A critical review of antibiotic resistance genes transmission driven by non-antibiotic pollutants: roles and molecular mechanisms

Abstract

The extensive use of antibiotics causes the abundant antibiotic residuals in the environment, further accelerating the transfer of antibiotic resistance genes (ARGs). ARGs pose a high risk to public health and environmental ecosystems. Pollutants and ARGs coexist in various environments such as livestock farms, landfills, constructed wetlands, etc. As a sink of various pollutants, wastewater treatment plants cannot completely remove antibiotics and ARGs, as well as provide a habitat for ARGs accumulation and transfer. In addition to antibiotics, numerous non-antibiotic pollutants, such as nanomaterials, disinfectants, non-antibiotic pharmaceuticals and microplastics, have also been reported to drive ARGs dissemination, especially their conjugative transfer. These non-antibiotic pollutants could induce bacterial oxidative stress, redistribute energy for metabolic pathways and upregulate the expression of plasmid-related genes. To fully understand the fate and risk of ARGs in ecosystems, it remains urgent to emphasize and fill the gap in the role and mechanism of non-antibiotic pollutants in facilitating ARGs transfer. Therefore, this review systematically summarizes the contribution of non-antibiotic pollutants to the accumulation and spread of ARGs and their regulatory mechanisms. More efforts could be paid to microbial behaviors and interactions under the stress of multiple non-antibiotic pollutants. It provides a holistic insight into the potential ecological risks of non-antibiotic pollutants and their resulting ARGs transfer, which probably facilitates the development of effective control strategies for resistance.

Graphical abstract

Keywords

Non-antibiotic pollutants / Antibiotic resistance genes / Gene Transfer / Molecular mechanism / Microbial community

Highlight

	● Non-antibiotic pollutants facilitated ARGs transfer, especially conjugation.
	● Various non-antibiotic pollutants showed different impacts on gene transfer frequency.
	● Regulatory mechanisms of non-antibiotic pollutants on HGT were summarized.
	● The future research needs and strategies were proposed.

References

[1] Arias-Andres M, Klümper U, Rojas-Jimenez K, Grossart H P. (2018). Microplastic pollution increases gene exchange in aquatic ecosystems. Environmental Pollution, 237: 253–261

[2] Baharoglu Z, Bikard D, Mazel D. (2010). Conjugative DNA transfer induces the bacterial SOS response and promotes antibiotic resistance development through integron activation. PLoS Genetics, 6(10): e1001165

[3] Biquet-Bisquert A, Carrio B, Meyer N, Fernandes T F D, Abkarian M, Seduk F, Magalon A, Nord A L, Pedaci F. (2024). Spatiotemporal dynamics of the proton motive force on single bacterial cells. Science Advances, 10(21): eadl5849

[4] Buberg M L, Witsø I L, L'Abée-Lund T M, Wasteson Y. (2020). Zinc and copper reduce conjugative transfer of resistance plasmids from extended-spectrum beta-lactamase-producing Escherichia coli. Microbial Drug Resistance, 26(7): 842–849

[5] Cao J R, Xue B, Yang S R, Yang X B, Zhang X, Qiu Z G, Shen Z Q, Wang J F. (2024). Chlorite and bromate alter the conjugative transfer of antibiotic resistance genes: co-regulation of oxidative stress and energy supply. Journal of Hazardous Materials, 471: 134257

[6] Cen T Y, Zhang X Y, Xie S S, Li D. (2020). Preservatives accelerate the horizontal transfer of plasmid-mediated antimicrobial resistance genes via differential mechanisms. Environment International, 138: 105544

[7] Chaturvedi P, Shukla P, Giri B S, Chowdhary P, Chandra R, Gupta P, Pandey A. (2021). Prevalence and hazardous impact of pharmaceutical and personal care products and antibiotics in environment: a review on emerging contaminants. Environmental Research, 194: 110664

[8] Chen B, Han J, Dai H, Jia P Q (2021). Biocide-tolerance and antibiotic-resistance in community environments and risk of direct transfers to humans: Unintended consequences of community-wide surface disinfecting during COVID-19? Environmental Pollution, 283: 117074

[9] Chen Y R, Guo X P, Feng J N, Lu D P, Niu Z S, Tou F Y, Hou L J, Liu M, Yang Y. (2019). Impact of ZnO nanoparticles on the antibiotic resistance genes (ARGs) in estuarine water: ARG variations and their association with the microbial community. Environmental Science: Nano, 6(8): 2405–2419

[10] Cheng Y, Lu J R, Fu S S, Wang S J, Senehi N, Yuan Q B. (2022). Enhanced propagation of intracellular and extracellular antibiotic resistance genes in municipal wastewater by microplastics. Environmental Pollution, 292: 118284

[11] Costa T R D, Harb L, Khara P, Zeng L Y, Hu B, Christie P J. (2021). Type IV secretion systems: advances in structure, function, and activation. Molecular Microbiology, 115(3): 436–452

[12] Ding D, Wang B, Zhang X A, Zhang J X, Zhang H H, Liu X X, Gao Z, Yu Z L. (2023). The spread of antibiotic resistance to humans and potential protection strategies. Ecotoxicology and Environmental Safety, 254: 114734

[13] Du J J, Kong Y H, Wen Y J, Shen E X, Xing H. (2024). HUH endonuclease: a sequence-specific fusion protein tag for precise DNA-protein conjugation. Bioorganic Chemistry, 144: 107118

[14] Fan N S, Zhu X L, Wu J, Tian Z, Bai Y H, Huang B C, Jin R C. (2019). Deciphering the microbial and genetic responses of anammox biogranules to the single and joint stress of zinc and tetracycline. Environment International, 132: 105097

[15] Feng G Q, Huang H N, Chen Y G. (2021). Effects of emerging pollutants on the occurrence and transfer of antibiotic resistance genes: a review. Journal of Hazardous Materials, 420: 126602

[16] Fiorentini D, Cappadone C, Farruggia G, Prata C. (2021). Magnesium: biochemistry, nutrition, detection, and social impact of diseases linked to its deficiency. Nutrients, 13(4): 1136

[17] Gonyar L A, Sauder A B, Mortensen L, Willsey G G, Kendall M M. (2024). The yad and yeh fimbrial loci influence gene expression and virulence in enterohemorrhagic Escherichia coli O157: H7. mSphere, 9(7): e00124–24

[18] Guo J H, Li J, Chen H, Bond P L, Yuan Z G. (2017). Metagenomic analysis reveals wastewater treatment plants as hotspots of antibiotic resistance genes and mobile genetic elements. Water Research, 123: 468–478

[19] Guo J J, Qiu X, Xie Y G, Hua Z S, Wang Y K. (2024). Regulation of intracellular process by two-component systems: exploring the mechanism of plasmid-mediated conjugative transfer. Water Research, 259: 121855

[20] Guo M T, Tian X B. (2019). Impacts on antibiotic-resistant bacteria and their horizontal gene transfer by graphene-based TiO₂&Ag composite photocatalysts under solar irradiation. Journal of Hazardous Materials, 380: 120877

[21] Guo M T, Zhang G S. (2017). Graphene oxide in the water environment could affect tetracycline-antibiotic resistance. Chemosphere, 183: 197–203

[22] Guo Y, Gao J F, Cui Y C, Wang Z Q, Li Z Q, Duan W J, Wang Y W, Wu Z J. (2022). Chloroxylenol at environmental concentrations can promote conjugative transfer of antibiotic resistance genes by multiple mechanisms. Science of the Total Environment, 816: 151599

[23] Han N N, Wang X P, Jin J A, Li W H, Yang W Y, Fan N S, Jin R C. (2025). Underrated risk of antibiotic resistance genes dissemination mediated by bioaerosols released from anaerobic biological wastewater treatment system. Water Research, 279: 123463

[24] Hu Z C, Yang L H, Liu Z S, Han J, Zhao Y X, Jin Y H, Sheng Y Q, Zhu L Z, Hu B L. (2023). Excessive disinfection aggravated the environmental prevalence of antimicrobial resistance during COVID-19 pandemic. Science of the Total Environment, 882: 163598

[25] Huang H N, Feng G Q, Wang M, Liu C, Wu Y, Dong L, Feng L Y, Zheng X, Chen Y G. (2022). Nitric oxide: a neglected driver for the conjugative transfer of antibiotic resistance genes among wastewater microbiota. Environmental Science & Technology, 56(10): 6466–6478

[26] Jahan I, Chowdhury G, Baquero A O, Couetard N, Hossain M A, Mian S, Iqbal M M. (2024). Microplastics pollution in the Surma River, Bangladesh: a rising hazard to upstream water quality and aquatic life. Journal of Environmental Management, 360: 121117

[27] Jia J, Liu Q, Zhao E, Li X, Xiong X, Wu C X. (2024). Biofilm formation on microplastics and interactions with antibiotics, antibiotic resistance genes and pathogens in aquatic environment. Eco-Environment & Health, 3(4): 516–528

[28] Jia Y Q, Wang Z Q, Fang D, Yang B Q, Li R C, Liu Y. (2021). Acetaminophen promotes horizontal transfer of plasmid-borne multiple antibiotic resistance genes. Science of the Total Environment, 782: 146916

[29] Jia Y Q, Yang B Q, Shi J R, Fang D, Wang Z Q, Liu Y. (2022). Melatonin prevents conjugative transfer of plasmid-mediated antibiotic resistance genes by disrupting proton motive force. Pharmacological Research, 175: 105978

[30] Jiang Q, Feng M B, Ye C S, Yu X. (2022). Effects and relevant mechanisms of non-antibiotic factors on the horizontal transfer of antibiotic resistance genes in water environments: a review. Science of the Total Environment, 806: 150568

[31] Juan C A, de la Lastra J M P, Plou F J, Pérez-Lebeña E. (2021). The chemistry of reactive oxygen species (ROS) revisited: outlining their role in biological macromolecules (DNA, lipids and proteins) and induced pathologies. International Journal of Molecular Sciences, 22(9): 4642

[32] Li G Y, Chen X F, Yin H L, Wang W J, Wong P K, An T C. (2020). Natural sphalerite nanoparticles can accelerate horizontal transfer of plasmid-mediated antibiotic-resistance genes. Environment International, 136: 105497

[33] Li Z Q, Gao J F, Guo Y, Cui Y C, Wang Y W, Duan W J, Wu Z J. (2022). Enhancement of antibiotic resistance dissemination by artificial sweetener acesulfame potassium: insights from cell membrane, enzyme, energy supply and transcriptomics. Journal of Hazardous Materials, 422: 126942

[34] Liao J Q, Huang H N, Chen Y G. (2019). CO₂ promotes the conjugative transfer of multiresistance genes by facilitating cellular contact and plasmid transfer. Environment International, 129: 333–342

[35] Lin H, Jiang L T, Li B, Dong Y B, He Y H, Qiu Y. (2019). Screening and evaluation of heavy metals facilitating antibiotic resistance gene transfer in a sludge bacterial community. Science of the Total Environment, 695: 133862

[36] Liu L, Zhang Q H, Li R T. (2023). In situ and individual-based analysis of the influence of polystyrene microplastics on Escherichia coli conjugative gene transfer at the single-cell level. Environmental Science & Technology, 57(42): 15936–15944

[37] Lu J, Wang Y, Jin M, Yuan Z G, Bond P, Guo J H. (2020). Both silver ions and silver nanoparticles facilitate the horizontal transfer of plasmid-mediated antibiotic resistance genes. Water Research, 169: 115229

[38] Lu J, Wu J, Wang J H. (2022a). Metagenomic analysis on resistance genes in water and microplastics from a mariculture system. Frontiers of Environmental Science & Engineering, 16(1): 4

[39] Lu J, Wu J, Zhang C, Wang J H, He X. (2024). Occurrence and possible sources of antibiotic resistance genes in seawater of the South China Sea. Frontiers of Environmental Science & Engineering, 18(9): 108

[40] Lu J, Yu Z G, Ding P B, Guo J H. (2022b). Triclosan promotes conjugative transfer of antibiotic resistance genes to opportunistic pathogens in environmental microbiome. Environmental Science & Technology, 56(21): 15108–15119

[41] Lu Y J, Zhou X Q, Zheng Y, Yang H L, Cao W B. (2025). How far do we still need to go with antibiotics in aquatic environments? Antibiotic occurrence, chemical-free or chemical-limited strategies, key challenges, and future perspectives. Water Research, 275: 123179

[42] Luo T Y, Dai X H, Wei W, Xu Q X, Ni B J. (2023). Microplastics enhance the prevalence of antibiotic resistance genes in anaerobic sludge digestion by enriching antibiotic-resistant bacteria in surface biofilm and facilitating the vertical and horizontal gene transfer. Environmental Science & Technology, 57(39): 14611–14621

[43] Ma W J, Ren Z Q, Yu L Q, Wu X X, Yao Y X, Zhang J T, Guo J Y, Fan N S, Jin R C. (2021a). Deciphering the response of anammox process to heavy metal and antibiotic stress: arsenic enhances the permeability of extracellular polymeric substance and aggravates the inhibition of sulfamethoxazole. Chemical Engineering Journal, 426: 130815

[44] Ma X Y, Zhang X W, Xia J T, Sun H H, Zhang X X, Ye L. (2021b). Phenolic compounds promote the horizontal transfer of antibiotic resistance genes in activated sludge. Science of the Total Environment, 800: 149549

[45] Mithuna R, Tharanyalakshmi R, Jain I, Singhal S, Sikarwar D, Das S, Ranjitha J, Ghosh D, Rahman M M, Das B. (2024). Emergence of antibiotic resistance due to the excessive use of antibiotics in medicines and feed additives: a global scenario with emphasis on the Indian perspective. Emerging Contaminants, 10(4): 100389

[46] Pu Q, Fan X T, Li H, An X L, Lassen S B, Su J Q. (2021a). Cadmium enhances conjugative plasmid transfer to a fresh water microbial community. Environmental Pollution, 268: 115903

[47] Pu Q, Fan X T, Sun A Q, Pan T, Li H, Lassen S B, An X L, Su J Q. (2021b). Co-effect of cadmium and iron oxide nanoparticles on plasmid-mediated conjugative transfer of antibiotic resistance genes. Environment International, 152: 106453

[48] Qiu Z G, Shen Z Q, Qian D, Jin M, Yang D, Wang J F, Zhang B, Yang Z W, Chen Z L, Wang X W. . (2015). Effects of nano-TiO₂ on antibiotic resistance transfer mediated by RP4 plasmid. Nanotoxicology, 9(7): 895–904

[49] Qiu Z G, Yu Y M, Chen Z L, Jin M, Yang D, Zhao Z G, Wang J F, Shen Z Q, Wang X W, Qian D. . (2012). Nanoalumina promotes the horizontal transfer of multiresistance genes mediated by plasmids across genera. Proceedings of the National Academy of Sciences, 109(13): 4944–4949

[50] Ren Z Y, Guo H, Jin H K, Wang Y J, Zhang G D, Zhou J, Qu G Z, Sun Q H, Wang T C. (2023). P, N, and C-related functional genes in SBR system promoted antibiotics resistance gene transmission under polystyrene microplastics stress. Water Research, 235: 119884

[51] Sakina A S, Khan A, Nasrullah F, Ullah N, Muhammad S, Kubra I U, Din Z. (2021). Effect of imidazolium’s ionic liquids with different anions and alkyl chain length on phytotoxicity and biochemical analysis of maize seedling. Journal of Molecular Liquids, 321: 114491

[52] Shamsizadeh Z, Nikaeen M, Mohammadi F, Farhadkhani M, Mokhtari M, Ehrampoush M H. (2024). Wastewater surveillance of antibiotic resistance and class 1 integron-integrase genes: potential impact of wastewater characteristics on genes profile. Heliyon, 10(9): e29601

[53] Shao B B, Shen L Y, Liu Z F, Tang L, Tan X F, Wang D B, Zeng W M, Wu T, Pan Y, Zhang X S. . (2023). Disinfection byproducts formation from emerging organic micropollutants during chlorine-based disinfection processes. Chemical Engineering Journal, 455: 140476

[54] Shi J H, Su Y L, Zhang Z J, Wei H W, Xie B (2019). How do zinc oxide and zero valent iron nanoparticles impact the occurrence of antibiotic resistance genes in landfill leachate? Environmental Science: Nano, 6(7): 2141–2151

[55] Shi X D, Xia Y, Wei W, Ni B J. (2022). Accelerated spread of antibiotic resistance genes (ARGs) induced by non-antibiotic conditions: roles and mechanisms. Water Research, 224: 119060

[56] Singh R, Ryu J, Park S S, Kim S, Kim K. (2024). Monitoring viruses and beta-lactam resistance genes through wastewater surveillance during a COVID-19 surge in Suwon, South Korea. Science of the Total Environment, 922: 171223

[57] Song Z, Zuo L, Li C, Tian Y M, Wang H N. (2021). Copper ions facilitate the conjugative transfer of SXT/R391 integrative and conjugative element across bacterial genera. Frontiers in Microbiology, 11: 616792

[58] SorokinaJSokolova IRybolovlevIShevlyaginaNTroitskiy VZhukhovitskyVBelyiY (2021). VirB4- and VirD4-like ATPases, components of a putative type 4C secretion system in Clostridioides difficile. Journal of Bacteriology, 203(21): 10.1128/jb.00359–21

[59] Su J Q, An X L, Li B, Chen Q L, Gillings M R, Chen H, Zhang T, Zhu Y G. (2017). Metagenomics of urban sewage identifies an extensively shared antibiotic resistome in China. Microbiome, 5(1): 84

[60] Su Z G, Chen L, Wen D H. (2024). Impact of wastewater treatment plant effluent discharge on the antibiotic resistome in downstream aquatic environments: a mini review. Frontiers of Environmental Science & Engineering, 18(3): 36

[61] Wang B Q, Wang Y, Zhang J, Hu C, Jiang J, Li Y M, Peng Z Y. (2023a). ROS-induced lipid peroxidation modulates cell death outcome: mechanisms behind apoptosis, autophagy, and ferroptosis. Archives of Toxicology, 97(6): 1439–1451

[62] Wang J L, Chu L B, Wojnárovits L, Takács E. (2020a). Occurrence and fate of antibiotics, antibiotic resistant genes (ARGs) and antibiotic resistant bacteria (ARB) in municipal wastewater treatment plant: an overview. Science of the Total Environment, 744: 140997

[63] Wang Q, Lu Q, Mao D Q, Cui Y X, Luo Y. (2015a). The horizontal transfer of antibiotic resistance genes is enhanced by ionic liquid with different structure of varying alkyl chain length. Frontiers in Microbiology, 6: 864

[64] Wang Q, Mao D Q, Luo Y. (2015b). Ionic liquid facilitates the conjugative transfer of antibiotic resistance genes mediated by plasmid RP4. Environmental Science & Technology, 49(14): 8731–8740

[65] Wang X L, Yang F X, Zhao J, Xu Y, Mao D Q, Zhu X, Luo Y, Alvarez P J J. (2018). Bacterial exposure to ZnO nanoparticles facilitates horizontal transfer of antibiotic resistance genes. NanoImpact, 10: 61–67

[66] Wang X N, Li J H, Pan X L. (2024a). How micro-/nano-plastics influence the horizontal transfer of antibiotic resistance genes-a review. Science of the Total Environment, 944: 173881

[67] Wang Y, Huang D Q, Yang J H, Li G F, Zhou Y X, Zhang J Y, Lu Y, Fan N S, Jin R C. (2023b). Polyamide microplastics act as carriers for cephalexin in the anammox process. Chemical Engineering Journal, 451: 138685

[68] Wang Y, Lu J, Mao L K, Li J, Yuan Z G, Bond P L, Guo J H. (2019). Antiepileptic drug carbamazepine promotes horizontal transfer of plasmid-borne multi-antibiotic resistance genes within and across bacterial genera. The ISME Journal, 13(2): 509–522

[69] Wang Y, Lu J, Zhang S, Li J, Mao L K, Yuan Z G, Bond P L, Guo J H. (2021). Non-antibiotic pharmaceuticals promote the transmission of multidrug resistance plasmids through intra- and intergenera conjugation. The ISME Journal, 15(9): 2493–2508

[70] Wang Y F, Qiao M, Zhu D, Zhu Y G. (2020b). Antibiotic resistance in the collembolan gut microbiome accelerated by the nonantibiotic drug carbamazepine. Environmental Science & Technology, 54(17): 10754–10762

[71] Wang Y J, Zhang S, Li L, Zhang Q, Yang L Y, Yang K, Liu Y, Zhu H R, Lai B S, Wu J. . (2024b). Airborne ARGs/MGEs from two sewage types during the COVID-21: population, microbe interactions, cytotoxicity, formation mechanism, and dispersion. Water Research, 254: 121368

[72] Wu J, Zhou J H, Liu D F, Wu J, He R L, Cheng Z H, Li H H, Li W W. (2023a). Phthalates promote dissemination of antibiotic resistance genes: an overlooked environmental risk. Environmental Science & Technology, 57(17): 6876–6887

[73] Wu Q, Wang X, Li H Y, Huang D Q, Huang B C, Jin R C, Fan N S. (2023b). Perturbation and mechanism of non-antibiotic drug in regulating resistome and metabolome of anammox consortia: an overlooked and underrated cause of multiresistance. Chemical Engineering Journal, 475: 146325

[74] Xu L, Zhou Z C, Zhu L, Han Y, Lin Z J, Feng W Q, Liu Y, Shuai X Y, Chen H. (2020). Antibiotic resistance genes and microcystins in a drinking water treatment plant. Environmental Pollution, 258: 113718

[75] Xu L K, Ouyang W Y, Qian Y Y, Su C, Su J Q, Chen H. (2016). High-throughput profiling of antibiotic resistance genes in drinking water treatment plants and distribution systems. Environmental Pollution, 213: 119–126

[76] Yang B Q, Wang Z Q, Jia Y Q, Fang D, Li R C, Liu Y. (2022). Paclitaxel and its derivative facilitate the transmission of plasmid-mediated antibiotic resistance genes through conjugative transfer. Science of the Total Environment, 810: 152245

[77] Yang Q E, Lin Z Y, Gan D H, Li M C, Liu X D, Zhou S G, Walsh T R. (2025). Microplastics mediates the spread of antimicrobial resistance plasmids via modulating conjugal gene expression. Environment International, 195: 109261

[78] Yang X B, Niu Y Y, Yang Y T, Zhou H R, Li J, Fu X Y, Shen Z Q, Wang J F, Qiu Z G. (2023a). Pheromone effect of estradiol regulates the conjugative transfer of pCF10 carrying antibiotic resistance genes. Journal of Hazardous Materials, 451: 131087

[79] Yang Y T, Guo X P, Xu T, Yin D Q. (2023b). Effects of carbamazepine on gut microbiota, ARGs and intestinal health in zebrafish. Ecotoxicology and Environmental Safety, 249: 114473

[80] Ye C S, Feng M B, Chen Y Q, Zhang Y T, Chen Q, Yu X. (2022). Dormancy induced by oxidative damage during disinfection facilitates conjugation of ARGs through enhancing efflux and oxidative stress: a lagging response. Water Research, 221: 118798

[81] Yu K Q, Chen F R, Yue L, Luo Y, Wang Z Y, Xing B S. (2020). CeO₂ nanoparticles regulate the propagation of antibiotic resistance genes by altering cellular contact and plasmid transfer. Environmental Science & Technology, 54(16): 10012–10021

[82] Yu X, Zhou Z C, Shuai X Y, Lin Z J, Liu Z, Zhou J Y, Lin Y H, Zeng G S, Ge Z Y, Chen H. (2023). Microplastics exacerbate co-occurrence and horizontal transfer of antibiotic resistance genes. Journal of Hazardous Materials, 451: 131130

[83] Yu Z G, Wang Y, Henderson I R, Guo J H. (2022). Artificial sweeteners stimulate horizontal transfer of extracellular antibiotic resistance genes through natural transformation. The ISME Journal, 16(2): 543–554

[84] Yu Z G, Wang Y, Lu J, Bond P L, Guo J H. (2021). Nonnutritive sweeteners can promote the dissemination of antibiotic resistance through conjugative gene transfer. The ISME Journal, 15(7): 2117–2130

[85] Yuan Q B, Sun R N, Yu P F, Cheng Y, Wu W B, Bao J M, Alvarez P J J. (2022). UV-aging of microplastics increases proximal ARG donor-recipient adsorption and leaching of chemicals that synergistically enhance antibiotic resistance propagation. Journal of Hazardous Materials, 427: 127895

[86] Zhang H N, Liu J B, Wang L, Zhai Z Z. (2021a). Glyphosate escalates horizontal transfer of conjugative plasmid harboring antibiotic resistance genes. Bioengineered, 12(1): 63–69

[87] Zhang S, Wang Y, Song H L, Lu J, Yuan Z G, Guo J H. (2019a). Copper nanoparticles and copper ions promote horizontal transfer of plasmid-mediated multi-antibiotic resistance genes across bacterial genera. Environment International, 129: 478–487

[88] Zhang S Q, Abbas M, Rehman M U, Huang Y H, Zhou R, Gong S Y, Yang H, Chen S L, Wang M S, Cheng A C. (2020). Dissemination of antibiotic resistance genes (ARGs) via integrons in Escherichia coli: a risk to human health. Environmental Pollution, 266: 115260

[89] Zhang S X, Li C R, Lv H, Cui B, Zhou D D. (2024). Anammox activity improved significantly by the cross-fed NO from ammonia-oxidizing bacteria and denitrifying bacteria to anammox bacteria. Water Research, 249: 120986

[90] Zhang T, Li X Y, Wang M F, Chen H X, Yang Y, Chen Q L, Yao M S. (2019b). Time-resolved spread of antibiotic resistance genes in highly polluted air. Environment International, 127: 333–339

[91] Zhang X X, Zhang T. (2011). Occurrence, abundance, and diversity of tetracycline resistance genes in 15 sewage treatment plants across China and other global locations. Environmental Science & Technology, 45(7): 2598–2604

[92] Zhang Y, Gu A Z, Cen T Y, Li X Y, He M, Li D, Chen J M. (2018a). Sub-inhibitory concentrations of heavy metals facilitate the horizontal transfer of plasmid-mediated antibiotic resistance genes in water environment. Environmental Pollution, 237: 74–82

[93] Zhang Y, Gu A Z, Cen T Y, Li X Y, Li D, Chen J M. (2018b). Petrol and diesel exhaust particles accelerate the horizontal transfer of plasmid-mediated antimicrobial resistance genes. Environment International, 114: 280–287

[94] Zhang Y, Gu A Z, He M, Li D, Chen J M. (2017). Subinhibitory concentrations of disinfectants promote the horizontal transfer of multidrug resistance genes within and across genera. Environmental Science & Technology, 51(1): 570–580

[95] Zhang Y, Zheng Y H, Zhu Z P, Chen Y X, Dong H M. (2021b). Dispersion of Antibiotic Resistance Genes (ARGs) from stored swine manure biogas digestate to the atmosphere. Science of the Total Environment, 761: 144108

[96] ZhangY PZhang C QParkerD BSnowD DZhouZ LiX (2013). Occurrence of antimicrobials and antimicrobial resistance genes in beef cattle storage ponds and swine treatment lagoons. Science of the Total Environment, 463–464: 463–464

[97] Zhao W X, Hou Y N, Wei L L, Wei W, Zhang K F, Duan H R, Ni B J. (2025). Chlorination-induced spread of antibiotic resistance genes in drinking water systems. Water Research, 274: 123092

[98] Zheng G M, Filippelli G M, Salamova A. (2020). Increased indoor exposure to commonly used disinfectants during the COVID-19 pandemic. Environmental Science & Technology Letters, 7(10): 760–765

[99] Zhou T, Zhang Z H, Liu H, Dong S M, Nghiem L D, Gao L, Chaves A V, Zamyadi A, Li X, Wang Q L. (2023). A review on microalgae-mediated biotechnology for removing pharmaceutical contaminants in aqueous environments: occurrence, fate, and removal mechanism. Journal of Hazardous Materials, 443: 130213

[100] Zhu S Y, Yang B Q, Jia Y Q, Yu F Y, Wang Z Q, Liu Y. (2023). Comprehensive analysis of disinfectants on the horizontal transfer of antibiotic resistance genes. Journal of Hazardous Materials, 453: 131428

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