Abstract
Utilizing the allelopathic effect of plants to inhibit algae growth has gained significant attention from researchers in recent years. However, there are large amounts of microplastics in the aquatic environment, which may influence the inhibitory effects of allelochemicals on algae. Consequently, this research aimed to examine the individual and combined toxicity of gallic acid (GA) and polyethylene glycol terephthalate (PET) microplastics on Microcystis aeruginosa. At a concentration of 50 mg/L, PET significantly enhanced algal cell growth and chlorophyll a synthesis, while inducing oxidative stress without damaging the cell membrane. On the other hand, low concentrations of GA promote algal cell growth. However, high concentrations of GA not only inhibit growth and photosynthesis but also result in cellular abnormalities and severe oxidative damage, as well as membrane disruption. Moreover, it was observed that the exposure of PET diminished the toxicity of GA to M. aeruginosa. The combined exposure to GA and PET resulted in a slight increase in chlorophyll a content, as well as phycocyanin (PC), alloxyphycocyanin (APC), and phycoerythrin (PE) content, along with maximum photochemical efficiency (Fv/Fm), compared to GA exposure alone. In the combined system of GA and PET, the contents of superoxide dismutase (SOD) and malondialdehyde (MDA) were lower than those in the single GA system. Additionally, both systems showed a degree of improvement compared to the control group. Scanning electron microscopy (SEM) observed that the presence of PET resulted in reduced damage to algal cells compared to exposure to GA alone. This research establishes a foundation for understanding the synergistic impacts of allelochemicals and microplastics on M. aeruginosa, thereby providing a reference for managing cyanobacteria in water blooms.
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References
Agathokleous, E., Peñuelas, J., Azevedo, R. A., Rillig, M. C., Sun, H., & Calabrese, E. J. (2022). Low levels of contaminants stimulate harmful algal organisms and enrich their toxins. Environmental Science & Technology, 56, 11991–12002. https://doi.org/10.1021/acs.est.2c02763
Arnon, D. I. (1949). Copper enzymes in isolated chloroplasts-polyphenoloxidase in beta vulgaris. Plant Physiology, 24, 1–15. https://doi.org/10.1104/pp.24.1.1
Bhatt, P., Engel, B. A., Reuhs, M., & Simsek, H. (2023). Cyanophage technology in removal of cyanobacteria mediated harmful algal blooms: A novel and eco-friendly method. Chemosphere, 315, 137769. https://doi.org/10.1016/j.chemosphere.2023.137769
Canniff, P. M., & Hoang, T. C. (2018). Microplastic ingestion by Daphnia magna and its enhancement on algal growth. Science of The Total Environment, 633, 500–507. https://doi.org/10.1016/j.scitotenv.2018.03.176
Chae, Y., Kim, D., & An, Y.-J. (2019). Effects of micro-sized polyethylene spheres on the marine microalga Dunaliella salina: Focusing on the algal cell to plastic particle size ratio. Aquatic Toxicology, 216, 105296. https://doi.org/10.1016/j.aquatox.2019.105296
Chavan, P., Kumar, R., Kirubagaran, R., & Venugopalan, V. P. (2017). Comparative toxicological effects of two antifouling biocides on the marine diatom Chaetoceros lorenzianus: Damage and post-exposure recovery. Ecotoxicology and Environmental Safety, 144, 97–106. https://doi.org/10.1016/j.ecoenv.2017.06.001
Cheng, R., Hou, S., Wang, J., Zhu, H., Shutes, B., & Yan, B. (2022). Biochar-amended constructed wetlands for eutrophication control and microcystin (MC-LR) removal. Chemosphere, 295, 133830. https://doi.org/10.1016/j.chemosphere.2022.133830
Cole, M., Lindeque, P., Fileman, E., Halsband, C., Goodhead, R., Moger, J., & Galloway, T. S. (2013). Microplastic ingestion by zooplankton. Environmental Science & Technology, 47, 6646–6655. https://doi.org/10.1021/es400663f
Ding, J., Huang, Y., Liu, S., Zhang, S., Zou, H., Wang, Z., Zhu, W., & Geng, J. (2020). Toxicological effects of nano- and micro-polystyrene plastics on red tilapia: Are larger plastic particles more harmless? Journal of Hazardous Materials, 396, 122693. https://doi.org/10.1016/j.jhazmat.2020.122693
Dong, J., Kang, Y., Kuang, S., Ma, H., Li, M., Xiao, J., Wang, Y., Guo, Z., & Wu, H. (2023). Combined biological effects of polystyrene microplastics and phenanthrene on Tubifex tubifex and microorganisms in wetland sediment. Chemical Engineering Journal, 462, 142260. https://doi.org/10.1016/j.cej.2023.142260
Feng, S., Lu, H., Tian, P., Xue, Y., Lu, J., Tang, M., & Feng, W. (2020). Analysis of microplastics in a remote region of the Tibetan Plateau: Implications for natural environmental response to human activities. Science of The Total Environment, 739, 140087. https://doi.org/10.1016/j.scitotenv.2020.140087
Ferreira, P., Fonte, E., Soares, M. E., Carvalho, F., & Guilhermino, L. (2016). Effects of multi-stressors on juveniles of the marine fish Pomatoschistus microps: Gold nanoparticles, microplastics and temperature. Aquatic Toxicology, 170, 89–103. https://doi.org/10.1016/j.aquatox.2015.11.011
Fossi, M. C., Marsili, L., Baini, M., Giannetti, M., Coppola, D., Guerranti, C., Caliani, I., Minutoli, R., Lauriano, G., Finoia, M. G., Rubegni, F., Panigada, S., Bérubé, M., Urbán Ramírez, J., & Panti, C. (2016). Fin whales and microplastics: The Mediterranean Sea and the Sea of Cortez scenarios. Environmental Pollution, 209, 68–78. https://doi.org/10.1016/j.envpol.2015.11.022
Gedik, K., & Eryaşar, A. R. (2020). Microplastic pollution profile of Mediterranean mussels (Mytilus galloprovincialis) collected along the Turkish coasts. Chemosphere, 260, 127570. https://doi.org/10.1016/j.chemosphere.2020.127570
Gil, C. S., & Eom, S. H. (2023). Two different anti-algal control mechanisms in Microcystis aeruginosa induced by robinin or tannin rich plants. Chemosphere, 323, 138202. https://doi.org/10.1016/j.chemosphere.2023.138202
Grobe, C. W., & Murphy, T. M. (1998). Solar ultraviolet-B radiation effects on growth and pigment composition of the intertidal alga Ulva expansa (Setch.) S. & G. (Chlorophyta). Journal of Experimental Marine Biology and Ecology, 225, 39–51. https://doi.org/10.1016/S0022-0981(97)00210-4
Hao, B., Wu, H., Zhang, S., & He, B. (2022). Individual and combined toxicity of microplastics and diuron differs between freshwater and marine diatoms. Science of The Total Environment, 853, 158334. https://doi.org/10.1016/j.scitotenv.2022.158334
Ivy, N., Bhattacharya, S., Dey, S., Gupta, K., Dey, A., & Sharma, P. (2023). Effects of microplastics and arsenic on plants: Interactions, toxicity and environmental implications. Chemosphere, 338, 139542. https://doi.org/10.1016/j.chemosphere.2023.139542
Jin, P., Wang, H., Huang, W., Liu, W., Fan, Y., & Miao, W. (2018). The allelopathic effect and safety evaluation of 3,4-dihydroxybenzalacetone on Microcystis aeruginosa. Pesticide Biochemistry and Physiology, 147, 145–152. https://doi.org/10.1016/j.pestbp.2017.08.011
Kibuye, F. A., Zamyadi, A., & Wert, E. C. (2021). A critical review on operation and performance of source water control strategies for cyanobacterial blooms: Part II-mechanical and biological control methods. Harmful Algae, 109, 102119. https://doi.org/10.1016/j.hal.2021.102119
Kong, Y., Peng, Y., Zhang, Z., Zhang, M., Zhou, Y., & Duan, Z. (2019). Removal of Microcystis aeruginosa by ultrasound: Inactivation mechanism and release of algal organic matter. Ultrasonics Sonochemistry, 56, 447–457. https://doi.org/10.1016/j.ultsonch.2019.04.017
Long, M., Paul-Pont, I., Hégaret, H., Moriceau, B., Lambert, C., Huvet, A., & Soudant, P. (2017). Interactions between polystyrene microplastics and marine phytoplankton lead to species-specific hetero-aggregation. Environmental Pollution, 228, 454–463. https://doi.org/10.1016/j.envpol.2017.05.047
Lusher, A. L., Hernandez-Milian, G., O’Brien, J., Berrow, S., O’Connor, I., & Officer, R. (2015). Microplastic and macroplastic ingestion by a deep diving, oceanic cetacean: The True’s beaked whale Mesoplodon mirus. Environmental Pollution, 199, 185–191. https://doi.org/10.1016/j.envpol.2015.01.023
Mohan, H., Vadivel, S., & Rajendran, S. (2022). Removal of harmful algae in natural water by semiconductor photocatalysis- A critical review. Chemosphere, 302, 134827. https://doi.org/10.1016/j.chemosphere.2022.134827
Nakai, S., Inoue, Y., Hosomi, M., & Murakami, A. (2000). Myriophyllum spicatum-released allelopathic polyphenols inhibiting growth of blue-green algae Microcystis aeruginosa. Water Research, 34, 3026–3032. https://doi.org/10.1016/S0043-1354(00)00039-7
Padgett, M. P., & Krogmann, D. W. (1987). Large scale preparation of pure phycobiliproteins. Photosynthesis Research, 11, 225–235. https://doi.org/10.1007/BF00055062
Podbielska, M., & Szpyrka, E. (2023). Microplastics – An emerging contaminants for algae. Critical review and perspectives. Science of The Total Environment, 885, 163842. https://doi.org/10.1016/j.scitotenv.2023.163842
Qin, B., Zhang, Y., Zhu, G., & Gao, G. (2023). Eutrophication control of large shallow lakes in China. Science of The Total Environment, 881, 163494. https://doi.org/10.1016/j.scitotenv.2023.163494
Qu, H., Ma, R., Wang, B., Yang, J., Duan, L., & Yu, G. (2019). Enantiospecific toxicity, distribution and bioaccumulation of chiral antidepressant venlafaxine and its metabolite in loach (Misgurnus anguillicaudatus) co-exposed to microplastic and the drugs. Journal of Hazardous Materials, 370, 203–211. https://doi.org/10.1016/j.jhazmat.2018.04.041
Samsonoff, W. A., & MacColl, R. (2001). Biliproteins and phycobilisomes from cyanobacteria and red algae at the extremes of habitat. Archives of Microbiology, 176, 400–405. https://doi.org/10.1007/s002030100346
Sha, J., Xiong, H. Y., Li, C. J., Lu, Z. Y., Zhang, J. C., Zhong, H., Zhang, W., & Yan, B. (2021). Harmful algal blooms and their eco-environmental indication. Chemosphere, 274, 129912. https://doi.org/10.1016/j.chemosphere.2021.129912
Song, C., Liu, Z., Wang, C., Li, S., & Kitamura, Y. (2020). Different interaction performance between microplastics and microalgae: The bio-elimination potential of Chlorella sp. L38 and Phaeodactylum tricornutum MASCC-0025. Science of The Total Environment, 723, 138146. https://doi.org/10.1016/j.scitotenv.2020.138146
Sun, S., Hu, S., Zhang, B., Sun, X., & Xu, N. (2021). Allelopathic effects and potential allelochemical of Sargassum fusiforme on red tide microalgae Heterosigma akashiwo. Marine Pollution Bulletin, 170, 112673. https://doi.org/10.1016/j.marpolbul.2021.112673
Suresh, K., Tang, T., van Vliet, M. T. H., Bierkens, M. F. P., Strokal, M., Sorger-Domenigg, F., & Wada, Y. (2023). Recent advancement in water quality indicators for eutrophication in global freshwater lakes. Environmental Research Letters, 18, 063004. https://doi.org/10.1088/1748-9326/acd071
Tao, Y., Mao, X., Hu, J., Mok, H. O. L., Wang, L., Au, D. W. T., Zhu, J., & Zhang, X. (2013). Mechanisms of photosynthetic inactivation on growth suppression of Microcystis aeruginosa under UV-C stress. Chemosphere, 93, 637–644. https://doi.org/10.1016/j.chemosphere.2013.06.031
Techer, D., Fontaine, P., Personne, A., Viot, S., & Thomas, M. (2016). Allelopathic potential and ecotoxicity evaluation of gallic and nonanoic acids to prevent cyanobacterial growth in lentic systems: A preliminary mesocosm study. Science of The Total Environment, 547, 157–165. https://doi.org/10.1016/j.scitotenv.2015.12.164
Wang, F., Zhao, W., Chen, J., & Zhou, Y. (2022). Allelopathic inhibitory effect on the growth of Microcystis aeruginosa by improved ultrasonic-cellulase extract of Vallisneria. Chemosphere, 298, 134245. https://doi.org/10.1016/j.chemosphere.2022.134245
Wang, Q., Liu, W. T., Zeb, A., Lian, Y. H., Shi, R. Y., Li, J. T., & Zheng, Z. Q. (2023). Toxicity effects of polystyrene nanoplastics and arsenite on Microcystis aeruginosa. Science of The Total Environment, 874, 162496. https://doi.org/10.1016/j.scitotenv.2023.162496
Xie, L., Ma, Z., Yang, G., Huang, Y., Wen, T., Deng, Y., Sun, J., Zheng, S., Wu, F., Huang, K., & Shao, J. (2023). Study on the inhibition mechanism of eucalyptus tannins against Microcystis aeruginosa. Ecotoxicology and Environmental Safety, 249, 114452. https://doi.org/10.1016/j.ecoenv.2022.114452
Xue, Y.-H., Sun, Z.-X., Feng, L.-S., Jin, T., Xing, J.-C., & Wen, X.-L. (2021). Algal density affects the influences of polyethylene microplastics on the freshwater rotifer Brachionus calyciflorus. Chemosphere, 270, 128613. https://doi.org/10.1016/j.chemosphere.2020.128613
Ya-Li, G., Hai-Yan, F., Guo-He, H., Pan-Feng, G., Tian, C., Bin, Y., & Huan, L. (2013). Allelopathy effects of ferulic acid and coumarin on Microcystis aeruginosa. Environmental Science, 34(04), 1492–1497. https://doi.org/10.13227/j.hjkx.2013.04.001
Yang, W., Gao, X., Wu, Y., Wan, L., Tan, L., Yuan, S., Ding, H., & Zhang, W. (2020). The combined toxicity influence of microplastics and nonylphenol on microalgae Chlorella pyrenoidosa. Ecotoxicology and Environmental Safety, 195, 110484. https://doi.org/10.1016/j.ecoenv.2020.110484
Yang, X., Man, Y. B., Wong, M. H., Owen, R. B., & Chow, K. L. (2022). Environmental health impacts of microplastics exposure on structural organization levels in the human body. Science of The Total Environment, 825, 154025. https://doi.org/10.1016/j.scitotenv.2022.154025
Yokota, K., Waterfield, H., Hastings, C., Davidson, E., Kwietniewski, E., & Wells, B. (2017). Finding the missing piece of the aquatic plastic pollution puzzle: Interaction between primary producers and microplastics. Limnology and Oceanography Letters, 2, 91–104. https://doi.org/10.1002/lol2.10040
Zhang, X., Li, Y., Ouyang, D., Lei, J., Tan, Q., Xie, L., Li, Z., Liu, T., Xiao, Y., Farooq, T. H., Wu, X., Chen, L., & Yan, W. (2021). Systematical review of interactions between microplastics and microorganisms in the soil environment. Journal of Hazardous Materials, 418, 126288. https://doi.org/10.1016/j.jhazmat.2021.126288
Zhang, H., Li, X., Wu, D., Yu, B., Lu, S., Wang, J., & Ding, J. (2023). A novel strategy for efficient capture of intact harmful algal cells using Zinc oxide modified carbon nitride composites. Algal Research, 69, 102932. https://doi.org/10.1016/j.algal.2022.102932
Zhang, X.-L., Zhu, Q.-Q., Chen, C.-Y., Xie, B., Tang, B.-G., Fan, M.-H., Hu, Q.-J., Liao, Z., & Yan, X.-J. (2023). The growth inhibitory effects and non-targeted metabolomic profiling of Microcystis aeruginosa treated by Scenedesmus sp. Chemosphere, 338, 139446. https://doi.org/10.1016/j.chemosphere.2023.139446
Zhang, C., Lin, X. X., Gao, P. P., Zhao, X., Ma, C. C., Wang, L., Sun, H. W., Sun, L., & Liu, C. G. (2023). Combined effects of microplastics and excess boron on Microcystis aeruginosa. Science of The Total Environment, 891, 164298. https://doi.org/10.1016/j.scitotenv.2023.164298
Zhao, F., Chu, H., Yu, Z., Jiang, S., Zhao, X., Zhou, X., & Zhang, Y. (2017). The filtration and fouling performance of membranes with different pore sizes in algae harvesting. Science of The Total Environment, 587–588, 87–93. https://doi.org/10.1016/j.scitotenv.2017.02.035
Zhao, Z. H., Jun-Qing, Z. I., Huang, B. S., & Branch, N. D. (2018). preliminary study on algae removal test of plant flocculants in Erhai lake. Environmental Science Survey, 37, 15–16. https://doi.org/10.13623/j.cnki.hkdk.2018.01.006
Zhu, Z., Liu, Y., Zhang, P., Zeng, G., Hu, X., Li, H., Guo, Y., & Guo, X. (2014). Co-culture with Cyperus alternifolius induces physiological and biochemical inhibitory effects in Microcystis aeruginosa. Biochemical Systematics and Ecology, 56, 118–124. https://doi.org/10.1016/j.bse.2014.05.008
Zhu, X., Dao, G., Tao, Y., Zhan, X., & Hu, H. (2021). A review on control of harmful algal blooms by plant-derived allelochemicals. Journal of Hazardous Materials, 401, 123403. https://doi.org/10.1016/j.jhazmat.2020.123403
Zhuang, S., & Wang, J. (2023). Interaction between antibiotics and microplastics: Recent advances and perspective. Science of The Total Environment, 897, 165414. https://doi.org/10.1016/j.scitotenv.2023.165414
Zuo, S., Zhou, S., Ye, L., & Ma, S. (2016). Synergistic and antagonistic interactions among five allelochemicals with antialgal effects on bloom-forming Microcystis aeruginosa. Ecological Engineering, 97, 486–492. https://doi.org/10.1016/j.ecoleng.2016.10.013
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This work was supported by the Postgraduate Research & Practice Innovation Program of Jiangsu Province (SJCX22_1571).
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All authors contributed to the study’s conception and design. Haicheng Liu, the corresponding author, provided research ideas, obtained funding, and critically revised the work. The first draft of the manuscript was written by Tiantian Wang, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Wang, T., Liu, H. Effects of PET and Gallic Acid on Growth, Photosynthesis, and Oxidative Stress of Microcystis aeruginosa. Water Air Soil Pollut 235, 158 (2024). https://doi.org/10.1007/s11270-024-06970-4
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DOI: https://doi.org/10.1007/s11270-024-06970-4