Abstract
Most antibiotics contain ionizable groups that undergo acid-base dissociation giving rise to diverse dissociated forms in aquatic systems depending on the pH of the system. In sunlit surface waters, photochemical transformation plays a crucial role in determining the fate of antibiotics. This study presents a comprehensive examination of the photo-transformation degradation kinetics, pathways and photoinduced toxicity of three widely detected tetracyclines (TCs): tetracycline (TC), oxytetracycline (OTC), and chlortetracycline (CTC). Under simulated sunlight (λ > 290 nm), their apparent photolysis followed pseudo-first-order kinetics, with rate constants significantly increasing from H2TCs0 to TCs2−. Through competition kinetic experiments and matrix calculations, it was found that the anions HTCs− or TCs2− (pH ∼ 8–10) were more reactive toward hydroxyl radicals (•OH), while TCs2− (pH ∼ 10) reacted the fastest with singlet oxygen (1O2). Considering the dissociated species, the total environmental photo-transformation half-lives of TCs were determined, revealing a strong dependence on the water pH and seasonal variation in sunlight. Generally, apparent photolysis was the dominant photochemical process, followed by 1O2 and •OH oxidation. Different transformation pathways for the three reactions were determined based on the key photoproducts identified using HPLC-MS/MS. Toxicity tests and ECOSAR software calculations confirmed that the intermediates produced by the •OH and 1O2 photo-oxidation processes were more toxic than the parent compounds. These findings significantly enhance our understanding of the complex photochemical fate and associated risks of TCs in aqueous environments.
Article PDF
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
References
Adamek E, Baran W, Sobczak A (2016). Assessment of the biodegradability of selected sulfa drugs in two polluted rivers in Poland: effects of seasonal variations, accidental contamination, turbidity and salinity. Journal of Hazardous Materials, 313: 147–158
Al Housari F, Vione D, Chiron S, Barbati S (2010). Reactive photoinduced species in estuarine waters: characterization of hydroxyl radical, singlet oxygen and dissolved organic matter triplet state in natural oxidation processes. Photochemical & Photobiological Sciences, 9(1): 78–86
An J, Chen H, Wei S, Gu J (2015). Antibiotic contamination in animal manure, soil, and sewage sludge in Shenyang, northeast China. Environmental Earth Sciences, 74(6): 5077–5086
Anjali R, Shanthakumar S (2019). Insights on the current status of occurrence and removal of antibiotics in wastewater by advanced oxidation processes. Journal of Environmental Management, 246: 51–62
Bodrato M, Vione D (2014). APEX (Aqueous photochemistry of environmentally occurring xenobiotics): a free software tool to predict the kinetics of photochemical processes in surface waters. Environmental Science. Processes & Impacts, 16(4): 732–740
Boreen A L, Arnold W A, Mcneill K (2004). Photochemical fate of sulfa drugs in the aquatic environment: sulfa drugs containing five-membered heterocyclic groups. Environmental Science & Technology, 38(14): 3933–3940
Boreen A L, Arnold W A, Mcneill K (2005). Triplet-sensitized photodegradation of sulfa drugs containing six-membered heterocyclic groups: identification of an SO2 extrusion photoproduct. Environmental Science & Technology, 39(10): 3630–3638
Chen W, Huang C (2011). Transformation kinetics and pathways of tetracycline antibiotics with manganese oxide. Environmental Pollution, 159(5): 1092–1100
Chen Y, Li H, Wang Z, Tao T, Hu C (2011). Photoproducts of tetracycline and oxytetracycline involving self-sensitized oxidation in aqueous solutions: effects of Ca2+ and Mg2+. Journal of Environmental Sciences, 23(10): 1634–1639
Cheng J, Jiang L, Sun T, Tang Y, Du Z, Lee L, Zhao Q (2019). Occurrence, seasonal variation and risk assessment of antibiotics in the surface water of north China. Archives of Environmental Contamination and Toxicology, 77(1): 88–97
Edhlund B L, Arnold W A, Mcneill K (2006). Aquatic photochemistry of nitrofuran antibiotics. Environmental Science & Technology, 40(17): 5422–5427
Felis E, Buta-Hubeny M, Zieliński W, Hubeny J, Harnisz M, Bajkacz S, Korzeniewska E (2022). Solar-light driven photodegradation of antimicrobials, their transformation by-products and antibiotic resistance determinants in treated wastewater. Science of the Total Environment, 836: 155447
Ge L, Chen J, Wei X, Zhang S, Qiao X, Cai X, Xie Q (2010). Aquatic photochemistry of fluoroquinolone antibiotics: kinetics, pathways, and multivariate effects of main water constituents. Environmental Science & Technology, 44(7): 2400–2405
Ge L, Halsall C, Chen C, Zhang P, Dong Q, Yao Z (2018). Exploring the aquatic photodegradation of two ionisable fluoroquinolone antibiotics-gatifloxacin and balofloxacin: degradation kinetics, photobyproducts and risk to the aquatic environment. Science of the Total Environment, 633: 1192–1197
Ge L, Na G, Zhang S, Li K, Zhang P, Ren H, Yao Z (2015). New insights into the aquatic photochemistry of fluoroquinolone antibiotics: direct photodegradation, hydroxyl-radical oxidation, and antibacterial activity changes. Science of the Total Environment, 527–528: 12–17
Ge L, Zhang P, Halsall C, Li Y, Chen C, Li J, Sun H, Yao Z (2019). The importance of reactive oxygen species on the aqueous phototransformation of sulfonamide antibiotics: kinetics, pathways, and comparisons with direct photolysis. Water Research, 149: 243–250
Guo H, Chen Z, Lu C, Guo J, Li H, Song Y, Han Y, Hou Y (2020). Effect and ameliorative mechanisms of polyoxometalates on the denitrification under sulfonamide antibiotics stress. Bioresource Technology, 305: 123073
Han C H, Park H D, Kim S B, Yargeau V, Choi J W, Lee S H, Park J A (2020). Oxidation of tetracycline and oxytetracycline for the photo-Fenton process: their transformation products and toxicity assessment. Water Research, 172: 115514
He Y, Yuan Q, Mathieu J, Stadler L, Senehi N, Sun R, Alvarez P J (2020). Antibiotic resistance genes from livestock waste: occurrence, dissemination, and treatment. npj Clean Water, 3(1): 4
Hu S, Zhang H, Yang Y, Cui K, Ao J, Tong X, Shi M, Wang Y, Chen X, Li C, et al. (2024). Comprehensive insight into the occurrence characteristics, influencing factors and risk assessments of antibiotics in the Chaohu Basin. Frontiers of Environmental Science & Engineering, 18(5): 57–71
Jiao S, Zheng S, Yin D, Wang L, Chen L (2008a). Aqueous oxytetracycline degradation and the toxicity change of degradation compounds in photoirradiation process. Journal of Environmental Sciences, 20(7): 806–813
Jiao S, Zheng S, Yin D, Wang L, Chen L (2008b). Aqueous photolysis of tetracycline and toxicity of photolytic products to luminescent bacteria. Chemosphere, 73(3): 377–382
Jin X, Xu H, Qiu S, Jia M, Wang F, Zhang A, Jiang X (2017). Direct photolysis of oxytetracycline: Influence of initial concentration, pH and temperature. Journal of Photochemistry and Photobiology A Chemistry, 332: 224–231
Knapp C, Cardoza L, Hawes J, Wellington E, Larive C, Graham D (2005). Fate and effects of enrofloxacin in aquatic systems under different light conditions. Environmental Science & Technology, 39(23): 9140–9146
Latch D E, Packer J L, Stender B L, Vanoverbeke J, Arnold W A, Mcneill K (2005). Aqueous photochemistry of triclosan: formation of 2,4-dichlorophenol, 2,8-dichlorodibenzo-p-dioxin, and oligomerization products. Environmental Toxicology and Chemistry, 24(3): 517–525
Li R, Zhao C, Yao B, Li D, Yan S, O’Shea K E, Song W (2016). Photochemical transformation of aminoglycoside antibiotics in simulated natural waters. Environmental Science & Technology, 50(6): 2921–2930
Li S, Shi W, Liu W, Li H, Zhang W, Hu J, Ke Y, Sun W, Ni J (2018). A duodecennial national synthesis of antibiotics in China’s major rivers and seas (2005–2016). Science of the Total Environment, 615: 906–917
Li T, Ouyang W, Lin C, Wang J, Cui X, Li Y, Guo Z, Zhu W, He M (2023). Occurrence, distribution, and potential ecological risks of antibiotics in a seasonal freeze-thaw basin. Journal of Hazardous Materials, 459: 132301
Liu H, Niu C, Huang D, Liang C, Guo H, Yang Y, Li L (2023). Unravelling the role of reactive oxygen species in ultrathin Z-scheme heterojunction with surface zinc vacancies for photocatalytic H2O2 generation and CTC degradation. Chemical Engineering Journal, 465: 143007
Liu X, Lu S, Guo W, Xi B, Wang W (2018). Antibiotics in the aquatic environments: a review of lakes, China. Science of the Total Environment, 627: 1195–1208
Liu Y, Mekic M, Carena L, Vione D, Gligorovski S, Zhang G, Jin B (2020). Tracking photodegradation products and bond-cleavage reaction pathways of triclosan using ultra-high resolution mass spectrometry and stable carbon isotope analysis. Environmental Pollution, 264: 114673
Mill T (1999). Predicting photoreaction rates in surface waters. Chemosphere, 38(6): 1379–1390
Niu J, Li Y, Wang W (2013). Light-source-dependent role of nitrate and humic acid in tetracycline photolysis: kinetics and mechanism. Chemosphere, 92(11): 1423–1429
Oka H, Ikai Y, Kawamura N, Yamada M, Harada K, Ito S, Suzuki M (1989). Photodecomposition products of tetracycline in aqueous solution. Journal of Agricultural and Food Chemistry, 37(1): 226–231
Park J A, Pineda M, Peyot M L, Yargeau V (2023). Degradation of oxytetracycline and doxycycline by ozonation: degradation pathways and toxicity assessment. Science of the Total Environment, 856: 159076
Ping Q, Yan T, Wang L, Li Y, Lin Y (2022). Insight into using a novel ultraviolet/peracetic acid combination disinfection process to simultaneously remove antibiotics and antibiotic resistance genes in wastewater: mechanism and comparison with conventional processes. Water Research, 210: 118019
Qi N, Wang P, Wang C, Ao Y (2018). Effect of a typical antibiotic (tetracycline) on the aggregation of TiO2 nanoparticles in an aquatic environment. Journal of Hazardous Materials, 341: 187–197
Riu A, Le Maire A, Grimaldi M, Audebert M, Hillenweck A, Bourguet W, Balaguer P, Zalko D (2011). Characterization of novel ligands of ERα, Erβ, and PPARγ: the case of halogenated bisphenol A and their conjugated metabolites. Toxicological Sciences, 122(2): 372–382
Sciscenko I, Arques A, Varga Z, Bouchonnet S, Monfort O, Brigante M, Mailhot G (2021). Significant role of iron on the fate and photodegradation of enrofloxacin. Chemosphere, 270: 129791
Song C, Liu H, Guo S, Wang S (2020). Photolysis mechanisms of tetracycline under UV irradiation in simulated aquatic environment surrounding limestone. Chemosphere, 244: 125582
Su Z, Wang K, Yang F, Zhuang T (2023). Antibiotic pollution of the Yellow River in China and its relationship with dissolved organic matter: distribution and source identification. Water Research, 235: 119867
Tian Y, Ying C, Zhang L, Huang H, Song S, Mei R, Li J (2024). Unveiling the inhibition of chlortetracycline photodegradation and the increase of toxicity when coexisting with silver nanoparticles. Science of the Total Environment, 912: 168443
Tran N H, Hoang L, Nghiem L D, Nguyen N M H, Ngo H H, Guo W, Trinh Q T, Mai N H, Chen H, Nguyen D D, et al. (2019). Occurrence and risk assessment of multiple classes of antibiotics in urban canals and lakes in Hanoi, Vietnam. Science of the Total Environment, 692: 157–174
Vione D, Minella M, Maurino V, Minero C (2014). Indirect photochemistry in sunlit surface waters: photoinduced production of reactive transient species. Chemistry, 20(34): 10590–10606
Wang Q, He X, Xiong H, Chen Y, Huang L (2022). Structure, mechanism, and toxicity in antibiotics metal complexation: recent advances and perspectives. Science of the Total Environment, 848: 157778
Werner J J, Arnold W A, Mcneill K (2006). Water hardness as a photochemical parameter: tetracycline photolysis as a function of calcium concentration, magnesium concentration, and pH. Environmental Science & Technology, 40(23): 7236–7241
Xu H, Cooper W J, Jung J, Song W (2011). Photosensitized degradation of amoxicillin in natural organic matter isolate solutions. Water Research, 45(2): 632–638
Xu L, Zhang H, Xiong P, Zhu Q, Liao C, Jiang G (2021a). Occurrence, fate, and risk assessment of typical tetracycline antibiotics in the aquatic environment: a review. Science of the Total Environment, 753: 141975
Xu T, Fang Y, Tong T, Xia Y, Liu X, Zhang L (2021b). Environmental photochemistry in hematite-oxalate system: Fe (III)-Oxalate complex photolysis and ROS generation. Applied Catalysis B: Environmental, 283: 119645
Ye C, Chen Y, Feng L, Wan K, Li J, Feng M, Yu X (2022). Effect of the ultraviolet/chlorine process on microbial community structure, typical pathogens, and antibiotic resistance genes in reclaimed water. Frontiers of Environmental Science & Engineering, 16(8): 100–113
Yu J, Chen X, Zhang Y, Cui X, Zhang Z, Guo W, Wang D, Huang S, Chen Y, Hu Y, et al. (2022). Antibiotic azithromycin inhibits brown/beige fat functionality and promotes obesity in human and rodents. Theranostics, 12(3): 1187–1203
Yuan X, Cui K, Chen Y, Wu S, Zhang Y, Liu T (2023). Response of antibiotic and heavy metal resistance genes to the co-occurrence of gadolinium and sulfamethoxazole in activated sludge systems. Frontiers of Environmental Science & Engineering, 17(12): 154–164
Zhang C, Chen Y, Chen S, Guan X, Zhong Y, Yang Q (2023). Occurrence, risk assessment, and in vitro and in vivo toxicity of antibiotics in surface water in China. Ecotoxicology and Environmental Safety, 255: 114817
Zhang M, He L, Liu Y, Zhao J, Liu W, Zhang J, Chen J, He L, Zhang Q, Ying G (2019). Fate of veterinary antibiotics during animal manure composting. Science of the Total Environment, 650: 1363–1370
Zhang T, Cheng F, Yang H, Zhu B, Li C, Zhang Y N, Qu J, Peijnenburg W J (2022a). Photochemical degradation pathways of cell-free antibiotic resistance genes in water under simulated sunlight irradiation: experimental and quantum chemical studies. Chemosphere, 302: 134879
Zhang X, Kamali M, Yu X, Costa M E V, Appels L, Cabooter D, Dewil R (2022b). Kinetics and mechanisms of the carbamazepine degradation in aqueous media using novel iodate-assisted photochemical and photocatalytic systems. Science of the Total Environment, 825: 153871
Zhang X, Su H, Gao P, Li B, Feng L, Liu Y, Du Z, Zhang L (2022c). Effects and mechanisms of aged polystyrene microplastics on the photodegradation of sulfamethoxazole in water under simulated sunlight. Journal of Hazardous Materials, 433: 128813
Zhang Y, Zhang C, Parker D B, Snow D D, Zhou Z, Li X (2013). Occurrence of antimicrobials and antimicrobial resistance genes in beef cattle storage ponds and swine treatment lagoons. Science of the Total Environment, 463–464: 631–638
Zheng J, Zhang P, Li X, Ge L, Niu J (2023). Insight into typical photoassisted AOPs for the degradation of antibiotic micropollutants: mechanisms and research gaps. Chemosphere, 343: 140211
Zhou Y, Cheng F, He D, Zhang Y, Qu J, Yang X, Chen J, Peijnenburg W J (2021). Effect of UV/chlorine treatment on photophysical and photochemical properties of dissolved organic matter. Water Research, 192: 116857
Acknowledgements
This work was supported by the Key Research and Development Program of Shaanxi Province (No. 2024SF-YBXM-567), the National Natural Science Foundation of China (Nos. 21976045 and 22076112), the China Scholarship Council (CSC) Scholarship (No. 202308610123), and the Shaanxi Key Laboratory of Environmental Monitoring and Forewarning of Trace Pollutants (No. SHJKFJJ202318).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interests The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Additional information
Highlights
• Mechanisms for multiple photochemical transformation of tetracyclines were reported.
• The degradation kinetics were dependent on pH and reactivities of dissociated forms.
• Anionic forms reacted faster in the apparent photolysis and photooxidation processes.
• Different pathways and various intermediates occurred for the three reactions.
• The major by-products showed similar or more toxicities than the parent antibiotics.
Rights and permissions
About this article
Cite this article
Ge, L., Zheng, J., Halsall, C. et al. Aquatic photo-transformation and enhanced photoinduced toxicity of ionizable tetracycline antibiotics. Front. Environ. Sci. Eng. 18, 139 (2024). https://doi.org/10.1007/s11783-024-1899-x
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11783-024-1899-x