Antibiotic fate in an artificial-constructed urban river planted with the algae Microcystis aeruginosa and emergent hydrophyte
Corresponding Author
Haidong Zhou
School of Environment and Architecture, University of Shanghai for Science and Technology, Shanghai, China
Correspondence
Haidong Zhou, School of Environment and Architecture, University of Shanghai for Science and Technology, No. 516, Jungong Road, Shanghai 200093, China.
Email: zhouhaidong@usst.edu.cn
Contribution: Conceptualization (lead), Funding acquisition (lead), Project administration (lead)
Search for more papers by this authorJinyu Cui
School of Environment and Architecture, University of Shanghai for Science and Technology, Shanghai, China
Contribution: Data curation (equal), Investigation (equal), Validation (equal)
Search for more papers by this authorXin Li
School of Environment and Architecture, University of Shanghai for Science and Technology, Shanghai, China
Contribution: Formal analysis (equal), Investigation (equal), Validation (equal)
Search for more papers by this authorYadan Wangjin
School of communication and Information Engineering, Shanghai Technical Institute of Electronics Information, Shanghai, China
Contribution: Data curation (equal), Investigation (equal)
Search for more papers by this authorLidan Pang
School of Environment and Architecture, University of Shanghai for Science and Technology, Shanghai, China
Contribution: Data curation (equal), Investigation (equal)
Search for more papers by this authorMengwei Li
School of Environment and Architecture, University of Shanghai for Science and Technology, Shanghai, China
Contribution: Investigation (equal), Methodology (equal)
Search for more papers by this authorXiaomeng Chen
School of Environment and Architecture, University of Shanghai for Science and Technology, Shanghai, China
Contribution: Data curation (equal), Investigation (equal)
Search for more papers by this authorCorresponding Author
Haidong Zhou
School of Environment and Architecture, University of Shanghai for Science and Technology, Shanghai, China
Correspondence
Haidong Zhou, School of Environment and Architecture, University of Shanghai for Science and Technology, No. 516, Jungong Road, Shanghai 200093, China.
Email: zhouhaidong@usst.edu.cn
Contribution: Conceptualization (lead), Funding acquisition (lead), Project administration (lead)
Search for more papers by this authorJinyu Cui
School of Environment and Architecture, University of Shanghai for Science and Technology, Shanghai, China
Contribution: Data curation (equal), Investigation (equal), Validation (equal)
Search for more papers by this authorXin Li
School of Environment and Architecture, University of Shanghai for Science and Technology, Shanghai, China
Contribution: Formal analysis (equal), Investigation (equal), Validation (equal)
Search for more papers by this authorYadan Wangjin
School of communication and Information Engineering, Shanghai Technical Institute of Electronics Information, Shanghai, China
Contribution: Data curation (equal), Investigation (equal)
Search for more papers by this authorLidan Pang
School of Environment and Architecture, University of Shanghai for Science and Technology, Shanghai, China
Contribution: Data curation (equal), Investigation (equal)
Search for more papers by this authorMengwei Li
School of Environment and Architecture, University of Shanghai for Science and Technology, Shanghai, China
Contribution: Investigation (equal), Methodology (equal)
Search for more papers by this authorXiaomeng Chen
School of Environment and Architecture, University of Shanghai for Science and Technology, Shanghai, China
Contribution: Data curation (equal), Investigation (equal)
Search for more papers by this authorAbstract
The behavior and removal of six antibiotics, that is, azithromycin, clarithromycin, sulfathiazole, sulfamethoxazole, ciprofloxacin, and tetracycline, in an artificial-controllable urban river (ACUR) were investigated. The ACUR was constructed to form five artificial eco-systems by planting three emergent hydrophytes and Microcystis aeruginosa: (1) Control; (2) MA: M. aeruginosa only; (3) MA-J-C: M. aeruginosa combined with Juncus effusus and Cyperus alternifolius; (4) MA-C-A: M. aeruginosa combined with C. alternifolius and Acorus calamus L.; (5) MA-A-J: M. aeruginosa combined with A. calamus L. and J. effusus. The MA-C-A system achieved the best removal of azithromycin and clarithromycin after 15-day test with the final concentrations 0.92 and 0.83 μg/L. The contents of ciprofloxacin and tetracycline in sediment were highest, up to 1453 and 1745 ng/g. The antibiotic plant bioaccumulation was higher in roots rather than the shoots (stem and leaves). No target antibiotics were detected in algae cells. The combination of hybrid hydrophytes had a certain effect on the removal of antibiotics, and thus selecting appropriate hydrophytes in urban rivers could greatly improve water quality. The overall removal of six antibiotics was greatly improved by the ACUR containing the hybrid hydrophytes and the algae, indicating a synergistic effect on antibiotic removal.
Practitioner points
- Controllable-mobile artificial eco-systems were developed with emergent hydrophytes and M. aeruginosa.
- The M. aeruginosa + Cyperus alternifolius + Acorus calamus L. system removed azithromycin and clarithromycin most at the end of tests.
- Emergent hydrophytes and M. aeruginosa have a synergistic effect on the removal of antibiotics.
- The combination of emergent hydrophytes did play an important role in the removal of antibiotics.
- The artificial eco-systems containing the hybrid hydrophytes and the algae could greatly improve the overall removal of antibiotics.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
REFERENCES
- Abhilash, P. C., Jamil, S., & Singh, N. (2009). Transgenic plants for enhanced biodegradation and phytoremediation of organic xenobiotics. Biotechnology Advances, 27(4), 474–488. https://doi.org/10.1016/j.biotechadv.2009.04.002
- Acuña, V., von Schiller, D., García-Galán, M. J., Rodríguez-Mozaz, S., Corominas, L., Petrovic, M., Poch, M., Barceló, D., & Sabater, S. (2015). Occurrence and in-stream attenuation of wastewater-derived pharmaceuticals in Iberian rivers. Science of the Total Environment, 503–504, 133–141. https://doi.org/10.1016/j.scitotenv.2014.05.067
- Azanu, D., Mortey, C., Darko, G., Weisser, J. J., Styrishave, B., & Abaidoo, R. C. (2016). Uptake of antibiotics from irrigation water by plants. Chemosphere, 157, 107–114. https://doi.org/10.1016/j.chemosphere.2016.05.035
- Blanco, I., Molle, P., Sáenz de Miera, L. E., & Ansola, G. (2016). Basic oxygen furnace steel slag aggregates for phosphorus treatment. Evaluation of its potential use as a substrate in constructed wetlands. Water Research, 89, 355–365. https://doi.org/10.1016/j.watres.2015.11.064
- Boxall, A. B. A., Johnson, P., Smith, E. J., Sinclair, C. J., Stutt, E., & Levy, L. S. (2006). Uptake of veterinary medicines from soils into plants. Journal of Agricultural and Food Chemistry, 54, 2288–2297. https://doi.org/10.1021/jf053041t
- Cardinal, P., Anderson, J. C., Carlson, J. C., Low, J. E., Challis, J. K., Beattie, S. A., Bartel, C. N., Elliott, A. D., Montero, O. F., Lokesh, S., Favreau, A., Kozlova, T. A., Knapp, C. W., Hanson, M. L., & Wong, C. S. (2014). Macrophytes may not contribute significantly to removal of nutrients, pharmaceuticals, and antibiotic resistance in model surface constructed wetlands. Science of the Total Environment, 482–483(1), 294–304. https://doi.org/10.1016/j.scitotenv.2014.02.095
- Chang, X., Meyer, M. T., Liu, X., Zhao, Q., Chen, H., Chen, J. A., Qiu, Z., Yang, L., Cao, J., & Shu, W. (2010). Determination of antibiotics in sewage from hospitals, nursery and slaughter house, wastewater treatment plant and source water in Chongqing region of Three Gorge Reservoir in China. Environmental Pollution, 158(5), 1444–1450. https://doi.org/10.1016/j.envpol.2009.12.034
- Chen, J., Ying, G. G., Wei, X. D., Liu, Y. S., Liu, S. S., Hu, L. X., He, L. Y., Chen, Z. F., Chen, F. R., & Yang, Y. Q. (2016). Removal of antibiotics and antibiotic resistance genes from domestic sewage by constructed wetlands: Effect of flow configuration and plant species. Science of the Total Environment, 571, 974–982. https://doi.org/10.1016/j.scitotenv.2016.07.085
- Chen, K., & Zhou, J. L. (2014). Occurrence and behavior of antibiotics in water and sediments from the Huangpu River, Shanghai, China. Chemosphere, 95, 604–612. https://doi.org/10.1016/j.chemosphere.2013.09.119
- Cui, H., Hense, B. A., Muller, J., & Schroder, P. (2015). Short term uptake and transport process for metformin in roots of Phragmites australis and Typha latifolia. Chemosphere, 134, 307–312. https://doi.org/10.1016/j.chemosphere.2015.04.072
- Cui, H., & Schroder, P. (2016). Uptake, translocation and possible biodegradation of the antidiabetic agent metformin by hydroponically grown Typha latifolia. Journal of Hazardous Materials, 308, 355–361. https://doi.org/10.1016/j.jhazmat.2016.01.054
- Dettenmaier, E. M., Doucette, W. J., & Bugbee, B. (2009). Chemical hydrophobicity and uptake by plant roots. Environmental Science & Technology, 43(2), 324–329. https://doi.org/10.1021/es801751x
- Ding, T., Lin, K., Yang, B., Yang, M., Li, J., Li, W., & Gan, J. (2017). Biodegradation of naproxen by freshwater algae Cymbella sp. and Scenedesmus quadricauda and the comparative toxicity. Bioresource Technology, 238, 164–173. https://doi.org/10.1016/j.biortech.2017.04.018
- Doucette, W. J., Shunthirasingham, C., Dettenmaier, E. M., Zaleski, R. T., Fantke, P., & Arnot, J. A. (2018). A review of measured bioaccumulation data on terrestrial plants for organic chemicals: Metrics, variability, and the need for standardized measurement protocols. Environmental Toxicology and Chemistry, 37, 21–33. https://doi.org/10.1002/etc.3992
- Figueroa, R. A., Leonard, A., & MacKay, A. A. (2004). Modeling tetracycline antibiotic sorption to clays. Environmental Science & Technology, 38(2), 476–483. https://doi.org/10.1021/es0342087
- Garcia-Galan, M. J., Garrido, T., Fraile, J., Ginebreda, A., Diaz-Cruz, M. S., & Barcelo, D. (2011). Application of fully automated online solid phase extraction-liquid chromatography-electrospray-tandem mass spectrometry for the determination of sulfonamides and their acetylated metabolites in groundwater. Analytical and Bioanalytical Chemistry, 399(2), 795–806. https://doi.org/10.1007/s00216-010-4367-3
- Göbel, A., McArdell, C. S., Joss, A., Siegrist, H., & Giger, W. (2007). Fate of sulfonamides, macrolides, and trimethoprim in different wastewater treatment technologies. Science of the Total Environment, 372(2–3), 361–371. https://doi.org/10.1016/j.scitotenv.2006.07.039
- Hao, R., Zhao, R., Qiu, S., Wang, L., & Song, H. (2015). Antibiotics crisis in China. Science, 348(6239), 1100–1101. https://doi.org/10.1126/science.348.6239.1100-d
- Herklotz, P. A., Gurung, P., Vanden Heuvel, B., & Kinney, C. A. (2010). Uptake of human pharmaceuticals by plants grown under hydroponic conditions. Chemosphere, 78(11), 1416–1421. https://doi.org/10.1016/j.chemosphere.2009.12.048
- Hijosa-Valsero, M., Fink, G., Schlüsener, M. P., Sidrach-Cardona, R., Martín-Villacorta, J., Ternes, T., & Bécares, E. (2011). Removal of antibiotics from urban wastewater by constructed wetland optimization. Chemosphere, 83(5), 713–719. https://doi.org/10.1016/j.chemosphere.2011.02.004
- Hu, Y., Jiang, L., Sun, X., Wu, J., Ma, L., Zhou, Y., Lin, K., Luo, Y., & Cui, C. (2021). Risk assessment of antibiotic resistance genes in the drinking water system. Science of the Total Environment, 800, 149650. https://doi.org/10.1016/j.scitotenv.2021.149650
- Hu, Y., Jin, L., Zhao, Y., Jiang, L., Yao, S., Zhou, W., Lin, K., & Cui, C. (2021). Annual trends and health risks of antibiotics and antibiotic resistance genes in a drinking water source in East China. Science of the Total Environment, 791, 148152. https://doi.org/10.1016/j.scitotenv.2021.148152
- Huang, C.-H., Renew, J. E., Smeby, K. L., Pinkston, K., & Sedlak, D. L. (2011). Assessment of potential antibiotic contaminants in water and preliminary occurrence analysis. Journal of Contemporary Water Research and Education, 120(1), 30–40.
- Imfeld, G., Braeckevelt, M., Kuschk, P., & Richnow, H. H. (2009). Monitoring and assessing processes of organic chemicals removal in constructed wetlands. Chemosphere, 74(3), 349–362. https://doi.org/10.1016/j.chemosphere.2008.09.062
- Kumar, R. R., Lee, J. T., & Cho, J. Y. (2012). Fate, occurrence, and toxicity of veterinary antibiotics in environment. Journal of the Korean Society for Applied Biological Chemistry, 55(6), 701–709. https://doi.org/10.1007/s13765-012-2220-4
- Li, D., Zhou, H., Huang, L., Zhang, J., Cui, J., & Li, X. (2021). Role of adsorption during nanofiltration of sulfamethoxazole and azithromycin solution. Separation Science and Technology, 56(12), 1996–2010. https://doi.org/10.1080/01496395.2020.1806326
- Li, G., Zhai, J., He, Q., Zhi, Y., Xiao, H., & Rong, J. (2014). Phytoremediation of levonorgestrel in aquatic environment by hydrophytes. Journal of Environmental Sciences, 26(9), 1869–1873. https://doi.org/10.1016/j.jes.2014.06.030
- Li, S., Shi, W., You, M., Zhang, R., Kuang, Y., Dang, C., Sun, W., Zhou, Y., Wang, W., & Ni, J. (2019). Antibiotics in water and sediments of Danjiangkou Reservoir, China: Spatiotemporal distribution and indicator screening. Environmental Pollution, 246, 435–442. https://doi.org/10.1016/j.envpol.2018.12.038
- Li, X.-N., Song, H.-L., Li, W., Lu, X.-W., & Nishimura, O. (2010). An integrated ecological floating-bed employing plant, freshwater clam and biofilm carrier for purification of eutrophic water. Ecological Engineering, 36(4), 382–390. https://doi.org/10.1016/j.ecoleng.2009.11.004
- Lindberg, R. H., Wennberg, P., Johansson, M. I., Tysklind, M., & Andersson, B. A. V. (2005). Screening of human antibiotic substances and determination of weekly mass flows in five sewage treatment plants in Sweden. Environmental Science & Technology, 39(10), 3421–3429. https://doi.org/10.1021/es048143z
- Liu, L., Liu, Y. H., Liu, C. X., Wang, Z., Dong, J., Zhu, G. F., & Huang, X. (2013). Potential effect and accumulation of veterinary antibiotics in Phragmites australis under hydroponic conditions. Ecological Engineering, 53, 138–143. https://doi.org/10.1016/j.ecoleng.2012.12.033
- Liu, L., Liu, Y. H., Wang, Z., Liu, C. X., Huang, X., & Zhu, G. F. (2014). Behavior of tetracycline and sulfamethazine with corresponding resistance genes from swine wastewater in pilot-scale constructed wetlands. Journal of Hazardous Materials, 278, 304–310. https://doi.org/10.1016/j.jhazmat.2014.06.015
- Liu, Y., Wang, Z., Yan, K., Wang, Z., Torres, O. L., Guo, R., & Chen, J. (2017). A new disposal method for systematically processing of ceftazidime: The intimate coupling UV/algae-algae treatment. Chemical Engineering Journal, 314, 152–159. https://doi.org/10.1016/j.cej.2016.12.110
- Lu, B., Xu, Z., Li, J., & Chai, X. (2018). Removal of water nutrients by different aquatic plant species: An alternative way to remediate polluted rural rivers. Ecological Engineering, 110, 18–26. https://doi.org/10.1016/j.ecoleng.2017.09.016
- Lu, X., Gao, Y., Luo, J., Yan, S., Rengel, Z., & Zhang, Z. (2014). Interaction of veterinary antibiotic tetracyclines and copper on their fates in water and water hyacinth (Eichhornia crassipes). Journal of Hazardous Materials, 280, 389–398. https://doi.org/10.1016/j.jhazmat.2014.08.022
- Osińska, A., Korzeniewska, E., Harnisz, M., Felis, E., Bajkacz, S., Jachimowicz, P., Niestępski, S., & Konopka, I. (2020). Small-scale wastewater treatment plants as a source of the dissemination of antibiotic resistance genes in the aquatic environment. Journal of Hazardous Materials, 381, 121221. https://doi.org/10.1016/j.jhazmat.2019.121221
- Paul, T., Miller, P. L., & Strathmann, T. J. (2007). Visible-light-mediated TiO2 photocatalysis of fluoroquinolone antibacterial agents. Environmental Science & Technology, 41(13), 4720–4727. https://doi.org/10.1021/es070097q
- Pérez, D. J., Doucette, W. J., & Moore, M. T. (2022). Atrazine uptake, translocation, bioaccumulation and biodegradation in cattail (Typha latifolia) as a function of exposure time. Chemosphere, 287, 132104. https://doi.org/10.1016/j.chemosphere.2021.132104
- Pilon-Smits, E. (2005). Phytoremediation. Annual Review of Plant Biology, 56, 15–39. https://doi.org/10.1146/annurev.arplant.56.032604.144214
- Schnoor, J. L., Licht, L. A., McCutcheon, S. C., Wolfe, N. L., & Carreira, L. H. (1995). Phytoremediation of organic and nutrient contaminants. Environmental Science & Technology, 29(7), 318A–323A. https://doi.org/10.1021/es00007a747
- Shenker, M., Harush, D., Ben-Ari, J., & Chefetz, B. (2011). Uptake of carbamazepine by cucumber plants—A case study related to irrigation with reclaimed wastewater. Chemosphere, 82(6), 905–910. https://doi.org/10.1016/j.chemosphere.2010.10.052
- Sun, H., Xu, J., Yang, S., Liu, G., & Dai, S. (2004). Plant uptake of aldicarb from contaminated soil and its enhanced degradation in the rhizosphere. Chemosphere, 54(4), 569–574. https://doi.org/10.1016/s0045-6535(03)00722-7
- Tolls, J. (2001). Sorption of veterinary pharmaceuticals in soils: A review. Environmental Science & Technology, 35(17), 3397–3406. https://doi.org/10.1021/es0003021
- Topp, E., Renaud, J., Sumarah, M., & Sabourin, L. (2016). Reduced persistence of the macrolide antibiotics erythromycin, clarithromycin and azithromycin in agricultural soil following several years of exposure in the field. Science of the Total Environment, 562, 136–144. https://doi.org/10.1016/j.scitotenv.2016.03.210
- Truu, M., Juhanson, J., & Truu, J. (2009). Microbial biomass, activity and community composition in constructed wetlands. Science of the Total Environment, 407(13), 3958–3971. https://doi.org/10.1016/j.scitotenv.2008.11.036
- Vermaat, J. E., & Hanif, M. K. (1998). Performance of common duckweed species (Lemnaceae) and the waterfern Azolla filiculoides on different types of wastewater. Water Research, 32(9), 2569–2576.
- Wu, C., Spongberg, A. L., Witter, J. D., Fang, M., & Czajkowski, K. P. (2010). Uptake of pharmaceutical and personal care products by soybean plants from soils applied with biosolids and irrigated with contaminated water. Environmental Science and Technology, 44, 6157–6161. https://doi.org/10.1021/es1011115
- Wu, S., Kuschk, P., Brix, H., Vymazal, J., & Dong, R. (2014). Development of constructed wetlands in performance intensifications for wastewater treatment: A nitrogen and organic matter targeted review. Water Research, 57, 40–55. https://doi.org/10.1016/j.watres.2014.03.020
- Yamamoto, H., Nakamura, Y., Moriguchi, S., Nakamura, Y., Honda, Y., Tamura, I., Hirata, Y., Hayashi, A., & Sekizawa, J. (2009). Persistence and partitioning of eight selected pharmaceuticals in the aquatic environment: Laboratory photolysis, biodegradation, and sorption experiments. Water Research, 43(2), 351–362. https://doi.org/10.1016/j.watres.2008.10.039
- Zhou, H., Chen, X., Liu, X., Xuan, Y., & Hu, T. (2019). Effects and control of metal nutrients and species on Microcystis aeruginosa growth and bloom. Water Environment Research, 91(1), 21–31. https://doi.org/10.2175/106143017X15131012188303
- Zhou, H., Liu, X., Chen, X., Ying, T., & Ying, Z. (2018). Characteristics of removal of waste-water marking pharmaceuticals with typical hydrophytes in the urban rivers. Science of the Total Environment, 636, 1291–1302. https://doi.org/10.1016/j.scitotenv.2018.04.384
- Zhou, H., Ying, T., Wang, X., & Liu, J. (2016). Occurrence and preliminarily environmental risk assessment of selected pharmaceuticals in the urban rivers, China. Scientific Reports, 6(1), 34928. https://doi.org/10.1038/srep34928
- Zhou, H., Zhang, Q., Wang, X., Zhang, Q., Ma, L., & Zhan, Y. (2014). Systematic screening of common wastewater-marking pharmaceuticals in urban aquatic environments: Implications for environmental risk control. Environmental Science and Pollution Reseach, 21(11), 7113–7129. https://doi.org/10.1007/s11356-014-2622-4
- Zhou, Q., He, F., Liping, Z., Wang, Y., & Wu, Z. (2009). Characteristics of the microbial communities in the integrated vertical-flow constructed wetlands. Journal of Environmental Sciences, 21(9), 1261–1267. https://doi.org/10.1016/s1001-0742(08)62413-4
- Zorita, S., Martensson, L., & Mathiasson, L. (2009). Occurrence and removal of pharmaceuticals in a municipal sewage treatment system in the south of Sweden. Science of the Total Environment, 407(8), 2760–2770. https://doi.org/10.1016/j.scitotenv.2008.12.030
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© 2021 Water Environment Federation
Research funding
- USST Program of Science and Technology Development. Grant Number: 2018KJFZ117
- Natural Science Foundation of Shanghai, China. Grant Number: 18ZR1426100
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Publication History
- 05 January 2022
- 05 January 2022
- 02 December 2021
- 23 November 2021
- 25 October 2021
- 23 June 2021