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Responses of submerged macrophyte Ceratophyllum demersum to the gradient concentrations of microcystin-LR (MC-LR)

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Abstract

The responses of Ceratophyllum demersum to gradient concentrations (0, 0.8, 3.2, and 10 µg/L) of microcystin-LR (MC-LR) were comprehensively investigated by laboratory simulation experiments. The high reduction and accumulation efficiency of MC-LR by C. demersum were verified in this study. Results showed that the reduction ratio of MC-LR in the cultivation medium was up to 99% after 14 days of exposure, and the accumulation of MC-LR in C. demersum was highest at an exposure concentration of 10 μg/L, the value of which was 0.9 ng/g fresh weight (FW). Meanwhile, a series of negative effects on C. demersum was detectable, accompanied by a significant biomass reduction of the plant and changes in microbial community composition. In particular, this study indicated that the amount of Flavobacteria was elevated under the stress of MC-LR, provoking great threats to aquatic ecosystems. Moreover, oxidative damage was evidenced by the changes in total antioxidant capacity, superoxide dismutase, and glutathione. The results also demonstrated significant increases in sugar (0.025 mg/g FW), protein (0.3 mg/g FW), and carotenoids (0.6 mg/g FW) in C. demersum stressed by 10 μg/L of MC-LR, compared with the control without microcystins, which were among the defense strategies for dealing with adverse conditions. These results verified the good potential of submerged macrophytes as an eco-friendly strategy for controlling cyanobacterial blooms. However, the negative effects of MC-LR on the macrophytes themselves were also demonstrated, which would be considered in future practice and management.

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References

  • Abed SN, Almuktar SA, Scholz M (2017) Remediation of synthetic greywater in mesocosm-scale floating treatment wetlands. Ecol Eng 102:303–319

    Article  Google Scholar 

  • Aguilera A, Haakonsson S, Martin MV, Salerno GL, Echenique RO (2018) Bloom forming cyanobacteria and cyanotoxins in Argentina: a growing health and environmental concern. Limnologica 69:103–114

    Article  CAS  Google Scholar 

  • Amorim CA, de Moura-Falcão RHD, Valenca CR, Souza VRD, Moura ADN (2019) Allelopathic effects of the aquatic macrophyte Ceratophyllum demersum L. on phytoplankton species: contrasting effects between cyanobacteria and chlorophytes. Acta Limnologica Brasiliensis 31:e21

    Article  CAS  Google Scholar 

  • Amorim CA, Moura AN (2020) Effects of the manipulation of submerged macrophytes, large zooplankton, and nutrients on a cyanobacterial bloom: a mesocosm study in a tropical shallow reservoir. Environ Pollut 265:114997

    Article  CAS  Google Scholar 

  • Amorim CA, Ulisses C, Moura AN (2017) Biometric and physiological responses of Egeria densa Planch. Cultivated with toxic and non-toxic strains of Microcystis. Aquat Toxicol 191:201–208

    Article  CAS  Google Scholar 

  • Babica P, Bláha L, Marŝálek B (2006) Exploring the natural role of microcystins-a review of effects on photoautotrophic organisms. J Phycol 42:9–20

    Article  Google Scholar 

  • Bartelme RP, Oyserman BO, Blom JE, Sepulveda-Villet QJ, Newton RJ (2018) Stripping away the soil: plant growth promoting microbiology opportunities in aquaponics. Front Microbiol 9:8

    Article  Google Scholar 

  • Bernardet JF, Segers P, Vancanneyt M, Berthe F, Kersters K, Vandamme P (1996) Cutting a Gordian knot: emended classification and description of the genus Flavobacterium, emended description of the family Flavobacteriaceae, and proposal of Flavobacterium hydatis nom. nov. (basonym, Cytophaga aquatilis Strohl and Tait 1978). Int J Syst Bacteriol 46(1):128–148

    Article  Google Scholar 

  • Bi XD, Dai W, Wang XY, Dong SJ, Zhang SL, Zhang DJ, Wu M (2019) Microcystins distribution, bioaccumulation, and Microcystis genotype succession in a fish culture pond. Sci Total Environ 688:380–388

    Article  CAS  Google Scholar 

  • Cao Q, Liu WJ, Gu YR, Xie LQ, Jiang WL, Gao Y, Yang LY (2020) Synergetic enhancement toxicity of copper, cadmium and microcystin-LR to the Ceratophyllum demersum L. Toxicon 186:151–159

    Article  CAS  Google Scholar 

  • Chang MY, Li CL, Dong J, Shang XY, Wang JH, Niu MM (2019) Dynamic changes of phytoplankton composition during cyanobacteria blooms in aquaculture ponds. Progr Fish Sci 40(1):36–45 (In Chinese)

    Google Scholar 

  • Chen GY, Zheng ZH, Bai MX, Li QS (2020) Chronic effects of microcystin-LR at environmental relevant concentrations on photosynthesis of Typa angustifolia Linn. Ecotoxicology 29:514–523

    Article  CAS  Google Scholar 

  • Cui WD, Leng XJ, Li XQ, Li XN, Xu J (2009) Effects of astaxanthin and canthaxanthin on pigmentation of muscle and total antioxidant capacity of liver in rainbow trout Oncorhynchus mykiss. J Fish China 33(6):987–995

    CAS  Google Scholar 

  • De Morais Calado SL, Esterhuizen-Londt M, de Assis HCS, Pflugmacher S (2019) Phytoremediation: green technology for the removal of mixed contaminants of a water supply reservoir. Int J Phytoremediation 21(4):372–379

    Article  Google Scholar 

  • Domonkos I, Kis M, Gombos Z, Ughy B (2013) Carotenoids, versatile components of oxygenic photosynthesis. Prog Lipid Res 52(4):539–561

    Article  CAS  Google Scholar 

  • Dong J, Li CL, Dai DJ, Zhang M, Gao YN, Li XJ, Li M, Zhang JX, Wang XF, Zhou CJ (2021) Protective effects of astaxanthin from Haematococcus pluvialis on the survival and oxidative stress of zebrafish embryos induced by microcystin-LR. J Appl Phycol 33:2261–2271

    Article  CAS  Google Scholar 

  • Duan JJ, Feng YF, Yu YL, He SY, Xue LH, Yang LZ (2016) Differences in the treatment efficiency of a cold-resistant floating bed plant receiving two types of low-pollution wastewater. Environ Monit Assess 188(5):283

    Article  Google Scholar 

  • Flores-Rojas NC, Esterhuizen-Londt M, Pflugmacher S (2015) Antioxidative stress responses in the floating macrophyte Lemna minor L. with cylindrospermopsin exposure. Aquat Toxicol 169:188–195

    Article  CAS  Google Scholar 

  • Gao L, Zhou WL, Wu SQ, He SB, Huang JC, Zhang X (2018) Nitrogen removal by thiosulfate-driven denitrification and plant uptake in enhanced floating treatment wetland. Sci Total Environ 621:1550–1558

    Article  CAS  Google Scholar 

  • Gong L, Zhang S, Chen D, Liu K, Lu J (2018) Response of biofilms-leaves of two submerged macrophytes to high ammonium. Chemosphere 192:152–160

    Article  CAS  Google Scholar 

  • Ha MH, Pflugmacher S (2013) Time-dependent alterations in growth, photosynthetic pigments and enzymatic defense systems of submerged Ceratophyllum demersum during exposure to the cyanobacterial neurotoxin anatoxin-a. Aquat Toxicol 138–139:26–34

    Article  Google Scholar 

  • Ha MH, Jara VC, Pflugmacher S (2014) Uptake of the cyanobacterial neurotoxin, anatoxin-a, and alternations in oxidative stress in the submerged aquatic plant Ceratophyllum demersum. Ecotox Environ Safe 101:205–212

    Article  CAS  Google Scholar 

  • Hilt S, Ghobrial M, Gross EM (2006) In situ allelopathic potential of Myriophyllum verticillatum (Haloragaceae) against selected phytoplankton species. J Phycol 42:1189–1198

    Article  Google Scholar 

  • Hu XB, Zhang RF, Ye JY, Wu X, Zhang YX, Wu CL (2018) Monitoring and research of microcystins and environmental factors in a typical artificial freshwater aquaculture pond. Environ Sci Pollut Res 25:5921–5933

    Article  CAS  Google Scholar 

  • Hu ZF, Li DS, Guan DT (2020) Water quality retrieval and algae inhibition from eutrophic freshwaters with iron-rich substrate based ecological floating beds treatment. Sci Total Environ 712:135584

    Article  CAS  Google Scholar 

  • Jiang J, Gu X, Song R, Wang X, Yang L (2011) Microcystin-LR induced oxidative stress and ultrastructural alterations in mesophyll cells of submerged macrophyte Vallisneria natans (Lour.) Hara. J Hazard Mater 190:188–196

    Article  CAS  Google Scholar 

  • Jiang MQ, Zhou YP, Wang N, Xu L, Zheng Z, Zhao JB (2019) Allelopathic effects of harmful algal extracts and exudates on biofilms on leaves of Vallisneria natans. Sci Total Environ 655:823–830

    Article  CAS  Google Scholar 

  • Lajayer BA, Ghorbanpour M, Nikabadi S (2017) Heavy metals in contaminated environment: destiny of secondary metabolite biosynthesis, oxidative status and phytoextraction in medical plants. Ecotox Environ Safe 145:377–390

    Article  Google Scholar 

  • Li D, Rothballer M, Schmid M, Esperschutz J, Hartmann A (2011) Acidovorax radicis sp nov., a wheat-root-colonizing bacterium. Int J Syst Evol Microb 61:2589–2594

    Article  CAS  Google Scholar 

  • Li Q, Fang Y, Xu Y (2018) Duckweed Landoltia punctata purifes micro-polluted surface water and produces starch. Chin J Appl Environ Biol 24(6):132–137

    Google Scholar 

  • Li HS, Sun Q, Zhao SJ (2000) The experiment principle and technique on plant physiology and biochemistry. Higher Education Press, Beijing, pp 194–197

    Google Scholar 

  • Li Q, Gu P, Ji XY, Li HM, Zhang JB, Zheng Z (2020a) Response of submerged macrophytes and periphyton biofilm to water flow in eutrophic environment: plant structural, physicochemical and microbial properties. Ecotox Environ Safe 189:109990

    Article  CAS  Google Scholar 

  • Li Q, Gu P, Luo X, Zhang H, Huang SZ, Zhang JB, Zheng Z (2020b) Pilot-scale study on the effects of cyanobacterial blooms on Vallisneria natans and biofilms at different phosphorus concentrations. Environ Pollut 265:114996

    Article  CAS  Google Scholar 

  • Li Q, Gu P, Zhang C, Luo X, Zhang H, Zhang JB, Zheng Z (2020c) Combined toxic effects of anatoxin-a and microcytin-LR on submerged macrophytes and biofilms. J Hazard Mater 389:122053

    Article  CAS  Google Scholar 

  • Li Q, Gu P, Zhang H, Luo X, Zhang JB, Zheng Z (2020d) Response of submerged macrophytes and leaf biofilms to the decline phase of Microcystis areuginosa: antioxidant response, ultrastructure, microbial properties, and potential mechanism. Sci Total Environ 699:134325

    Article  CAS  Google Scholar 

  • Li XN, Song HL, Li W, Lu XW, Nishimura O (2010) An integrated ecological floating-bed employing plant, freshwater clam and biofilm carrier for purification of eutrophic water. Ecol Eng 36:382–390

    Article  Google Scholar 

  • Limbu SM, Zhou L, Sun SX, Zhang ML, Du ZY (2018) Chronic exposure to low environmental concentrations and legal aquaculture doses of antibiotics cause systemic adverse effects in Nile tilapia and provoke differential human health risk. Environ Int 115:205–219

    Article  CAS  Google Scholar 

  • Lürling M, Van Geest G, Scheffer M (2006) Importance of nutrient competition and allelopathic effects in suppression of the green alga Scenedesmus obliquus by the macrophytes Chara, Elodea and Myriophyllum. Hydrobiologia 556:209–220

    Article  Google Scholar 

  • Maranda NCFR, Pflugmacher ELS (2015) Antioxidative stress responses in the floating macrophyte Lemna minor L. with cylindrospermopsin exposure. Aquat Toxicol 169:188–195

    Article  Google Scholar 

  • Mitrovic SM, Allis O, Furey A, James KJ (2005) Bioaccumulation and harmful effects of microcystin-LR in the aquatic plants Lemna minor and Wolffia arrhiza and the filamentous alga Chladophora fracta. Ecotox Environ Safe 61:345–352

    Article  CAS  Google Scholar 

  • Nimptsch J, Wiegand C, Pflugmacher S (2008) Cyanobacterial toxin elimination via bioaccumulation of MC-LR in aquatic macrophytes: an application of the green liver concept. Environ Sci Technol 48:8552–8557

    Article  Google Scholar 

  • Oliva CSR, Jara VC, Pflugmacher S (2015) Antioxidative response of the three macrophytes Ceratophyllum demersum, Egeria densa, and Hydrilla verticillata to a time dependent exposure of cell-free crude extracts containing three microcystins from cyanobacterial blooms of Lake Amatitlán, Guatemala. Aquat Toxicol 163:130–139

    Article  Google Scholar 

  • Omidi A, Esterhuizen-Londt M, Pflugmacher S (2018) Still challenging: the ecological function of the cyanobacterial toxin microcystin-what we know so far. Toxin Rev 37(2):87–105

    Article  CAS  Google Scholar 

  • Pakdel FM, Sim L, Bearda J, Davis J (2013) Allelopathic inhibition of microalgae by the freshwater stonewort, Chara australis, and a submerged angiosperm, Potamogeton crispus. Aquat Bot 110:24–30

    Article  Google Scholar 

  • Pflugmacher S (2002) Possible allelopathic effects of cyanotoxins, with reference to microcystin-LR, in aquatic ecosystems. Environ Toxicol 17(4):407–413

    Article  CAS  Google Scholar 

  • Pflugmacher S (2004) Promotion of oxidative stress in C. demersum due to exposure to cyanobacterial toxin. Aquat Toxicol 70:169–178

    Article  CAS  Google Scholar 

  • Pflugmacher S, Codd GA, Steinberg CEW (1999) Effects of the cyanobacterial toxin microcystin-LR on detoxication enzymes in aquatic plants. Environ Toxicol 14(1):111–115

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Pradhan A, Silva CO, Silva C, Pascoal C, Cassio F (2016) Enzymatic biomarkers can portray nanoCuO-induced oxidative and neuronal stress in freshwater shredders. Aquat Toxicol 180:227–235

    Article  CAS  Google Scholar 

  • Qifang G (2008) Drought tolerance through overexpression of monoubiquitin in transgenic tobacco. J Plant Physiol 16:1745–1755

    Google Scholar 

  • Qing M, Lin LJ, Sun J, Liao MA (2018) Effects of cadmium stress on antioxidant enzymes activities and soluble protein content in Cyphomandra betacea seedlings. Earth Environ Sci 199:032025

    Google Scholar 

  • Rippka R, Deruelle J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microb 111:1–61

    Google Scholar 

  • Rojo C, Segura M, Cortés F, Rodrigo MA (2013) Allelopathic effects of microcystin-LR on the germination, growth and metabolism of five charophyte species and a submerged angiosperm. Aquat Toxicol 144–145:1–10

    Article  Google Scholar 

  • Samal K, Kar S, Trivedi S (2019) Ecological floating bed (EFB) for decontamination of polluted water bodies: design, mechanism and performance. J Environ Manage 251:109550

    Article  CAS  Google Scholar 

  • Santos C, Azevedo J, Campos A, Vasconcelos V, Pereira A (2015) Biochemical and growth performance of the aquatic macrophyte Azolla filiculoides to sub-chronic exposure to cylindrospermopsin. Ecotoxicology 24:1848–1857

    Article  CAS  Google Scholar 

  • Saqrane S, Ghazali IE, Ouahid Y, Hassni ME, Hadrami IE, Bouarab L, del Campo FF, Oudra B, Vasconcelos V (2007) Phytotoxic effects of cyanobacterial extract on the aquatic plant Lemna gibba: microsystin accumulation, detoxication and oxidative stress induction. Aquat Toxicol 83:284–294

    Article  CAS  Google Scholar 

  • Schloss PD, Dirk G, Westcott SL (2013) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS ONE 6:e27310

    Article  Google Scholar 

  • Shan Y, Wang ZF, Luo XZ, Zheng Z (2015) Allelopathic inhibition effect of four aquatic macrophytes on Microcystis aeruginosa growth. Fresen Environ Bull 24(11B):4025–4033

    CAS  Google Scholar 

  • Song J, Li Q, Wang XC (2019) Superposition effect of floating and fixed beds in series for enhancing nitrogen and phosphorus removal in a multistage pond system. Sci Total Environ 695:133678

    Article  CAS  Google Scholar 

  • Svany A, Paskauskas R, Hilt S (2014) Effects of the allelopathically activemacrophyte Myriophyllum spicatum on a natural phytoplankton community: a mesocosm study. Hydrobiologia 737(1):57–66

    Article  Google Scholar 

  • Tsujimoto R, Kotani H, Nonaka A, Miyahara Y, Hiraide Y, Fujita Y (2015) Transformation of the cyanobacterium Leptolyngbya boryana by electroporation. Bio-Protoc 5(24):e1690

    Article  Google Scholar 

  • Ujvárosi AZ, Riba M, Garda T, Gyémánt G, Vereb G, Hamvas MM, Vasas G, Máthé C (2019) Attack of Microcystis aeruginosa bloom on a Ceratophyllum submersum field: ecotoxicological measurements in real environment with real microcystin exposure. Sci Total Environ 662:735–745

    Article  Google Scholar 

  • Vanderstukken M, Declerck SAJ, Decaestecker E, Muylaert K (2014) Long-term allelopathic control of phytoplankton by the submerged macrophyte Elodea nuttallii. Freshwater Biol 59(5):930–941

    Article  Google Scholar 

  • Wang HP, Liu F, Luo P, Li ZH, Zheng LG, Wang H, Zou DS, Wu JS (2017) Allelopathic effects of Myriophyllum aquaticum on two cyanobacteria of Anabaena flos-aquae and Microcystis aeruginosa. B Environ Contam Tox 98:556–561

    Article  CAS  Google Scholar 

  • Wang NY, Wang C (2018) Effects of microcystin-LR on the tissue growth and physiological response of the aquatic plant Iris pseudacorus L. Aquat Toxicol 200:197–205

    Article  CAS  Google Scholar 

  • Wellbum AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

    Article  Google Scholar 

  • Wu F, Ghamkhar R, Ashton W, Hicks AL (2019) Sustainable seafood and vegetable production: aquaponics as a potential opportunity in urban areas. Integr Environ Assess Manag 15(6):832–843

    Article  Google Scholar 

  • Xian QM, Chen HD, Zhou HX, Yin DQ (2007) Allelopathic activity and nutrient competition between Ceratophyllum demersum and Microcystis aeruginosa. Allelopathy J 19(1):227–232

    Google Scholar 

  • Xie B, Wu JX, Huang LF (2019) Temporal and spatial variations of macrofouling organisms on ecological floating beds in Yundang Lagoon, China. Mar Pollut Bull 148:156–167

    Article  CAS  Google Scholar 

  • Yang Z, Lu K, Chen Y, Montagnes DJS (2012) The interactive effects of ammonia and microcystin on life-history traits of the cladoceran Daphnia magna synergistic or antagonistic? PLoS ONE 7(3):e32285

    Article  CAS  Google Scholar 

  • Yu S, Miao C, Song H, Huang YQ, Chen W, He XY (2019) Efficiency of nitrogen and phosphorus removal by six macrophytes from eutrophic water. Int J Phytoremediat 21:643–651

    Article  CAS  Google Scholar 

  • Zhang L, Sun Z, Xie J, Wu J, Cheng SP (2018) Nutrient removal, biomass accumulation and nitrogen-transformation functional gene response to different nitrogen forms in enhanced floating treatment wetlands. Ecol Eng 112:21–25

    Article  Google Scholar 

  • Zhao JG, He FF, Chen ZH, Li HJ, Hu JM, Liu FP (2012) Effect of culture and extract solutions of macrophytes on the growth of three common algae. J Freshw Ecol 27:367–379

    Article  Google Scholar 

  • Zuluaga M, Gueguen V, Pavon-Djavid G, Letourneur D (2017) Carotenoids from microalgae to block oxidative stress. Bioimpacts 7:1–3

    Article  CAS  Google Scholar 

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Funding

This work was financially supported by the Young Backbone Teachers Project of Henan Province (No. 2020GGJS064), the National Nature Science Foundation Project of China (No. 31500380), the Scientific Fund of Henan Normal University (No. 2020QK02), and the Major public welfare projects in Henan Province (No. 201300311300).

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  1. College of Fisheries, Henan Normal University, Xinxiang, Henan, People’s Republic of China, 453007

    Jing Dong, Dujuan Dai, Yue Yang, Feihu Wang, Xuejun Li, Jie Yuan, Yuhuan Chen, Yunni Gao, Man Zhang, Xiaofei Gao, Mei Li & Jingxiao Zhang

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  1. Jing Dong
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  2. Dujuan Dai
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Contributions

Jing Dong: experiments design, data analysis and draft writing; Dujuan Dai: conducting of the experiments; Yue Yang: data analysis and graphing; Feihu Wang, Jie Yuan, and Yuhuan Chen: assistance in the conduction of the experiments; Yunni Gao and Man Zhang: language improvement and reviewing of the original draft; Xiaofei Gao, Mei Li, and Jingxiao Zhang: assistance in microbial community analysis; Xuejun Li: revision and supervision.

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Dong, J., Dai, D., Yang, Y. et al. Responses of submerged macrophyte Ceratophyllum demersum to the gradient concentrations of microcystin-LR (MC-LR). Environ Sci Pollut Res 29, 71257–71269 (2022). https://doi.org/10.1007/s11356-022-20917-4

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