Abstract
The environmental fate and toxic effects of antibiotics such as tetracycline (TC) could be influenced by the ubiquitous dissolved organic matter (DOM). However, DOM from different origins has different hydrophilic and hydrophobic properties. It is still unknown the effects of hydrophilic and hydrophobic DOM on the toxic effect of TC. In this study, DOM with hydrophilicity and hydrophobicity was separated and used to investigate their roles in affecting TC toxicity to the photosynthesis of green algae Chlorella vulgaris. Results showed that 10 mg L−1 TC inhibited the efficiency of photosystem II (PSII) of C. vulgaris using light by hindering electron transfer from QA− to QB/QB−, and the O2 release rate of C. vulgaris decreased by a third after 12-h treatment of 10 mg L−1 TC, while both hydrophilic and hydrophobic DOM (20 mg L−1 TOC) alleviated TC toxicity to the photosynthesis of C. vulgaris. In the presence of hydrophilic or hydrophobic DOM, stable complex of TC-hydrophilic DOM or TC-hydrophobic DOM was formed immediately, due to the good affinity of both DOM for TC. Fourier transform infrared spectroscopy result showed that both hydrophilic and hydrophobic DOM could reduce C=O in TC to C–O, and isothermal titration calorimetry result suggested that reactions of both DOM with TC were exothermic (△H < 0) and spontaneous (△G < 0). Thereinto, the reaction constant (Ka) of TC reacting with hydrophobic DOM (Ka=9.70) was higher than that with hydrophilic DOM (Ka=8.93), indicating hydrophobic DOM with more chemical binding sites and accessible fractions for TC. The present study suggests that DOM, especially the hydrophobic DOM, is an important consideration in the environmental impact assessment of antibiotics.
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References
Cady C, Crabtree R, Brudvig G (2008) Functional models for the oxygen-evolving complex of photosystem II. Coord Chem Rev 252:444–455
Cai X, ThomasArrigo LK, Fang X, Bouchet S, Cui Y, Kretzschmar R (2021) Impact of organic matter on microbially-mediated reduction and mobilization of arsenic and iron in arsenic(V)-bearing ferrihydrite. Environ Sci Technol 55:1319–1328
Chen W, Westerhoff P, Leenheer JA, Booksh K (2003) Fluorescence excitation-emission matrix regional integration to quantify spectra for dissolved organic matter. Environ Sci Technol 37:5701–5710
Chen G, Lin C, Chen L, Yang H (2010) Effect of size-fractionation dissolved organic matter on the mobility of prometryne in soil. Chemosphere 79:1046–1055
Chen Z, Zhang Y, Gao Y, Boyd SA, Zhu D, Li H (2015) Influence of dissolved organic matter on tetracycline bioavailability to an antibiotic-resistant bacterium. Environ Sci Technol 49:10903–10910
Deng CN, Zhang DY, Pan XL (2014) Toxic effects of erythromycin on photosystem I and II in Microcystis aeruginosa. Photosynthetica 52:574–580
Ding F, Zhao G, Chen S, Liu F, Sun Y, Zhang L (2009) Chloramphenicol binding to human serum albumin: determination of binding constants and binding sites by steady-state fluorescence. J Mol Struct 929:159–166
Ding Y, Teppen BJ, Boyd SA, Li H (2013) Measurement of associations of pharmaceuticals with dissolved humic substances using solid phase extraction. Chemosphere 91:314–319
Fu Q, Long C, Qin L, Jiang Z, Qing T, Zhang P, Feng B (2021) Fluorescent and colorimetric dual-mode detection of tetracycline in wastewater based on heteroatoms-doped reduced state carbon dots. Environ Pollut 283:117109
Gehlen MH (2020) The centenary of the Stern-Volmer equation of fluorescence quenching: from the single line plot to the SV quenching map. J Photochem Photobiol C 42:100338
González-Pleiter M, Gonzalo S, Rodea-Palomares I, Leganés F, Rosal R, Boltes K, Marco E, Fernández-Piñas F (2013) Toxicity of five antibiotics and their mixtures towards photosynthetic aquatic organisms: implications for environmental risk assessment. Water Res 47:2050–2064
Huang W, Zhang SB, Cao KF (2010) Stimulation of cyclic electron flow during recovery after chilling-induced photoinhibition of PSII. Plant Cell Physiol 51:1922–1928
Kulikova NA, Perminova IV (2002) Binding of atrazine to humic substances from soil, peat, and coal related to their structure. Environ Sci Technol 36:3720–3724
Kümmerer K (2009) Antibiotics in the aquatic environment–a review–Part II. Chemosphere 75:435–441
Kurek MR, Poulin BA, McKenna AM, Spencer RGM (2020) Deciphering dissolved organic matter: ionization, dopant, and fragmentation insights via fourier transform-ion cyclotron resonance mass spectrometry. Environ Sci Technol 54:16249–16259
Ma Z, Liu J, Li H, Zhang W, Williams MA, Gao Y, Gudda FO, Lu C, Yang B, Waigi MG (2019) A fast and easily parallelizable biosensor method for measuring extractable tetracyclines in soils. Environ Sci Technol 54:758–767
Ocampo-Pérez R, Rivera-Utrilla J, Gómez-Pacheco C, Sánchez-Polo M, López-Peñalver JJ (2012) Kinetic study of tetracycline adsorption on sludge-derived adsorbents in aqueous phase. Chem Eng J 213:88–96
Ohore OE, Zhang S, Guo S, Manirakiza B, Addo FG, Zhang W (2021) The fate of tetracycline in vegetated mesocosmic wetlands and its impact on the water quality and epiphytic microbes. J Hazard Mater 417:126148
Ouyang S, Hu X, Zhou Q, Li X, Miao X, Zhou R (2018) Nanocolloids in natural water: isolation, characterization, and toxicity. Environ Sci Technol 52:4850–4860
Pan XL, Deng CN, Zhang DY, Wang J, Mu G, Chen Y (2008) Toxic effects of amoxicillin on the photosystem II of Synechocystis sp. characterized by a variety of in vivo chlorophyll fluorescence tests. Aquat Toxicol 89:207–213
Pan XL, Liu J, Zhang DY (2010) Binding of phenanthrene to extracellular polymeric substances (EPS) from aerobic activated sludge: a fluorescence study. Colloid Surface B 80:103–106
Salati S, Papa G, Adani F (2011) Perspective on the use of humic acids from biomass as natural surfactants for industrial applications. Biotechnol Adv 29:913–922
Santos LHML, Araújo AN, Fachini A, Pena A, Delerue-Matos C, Montenegro MCBS (2010) Ecotoxicological aspects related to the presence of pharmaceuticals in the aquatic environment. J Hazard Mater 175:45–95
Scaria J, Anupama KV, Nidheesh PV (2021) Tetracyclines in the environment: an overview on the occurrence, fate, toxicity, detection, removal methods, and sludge management. Sci Total Environ 771:145291
Song C, Sun X, Xing S, Xia P, Shi Y, Wang S (2014) Characterization of the interactions between tetracycline antibiotics and microbial extracellular polymeric substances with spectroscopic approaches. Environ Sci Pollut Res 21:1786–1795. https://doi.org/10.1007/s11356-013-2070-6
Wang S, Zhang DY, Pan XL (2012) Effects of arsenic on growth and photosystem II (PSII) activity of Microcystis aeruginosa. Ecotox Environ Safe 84:104–111
Wang S, Chen F, Mu S, Zhang DY, Pan XL, Lee D (2013) Simultaneous analysis of photosystem responses of Microcystis aeruginoga under chromium stress. Ecotox Environ Safe 88:163–168
Wang Y, Liu J, Liem-Nguyen V, Tian S, Zhang S, Wang D, Jiang T (2022) Binding strength of mercury (II) to different dissolved organic matter: the roles of DOM properties and sources. Sci Total Environ 807:150979
Wu C, Tang R, Li H, Liu X, Fu L, Yu Y, Wan C (2022) Interaction between organic matter and tetracycline in river sediments in cold regions. Environ Sci Pollut R 29(17):24941–24950
Xia X, Zhai Y, Dong J (2013) Contribution ratio of freely to total dissolved concentrations of polycyclic aromatic hydrocarbons in natural river waters. Chemosphere 90:1785–1793
Xiao Y, Huang Q, Vähätalo AV, Li F, Chen L (2014) Effects of dissolved organic matter from a eutrophic lake on the freely dissolved concentrations of emerging organic contaminants. Environ Toxicol Chem 33:1739–1746
Yang W, Tang Z, Zhou F, Zhang W, Song L (2013) Toxicity studies of tetracycline on Microcystis aeruginosa and Selenastrum capricornutum. Environ Toxicol Pharmacol 35:320–324
Zhang H, Qu J, Liu H, Zhao X (2009) Characterization of isolated fractions of dissolved organic matter from sewage treatment plant and the related disinfection by-products formation potential. J Hazard Mater 164:1433–1438
Zhang C, Zhang D, Xiao Z, Li Z, Suzuki D, Katayama A (2015) Characterization of humins from different natural sources and the effect on microbial reductive dechlorination of pentachlorophenol. Chemosphere 131:110–116
Funding
This research was supported by the National Key Research and Development Program of China (2018YFC1802900), National Natural Science Foundation of China (4210070598, U1703243), Zhejiang Provincial Natural Science Foundation of China (LQ22D030004), and Scientific Starting Foundation of Zhejiang University of Technology (2020129007029).
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Caiqin Wang performed formal analysis and wrote the original draft; Hang Xu provided methodology and investigation; Tingfeng Cheng and Shuting Tang provided methodology and analyzed the data; Daoyong Zhang and Meichao Li reviewed the manuscript; Xiangliang Pan supervised the entire project, processed the concept, and provided methodology. All authors read and approved the final manuscript.
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Wang, C., Xu, H., Cheng, T. et al. Affinity-based alleviation of dissolved organic matter (DOM) on tetracycline toxicity to photosynthesis of green algae Chlorella vulgaris: roles of hydrophilic and hydrophobic DOM. Environ Sci Pollut Res 30, 42165–42175 (2023). https://doi.org/10.1007/s11356-023-25201-7
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DOI: https://doi.org/10.1007/s11356-023-25201-7