The dispersion characteristics and exposure risks of antibiotic resistance genes and resistant pathogenic bacteria in air——Take a typical municipal sewage treatment plant as an example
GAO Shan-shan1, LIU Shuo1,2, LI Shao-bin1,2, WEI Ze-ran2, XIN Hui-bo2, TIAN Jia-yu1, GAO Min2
1. School of Civil and Transportation Engineering, Hebei University of Technology, Tianjin 300401, China; 2. Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China
Abstract:A systematic study on antibiotic resistance genes (ARGs) and resistant pathogenic bacteria in the air and corresponding sewage of the sewage treatment plant was conducted. Their enrichment rate in the air and influencing factors were analyzed, and daily respiratory exposure was assessed. A divergence in the distribution of predominant ARGs in ambient air and sewage was revealed, with Sul1 and tetW being identified as the most abundantly detected genetic markers. The taxonomic composition of the dominant pathogenic bacteria was found to be similar across both matrices, with Bacteroides, Klebsiella, and Enterococcus genera being identified as the most prevalent in sequential order. Enrichment of certain ARGs and pathogenic bacteria was observed in the air of wastewater treatment plants, with the highest enrichment rates being attributed to the tetW gene and Megamonas genus, respectively. The transfer process of ARGs and pathogenic bacteria from wastewater to air was influenced by factors such as water quality and aeration processes. Tracing analysis indicated that approximately 73.59%±3.61% of the bacteria in the air of wastewater treatment plants originated from the sewage. Methicillin-resistant Staphylococcus aureus (MRSA) was successfully isolated from both air and sewage samples, with MRSA in the air being observed to exhibit an antibiotic resistance index (0.24) that was significantly higher than that in sewage (0.077±0.045). Furthermore, MRSA's resistance to vancomycin in the air was also found to be greater than that of the corresponding isolates from sewage. The daily inhalation exposure to bacteria for workers at the wastewater treatment plant was estimated to be (1.9±1.5)×105 copies/d, with average exposure to ARGs and mobile genetic elements (MGEs) being calculated as (7.4±7.5)×104 copies/d and (0.8±1.0)×104 copies/d, respectively. The findings of this study were expected to provide scientific data for a comprehensive assessment of health risks associated with air quality in wastewater treatment plants and for the development of corresponding control strategies.
高珊珊, 刘硕, 李少斌, 魏泽冉, 辛会博, 田家宇, 高敏. 空气中耐药基因和致病菌逸散特征与暴露风险——以典型市政污水处理厂为例[J]. 中国环境科学, 2025, 45(4): 2276-2287.
GAO Shan-shan, LIU Shuo, LI Shao-bin, WEI Ze-ran, XIN Hui-bo, TIAN Jia-yu, GAO Min. The dispersion characteristics and exposure risks of antibiotic resistance genes and resistant pathogenic bacteria in air——Take a typical municipal sewage treatment plant as an example. CHINA ENVIRONMENTAL SCIENCECE, 2025, 45(4): 2276-2287.
[1] Chen X, Yang Y, Ke Y, et al. A comprehensive review on biodegradation of tetracyclines:Current research progress and prospect[J]. Science of the Total Environment, 2022,814,152852. [2] Watanabe N, Bergamaschi B A, Loftin K A, et al. Use and environmental occurrence of antibiotics in freestall dairy farms with manured forage fields[J]. Environment Science Technology, 2010, 44(17):6591-600. [3] Ding D, Wang B, Zhang X, et al. The spread of antibiotic resistance to humans and potential protection strategies[J]. Ecotoxicology and Environment Safety, 2023,254,114734. [4] Wu D, Zhao J, Su Y, et al. Explaining the resistomes in a megacity's water supply catchment:Roles of microbial assembly-dominant taxa, niched environments and pathogenic bacteria[J]. Water Research, 2023,228(Pt A),119359. [5] Mancuso G, Midiri A, Gerace E, et al. Bacterial antibiotic resistance:The most critical pathogens[J]. Pathogens, 2021,10(10):1310. [6] Ding L, Yang Y, Zheng C, et al. Activities of eravacycline, tedizolid, norvancomycin, nemonoxacin, ceftaroline, and comparators against 1,871Staphylococcus and 1,068Enterococcus species isolates from China:Updated report of the CHINET study 2019[J]. Microbiology Spectrum, 2022,10(6),e0171522. [7] Davis B C, Riquelme M V, Ramirez-Toro G, et al. Demonstrating an integrated antibiotic resistance gene surveillance approach in puerto rican watersheds post-hurricane maria[J]. Environment Science Technology, 2020,54(23):15108-15119. [8] Barrios R E, Bartelt-Hunt S L, Li Y, et al. Modeling the vertical transport of antibiotic resistance genes in agricultural soils following manure application[J]. Environmental Pollution, 2021,285,117480. [9] Zhang T, Li X, Wang M, et al. Time-resolved spread of antibiotic resistance genes in highly polluted air[J]. Environment International, 2019,127,333-339. [10] Xie W Y,Yuan Y,Wang Y T, et al.Hazard reduction and persistence of risk of antibiotic resistance during thermophilic composting of animal waste[J]. Journal of Environmental Management, 2023,330,117249. [11] Xin H, Gao M, Wang X, et al. Animal farms are hot spots for airborne antimicrobial resistance[J]. Science of the Total Environment, 2022, 851,158050. [12] Shi B, Zhao R, Su G, et al. Metagenomic surveillance of antibiotic resistome in influent and effluent of wastewater treatment plants located on the Qinghai-Tibetan Plateau[J]. Science of the Total Environment, 2023,870,162031. [13] Zhang R, Yang S, An Y, et al. Antibiotics and antibiotic resistance genes in landfills:A review[J]. Science of the Total Environment, 2022,806(Pt 2),150647. [14] Wang Y, Zhang S, Yang L, et al. Spatiotemporal distribution, interactions and toxic effect of microorganisms and ARGs/MGEs from the bioreaction tank in hospital sewage treatment facility[J]. Science of the Total Environment, 2024,923,171481. [15] Guo J, Li J, Chen H, et al. Metagenomic analysis reveals wastewater treatment plants as hotspots of antibiotic resistance genes and mobile genetic elements[J]. Water Research, 2017,123:468-478. [16] Han Y, Yang T, Xu G, et al. Characteristics and interactions of bioaerosol microorganisms from wastewater treatment plants[J]. Journal of Hazardous Materials, 2020,391,122256. [17] Yang T, Han Y, Zhang M, et al. Characteristics and exposure risks of potential pathogens and toxic metal (loid) s in aerosols from wastewater treatment plants[J]. Ecotoxicology Environmental Safety, 2019,183, 109543. [18] Xie J, Jin L, Wu D, et al. Inhalable antibiotic resistome from wastewater treatment plants to urban areas:Bacterial hosts, dissemination risks, and source contributions[J]. Environment Science Technology, 2022,56(11):7040-7051. [19] Yan C, Wang R-n, Zhao X-y. Emission characteristics of bioaerosol and quantitative microbiological risk assessment for equipping individuals with various personal protective equipment in a WWTP[J]. Chemosphere, 2021,265,129117. [20] Liang Z, Yu Y, Ye Z, et al. Pollution profiles of antibiotic resistance genes associated with airborne opportunistic pathogens from typical area, Pearl River Estuary and their exposure risk to human[J]. Environment International, 2020,143,105934. [21] Yang K, Li L, Wang Y, et al. Airborne bacteria in a wastewater treatment plant:Emission characterization, source analysis and health risk assessment[J]. Water Research, 2019,149:596-606. [22] Wang Y, Han Y, Li L, et al. Distribution, sources, and potential risks of antibiotic resistance genes in wastewater treatment plant:A review[J]. Environmental Pollution, 2022,310,119870. [23] Tian H, Liu J, Sun J, et al. Cross-media migration behavior of antibiotic resistance genes (ARGs) from municipal wastewater treatment systems (MWTSs):Fugitive characteristics, sharing mechanisms, and aerosolization behavior[J]. Science of the Total Environment, 2023,893,164710. [24] Wang Y, Wang C, Song L. Distribution of antibiotic resistance genes and bacteria from six atmospheric environments:Exposure risk to human[J]. Science of the Total Environment, 2019,694,133750. [25] 王凡,武亚林,徐井旭,等.北京市污水处理厂出水中典型抗生素药物的浓度水平[J].环境科学, 2024:1-13. Wang F, Wu Y L, Xu J X, et al. Concentration levels of typical antibiotic drugs in the effluent of sewage treatment plants in Beijing[J]. Environmental Science, 2024:1-13. [26] Xie J, Jin L, He T, et al. Bacteria and antibiotic resistance genes (ARGs) in PM2.5 from China:Implications for human exposure[J]. Environment Science Technology, 2019,53(2):963-972. [27] Knights D, Kuczynski J, Charlson E S, et al. Bayesian community-wide culture-independent microbial source tracking[J]. Nature Methods, 2011,8(9):761-763. [28] Li J, Zhou L, Zhang X, et al. Bioaerosol emissions and detection of airborne antibiotic resistance genes from a wastewater treatment plant[J]. Atmospheric Environment, 2016,124:404-412. [29] Yang T, Jiang L, Bi X, et al. Submicron aerosols share potential pathogens and antibiotic resistomes with wastewater or sludge[J]. Science of the Total Environ, 2022,821,153521. [30] Xie Y W, Yu C S, Li FF, et al. Distribution characteristics of antibiotics and antibiotic resistance genes in wastewater treatment plants[J]. Environment Science, 2021,42(1):315-322. [31] Wen Q, Yang L, Duan R, et al. Monitoring and evaluation of antibiotic resistance genes in four municipal wastewater treatment plants in Harbin, Northeast China[J]. Environmental Pollution, 2016,212:34-40. [32] 张欢欢,贲伟伟,邵天华,等.升级A/O工艺污水处理系统中抗生素抗性基因的分布与去除研究[J].环境科学学报, 2020,40(4):1160-1166. Zhang H H, Ben W W, Shao T H, et al. Study on distribution and removal of antibiotic resistance genes in upgraded A/O process wastewater treatment system[J]. Acta Scientiae Circumstantiae, 2020, 40(4):1160-1166. [33] Sabri N A, van Holst S, Schmitt H, et al. Fate of antibiotics and antibiotic resistance genes during conventional and additional treatment technologies in wastewater treatment plants[J]. Science of the Total Environment, 2020,741,140199. [34] Wang Y, Yang K, Li L, et al. Change characteristics, bacteria host, and spread risks of bioaerosol ARGs/MGEs from different stages in sewage and sludge treatment process[J]. Journal of Hazardous Materials, 2024,469,134011. [35] Zhang Q Q, Ying G G, Pan C G, et al. Comprehensive evaluation of antibiotics emission and fate in the river basins of China:source analysis, multimedia modeling, and linkage to bacterial resistance[J]. Environmental Science Technology, 2015,49(11):6772-82. [36] Luo Y, Xu L, Rysz M, et al. Occurrence and transport of tetracycline, sulfonamide, quinolone, and macrolide antibiotics in the Haihe River Basin, China[J]. Environmental Science Technology, 2011,45(5):1827-1833. [37] Szulc J, Okrasa M, Majchrzycka K, et al. Microbiological and toxicological hazards in sewage treatment plant bioaerosol and dust[J]. Toxins (Basel), 2021,13(10),691. [38] Yang Y, Chen Y, Cai Y, et al. The relationship between culturable doxycycline-resistant bacterial communities and antibiotic resistance gene hosts in pig farm wastewater treatment plants[J]. Ecotoxicology Environmental Safety, 2020,206,111164. [39] Gangamma S, Patil R S, Mukherji S. Characterization and proinflammatory response of airborne biological particles from wastewater treatment plants[J]. Environmental Science Technology, 2011,45(8):3282-3287. [40] Royer G, Roisin L, Demontant V, et al. Microdiversity of enterococcus faecalis isolates in cases of infective endocarditis:selection of non-synonymous mutations and large deletions is associated with phenotypic modifications[J]. Emerging Microbes Infections, 2021,10(1):929-938. [41] Zhao S, Liu Y, Chang J, et al. Bioaerosols in deodorization covers of wastewater treatment plants:Emission characteristics and health risks[J]. Chemosphere, 2024,353,141552. [42] Puljko A, Barišić I, Dekić Rozman S, et al. Molecular epidemiology and mechanisms of carbapenem and colistin resistance in Klebsiella and other Enterobacterales from treated wastewater in Croatia[J]. Environmental International, 2024,185,108554. [43] Zhu L, Zhao Y, Yang K, et al. Host bacterial community of MGEs determines the risk of horizontal gene transfer during composting of different animal manures[J]. Environmental Pollution, 2019,250:166-174. [44] Zarei-Baygi A,Smith AL.Intracellular versus extracellular antibiotic resistance genes in the environment:Prevalence, horizontal transfer, and mitigation strategies[J]. Bioresource Technology, 2021,319, 124181. [45] Li Z, Wan C, Liu X, et al. Understanding of the mechanism of extracellular polymeric substances of aerobic granular sludge against tetracycline from the perspective of fluorescence properties[J]. Science of the Total Environment, 2021,756,144054. [46] Hu X R, Han M F, Wang C, et al. A short review of bioaerosol emissions from gas bioreactors:Health threats, influencing factors and control technologies[J]. Chemosphere, 2020,253,126737. [47] Zhang J, Chen M, Sui Q, et al. Fate of antibiotic resistance genes and its drivers during anaerobic co-digestion of food waste and sewage sludge based on microwave pretreatment[J]. Bioresource Technology, 2016,217:28-36. [48] Wang Y, Yang L, Wild O, et al. ADMS simulation and influencing factors of bioaerosol diffusion from BRT under different aeration modes in six wastewater treatment plants[J]. Water Research, 2023, 231,119624. [49] Davin-Regli A, Lavigne J P, Pagès J M. Enterobacter spp.:Update on taxonomy, clinical aspects, and emerging antimicrobial resistance[J]. Clinical Microbiology Reviews, 2019,32(4):2-19. [50] Herrera-Hidalgo L, Fernández-Rubio B, Luque-Márquez R, et al. Treatment of Enterococcus faecalis infective endocarditis:A continuing challenge[J]. Antibiotics (Basel), 2023,12(4),704. [51] Yang T, Han Y, Liu J, et al. Aerosols from a wastewater treatment plant using oxidation ditch process:Characteristics, source apportionment, and exposure risks[J]. Environmental Pollution, 2019,250:627-638. [52] Sun H, Liu J, Tan S, et al. Spatiotemporal distribution of bacterial dimethylsulfoniopropionate producing and catabolic genes in the Changjiang Estuary[J]. Environmental Microbiology, 2021,23(11):7073-7092. [53] Frank D N, Feazel L M, Bessesen M T, et al. The human nasal microbiota and Staphylococcus aureus carriage[J]. PLoS ONE, 2010, 5(5),e10598. [54] Dinu V, Lu Y, Weston N, et al. The antibiotic vancomycin induces complexation and aggregation of gastrointestinal and submaxillary mucins[J]. Scientific Reports, 2020,10(1),960. [55] Xin H,Gao M,Wang X, et al.Animal farms are hot spots for airborne antimicrobial resistance[J]. Science of the Total Environment, 2022, 851(Pt 1), 158050. [56] Brito IL.Examining horizontal gene transfer in microbial communities[J]. Nature Reviews Microbiology, 2021,19(7):442-453. [57] Makowska N, Koczura R, Mokracka J. Class 1 integrase, sulfonamide and tetracycline resistance genes in wastewater treatment plant and surface water[J]. Chemosphere, 2016,144:1665-1673.