Yu SZ (1996) Detection of microcystins, a blue-green algal hepatotoxin, in drinking water sampled in Haimen and Fusui, endemic areas of, primary liver cancer in China, by highly sensitive immunoassay. Carcinogenesis 17(6):1317–1321

    CAS  Google Scholar 

  • Van der Westhuizen AJ, Eloff JN (1985) Effect of temperature and light on the toxicity and growth of the blue-green alga Microcystis aeruginosa (UV-006). Planta 163(1):55–59

    Google Scholar 

  • Vezie C, Brient L, Sivonen K, Bertru G, Lefeuvre JC, Salkinoja-Salonen M (1998) Variation of microcystin content of Cyanobacterial blooms and isolated strains in Lake Grand-Lieu (France). Microb Ecol 35(2):126–135

    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

    CAS  Google Scholar 

  • Wang WQ, ** YT, Wu B, Sun XY, Pang XL, Wang J (2010) Assessment on genotoxicity and health risks of microcystin in drinking water sources. China Environ Sci 30(4):468–476

    CAS  Google Scholar 

  • Welker M, Von Döhren H, Tauscher H, Steinberg C, Erhard M (2003) Toxic Microcystis in shallow lake Muggelsee (Germany)-dynamics, distribution, diversity. Arch Hydrobiol 157(2):227–248

    Article  Google Scholar 

  • Wiedner C, Visser PM, Fastner J, Metcalf JS, Codd GA, Mur LR (2003) Effects of light on the microcystin content of Microcystis strain PCC 7806. Appl Environ Microbiol 69(3):1475–1481

    Article  CAS  Google Scholar 

  • Woodburn AT (2000) Glyphosate: production, pricing and use worldwide. Pest Manag Sci 56:309–312

    Article  CAS  Google Scholar 

  • Ye J, Wang L, Zhang Z, Liu W (2013) Enantioselective physiological effects of the herbicide diclofop on cyanobacterium Microcystis aeruginosa. Enciron Sci Technol 47:3893–3901

    Article  CAS  Google Scholar 

  • Yu SZ (1995) Primary prevention of hepatacelluar carcinoma. J Gastroen Hepatol 10:674–682

    Article  CAS  Google Scholar 

  • Zhang P, Zhai C, Chen R, Liu C, Xue Y, Jiang J (2012) The dynamics of the waterbloom-forming Microcystis aeruginosa and its relationship with biotic andabiotic factors in Lake Taihu, China. Ecol Eng 47:274–277

    Google Scholar 

  • Zhang Q, Song Q, Wang C, Zhou C, Lu C, Zhao M (2016) Effects of glufosinate on the growth of and microcystin production by Microcystis aeruginosa at environmentally relevant concentrations. Sci Total Environ 575:513–518

    Google Scholar 

  • Zhang Q, Qin WD, Yang LY, An J, Zhang XX, Hong H, Xu LZ, Wang YP (2018) Microcystis bloom containing microcystin-LR induces type 2 diabetes mellitus. Toxicol Lett 294:87–94

    CAS  Google Scholar 

  • Zheng WW, Yang L, Ma WR, Huang Y, Crabbe MJC, Qu WD (2018) The occurrence and potential health risk of microcystins in drinking water of rural areas in China. https://doi.org/10.1016/B978-0-12-409548-9.11541-6

  • Zhu L, Zuo J, Song LR, Gan NQ (2016) Microcystin-degrading bacteria affect mcyD expression and microcystin synthesis in Microcystis spp. J Environ Sci-China 41:195–201

    CAS  Google Scholar 

Download references

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Authors and Affiliations

  1. School of Chemical and Environmental Engineering, Shanghai Institute of Technology, Shanghai, 201418, China

    **g Ye, Ying Guan, Chunhui Wang & Jiawen Chen

  2. Department of Chemical and Environmental Engineering, University of California, Riverside, CA, 92521, USA

    Liang Wu

  3. Program of Environmental Toxicology, University of California, Riverside, CA, 92521, USA

    Liang Wu

  4. College of Environment, Zhejiang University of Technology, Hangzhou, 310032, China

    Shanshan Zhou & Chao Xu

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  1. **g Ye
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Ye, J., Guan, Y., Wu, L. et al. Effects of glyphosate on microcystin-LR production and release from Microcystis aeruginosa at different temperatures. Environ Sci Pollut Res 27, 41961–41969 (2020). https://doi.org/10.1007/s11356-020-10185-5

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  • DOI: https://doi.org/10.1007/s11356-020-10185-5

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