Reductions of bacterial antibiotic resistance through five biological ...

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Jul 6, 2016 - biological treatment processes treated municipal wastewater. Qing-Bin Yuan1,2 .... tetQ, tetW, sulI, and sulII) by three advanced treatment pro-.
Environ Sci Pollut Res (2016) 23:19495–19503 DOI 10.1007/s11356-016-7048-8

RESEARCH ARTICLE

Reductions of bacterial antibiotic resistance through five biological treatment processes treated municipal wastewater Qing-Bin Yuan 1,2 & Mei-Ting Guo 2 & Wu-Ji Wei 1 & Jian Yang 2

Received: 25 December 2015 / Accepted: 6 June 2016 / Published online: 6 July 2016 # Springer-Verlag Berlin Heidelberg 2016

Abstract Wastewater treatment plants are hot spots for antibiotic-resistant bacteria (ARB) and antibiotic resistance genes (ARGs). However, limited studies have been conducted to compare the reductions of ARB and ARGs by various biological treatment processes. The study explored the reductions of heterotrophic bacteria resistant to six groups of antibiotics (vancomycin, gentamicin, erythromycin, cephalexin, tetracycline, and sulfadiazine) and corresponding resistance genes (vanA, aacC1, ereA, ampC, tetA, and sulI) by five benchscale biological reactors. Results demonstrated that membrane bioreactor (MBR) and sequencing batch reactor (SBR) significantly reduced ARB abundances in the ranges of 2.80∼3.54 log and 2.70∼3.13 log, respectively, followed by activated sludge (AS). Biological filter (BF) and anaerobic (upflow anaerobic sludge blanket, UASB) techniques led to relatively low reductions. In contrast, ARGs were not equally reduced as ARB. AS and SBR also showed significant potentials on ARGs reduction, whilst MBR and UASB could not reduce ARGs effectively. Redundancy analysis implied that the purification of wastewater quality parameters (COD, NH4+-N, and turbidity) performed a positive correlation to ARB and ARGs reductions.

Responsible editor: Gerald Thouand Electronic supplementary material The online version of this article (doi:10.1007/s11356-016-7048-8) contains supplementary material, which is available to authorized users. * Mei-Ting Guo [email protected]

1

College of Environment, Nanjing Tech University, Nanjing, Jiangsu 211800, China

2

College of Environmental Science and Engineering, Tongji University, Shanghai 200092, China

Keywords Antibiotic-resistant bacteria . Antibiotic resistance genes . Reduction . Biological treatment process . Municipal wastewater . Redundancy analysis

Introduction Wastewater treatment plants (WWTPs) are considered as important reservoirs of antibiotic-resistant bacteria (ARB) and antibiotic resistance genes (ARGs) (Rizzo et al. 2013; Pruden 2014). Wastewater provides a favorable environment, including high contents of microbial biomass, relatively abundant nutrients and antibiotic agents, for both the ARB survival and the ARGs transfer (Guardabassi et al. 2002; Rizzo et al. 2013). Bacteria including many pathogens (e.g., enterobacteria, enterococci, Staphylococcus aureus, and Aeromonas) resistant to nearly all clinically relevant antibio t i c s h av e b ee n re p o r t e d i n W W T P s w o r l d w i d e (Guardabassi et al. 2002; Castiglioni et al. 2008; Borjesson et al. 2009; Novo and Manaia 2010; Reinthaler et al. 2010). More than 140 ARGs have also been detected in WWTPs up to 2009 (Szczepanowski et al. 2009; Zhang et al. 2009). Because WWTPs are not specially designed for the removal of ARB and ARGs (Pruden et al. 2013), their excess sludge biomass and effluents still contain large amounts of the contaminants (Reinthaler et al. 2003; Borjesson et al. 2009; Novo and Manaia 2010), which transfer to the subsequent environments and impose great potential threats on public health. Controlling antibiotic resistance in WWTPs is of great concerns of microbiologists and wastewater engineers (Rizzo et al. 2013). Wastewater disinfection, as a pathogen inactivation process, is considered as an important barrier to limit the release of ARB and ARGs into the environment (Guo et al. 2013b). However, the general observation is that the disinfection adopted in WWTPs shows limited efficacy on antibiotic

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resistance reduction. Some kinds of ARB are reported to express tolerance to chlorination (Huang et al. 2011; Yuan et al. 2015a), causing them difficult to be removed. Ultraviolet (UV) disinfection is also frequently reported for a weak reduction of ARB or ARGs (Munir et al. 2011; Guo et al. 2013a; Zhang et al. 2015). The limited reduction by chlorination and UV disinfection possibly partly attributes to the excessive abundances of ARB or ARGs. Increasing the dose usually contribute to the significant improvement of reduction efficiency (Engemann et al. 2006; Macauley et al. 2006; Zhang et al. 2015). One lab-scale study noted that doubling the typical UV dose applied in WWTPs was required to destroy vanA, mecA, tetA, and ampC (McKinney and Pruden 2012). Apparently, a biological process with the effective reduction of ARB and ARGs is essential for the subsequent disinfection. Numerous studies have explored the effects of biological treatment on the reduction of antibiotic resistance level (Sharma et al. 2016). Christgen and colleagues used metagenomics approaches to contrast the fate of ARGs in anaerobic, aerobic, and anaerobic–aerobic sequence (AAS) bioreactors treating domestic wastewater (Christgen et al. 2015); they found that AAS and aerobic reactors were better than anaerobic units in reducing ARGs abundances. Result of Munir et al. (2011) indicated that membrane bioreactor displayed significantly higher removals of ARGs and ARB than conventional treatment plants. Chen and Zhang (2013) investigated the removal efficiencies of 6 ARGs (tetM, tetO, tetQ, tetW, sulI, and sulII) by three advanced treatment processes and found that constructed wetlands showed higher reductions (1∼3 log) than biological aerated filter (0.6∼1.2 log). However, most current studies are conducted in various WWTPs with different raw sewage and abiotic environments (Chen and Zhang 2013). The reduction of antibiotic resistance by various biological treatment processes with identical conditions is rarely reported. This possibly weakens the reliability of the comparison, since wastewater qualities and abiotic conditions are frequently reported to affect the ARB/ARGs fates during biological treatment processes (Mc Mahon et al. 2007; Novo et al. 2013; Yang et al. 2014; Yuan et al. 2014). On the other hand, the fate of ARGs in WWTPs was usually inconsistent with their ARB (Gao et al. 2012; Huang et al. 2014; Huang et al. 2015). The single exploration of ARB or ARGs might both make biases, since numerous genes usually encode resistance to the same antibiotic, and only a tiny minority ( 0.05). The purifications of COD, NH4+-N, and turbidity all exhibited positive correlations to ARB or ARG reductions. Biological processes with effective purifications of conventional wastewater quality parameters would partially contribute to the promotion of antibiotic resistance reduction. Acknowledgment This project was funded by the National Natural Science Foundation of China (51308399) and the Shanghai Natural Science Foundation (13ZR1443300). The authors would like to thank the engineers of the WWTP for their assistance in obtaining the wastewater samples.

References Al-Jassim N, Ansari MI, Harb M, Hong PY (2015) Removal of bacterial contaminants and antibiotic resistance genes by conventional wastewater treatment processes in Saudi Arabia: is the treated wastewater safe to reuse for agricultural irrigation? Water Res 73:277–290 Amann RI, Ludwig W, Schleifer K (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169 Blanch AR, Caplin JL, Iversen A, Kuhn I, Manero A, Taylor HD, Vilanova X (2003) Comparison of enterococcal populations related to urban and hospital wastewater in various climatic and geographic European regions. J Appl Microbiol 94:994–1002 Borjesson S, Melin S, Matussek A, Lindgren PE (2009) A seasonal study of the mecA gene and Staphylococcus aureus including methicillinresistant S. aureus in a municipal wastewater treatment plant. Water Res 43:925–932 Breazeal MV, Novak JT, Vikesland PJ, Pruden A (2013) Effect of wastewater colloids on membrane removal of antibiotic resistance genes. Water Res 47:130–140 Castiglioni S, Pomati F, Miller K, Burns BP, Zuccato E, Calamari D, Neilan BA (2008) Novel homologs of the multiple resistance regulator marA in antibiotic-contaminated environments. Water Res 42: 4271–4280 Chen H, Zhang M (2013) Effects of advanced treatment systems on the removal of antibiotic resistance genes in wastewater treatment plants from Hangzhou, China. Environ Sci Technol 47:8157–8163 Chen J, Liu YS, Su HC, Ying GG, Liu F, Liu SS, He LY, Chen ZF, Yang YQ, Chen FR (2015) Removal of antibiotics and antibiotic resistance genes in rural wastewater by an integrated constructed wetland. Environ Sci Pollut Res 22: 1794–1803 Cheng SF, Lee YC, Kuo CY, Wu TN (2015) A case study of antibiotic wastewater treatment by using a membrane biological reactor system. Int Biodeterior Biodegrad 102:398–401

19502 Christgen B, Yang Y, Ahammad SZ, Li B, Rodriquez DC, Zhang T, Graham DW (2015) Metagenomics shows that low-energy anaerobic–aerobic treatment reactors reduce antibiotic resistance gene levels from domestic wastewater. Environ Sci Technol 49:2577– 2584 Clinical and Laboratory Standards Institute (CLSI) (2011) Performance standards for antimicrobial susceptibility testing: twenty-first informational supplement, 31 Dodd MC (2012) Potential impacts of disinfection processes on elimination and deactivation of antibiotic resistance genes during water and wastewater treatment. J Environ Monit 14:1754–1771 Du J, Geng J, Ren H, Ding L, Xu K, Zhang Y (2014) Variation of antibiotic resistance genes in municipal wastewater treatment plant with A2O-MBR system. Environ Sci Pollut Res 22:3715–3726 Engemann CA, Adams L, Knapp CW, Graham DW (2006) Disappearance of oxytetracycline resistance genes in aquatic systems. FEMS Microbiol Lett 263:176–182 Gao P, Munir M, Xagoraraki I (2012) Correlation of tetracycline and sulfonamide antibiotics with corresponding resistance genes and resistant bacteria in a conventional municipal wastewater treatment plant. Sci Total Environ 421-422:173–183 Guardabassi L, Lo Fo Wong DMA, Dalsgaard A (2002) The effects of tertiary wastewater treatment on the prevalence of antimicrobial resistant bacteria. Water Res 36:1955–1964 Guo MT, Yuan QB, Yang J (2013a) Microbial selectivity of UV treatment on antibiotic-resistant heterotrophic bacteria in secondary effluents of a municipal wastewater treatment plant. Water Res 47:6388–6394 Guo MT, Yuan QB, Yang J (2013b) Ultraviolet reduction of erythromycin and tetracycline resistant heterotrophic bacteria and their resistance genes in municipal wastewater. Chemosphere 93:2864–2868 Guo MT, Yuan QB, Yang J (2015) Insights into the amplification of bacterial resistance to erythromycin in activated sludge. Chemosphere 136:79–85 HØiby N, Bjarnsholt T, Givskov M, Molin S, Oana C (2010) Antibiotic resistance of bacterial biofilm. Int J Antimicrob Agents 25:322–332 Huang JJ, Hu HY, Tang F, Li Y, Lu SQ, Lu Y (2011) Inactivation and reactivation of antibiotic-resistant bacteria by chlorination in secondary effluents of a municipal wastewater treatment plant. Water Res 45:2775–2781 Huang MH, Zhang W, Zheng Y, Zhang W (2014) Correlation among extracellular polymeric substances, tetracycline resistant bacteria and tetracycline resistance genes under trace tetracycline. Chemosphere 117:658–662 Huang MH, Zhang W, Liu C, Hu HY (2015) Fate of trace tetracycline with resistant bacteria and resistance genes in an improved AAO wastewater treatment plant. Process Saf Environ Prot 93:68–74 Macauley JJ, Qiang Z, Adams CD, Surampalli R, Mormile MR (2006) Disinfection of swine wastewater using chlorine, ultraviolet light and ozone. Water Res 40:2017–2026 Mc Mahon MA, Blair IS, Moore JE, Mc Dowell DA (2007) The rate of horizontal transmission of antibiotic resistance plasmids is increased in food preservation-stressed bacteria. J Appl Microbiol 103:1883– 1888 McKinney CW, Pruden A (2012) Ultraviolet disinfection of antibiotic resistant bacteria and their antibiotic resistance genes in water and wastewater. Environ Sci Technol 46:13393–13400 Munir M, Wong K, Xagoraraki I (2011) Release of antibiotic resistant bacteria and genes in the effluent and biosolids of five wastewater utilities in Michigan. Water Res 45:681–693 Novo A, Manaia CM (2010) Factors influencing antibiotic resistance burden in municipal wastewater treatment plants. Appl Microbiol Biotechnol 87:1157–1166

Environ Sci Pollut Res (2016) 23:19495–19503 Novo A, Andre S, Viana P, Nunes OC, Manaia CM (2013) Antibiotic resistance, antimicrobial residues and bacterial community composition in urban wastewater. Water Res 47:1875–1887 Pruden A (2014) Balancing water sustainability and public health goals in the face of growing concerns about antibiotic resistance. Environ Sci Technol 48:5–14 Pruden A, Larsson DG, Amezquita A, Collignon P, Brandt KK, Graham DW, Lazorchak JM, Suzuki S, Silley P, Snape JR, Topp E, Zhang T, Zhu YG (2013) Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environ Health Perspect 121:878–885 Reinthaler FF, Posch J, Feierl G, Wüst G, Haas D, Ruckenbauer G, Mascher F, Marth E (2003) Antibiotic resistance of E. coli in sewage and sludge. Water Res 37:1685–1690 Reinthaler FF, Feierl G, Galler H, Haas D, Leitner E, Mascher F, Melkes A, Posch J, Winter I, Zarfel G, Marth E (2010) ESBL-producing E. coli in Austrian sewage sludge. Water Res 44:1981–1985 Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy MC, Michael I, Fatta-Kassinos D (2013) Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci Total Environ 447C:345–360 Sharma VK, Johnson N, Cizmas L, McDonald TJ, Kim H (2016) A review of the influence of treatment strategies on antibiotic resistant bacteria and antibiotic resistance genes. Chemosphere 150:702–714 Smith AL, Skerlos SJ, Raskin L (2013) Psychrophilic anaerobic membrane bioreactor treatment of domestic wastewater. Water Res 47: 1655–1665 Szczepanowski R, Linke B, Krahn I, Gartemann KH, Gutzkow T, Eichler W, Puhler A, Schluter A (2009) Detection of 140 clinically relevant antibiotic-resistance genes in the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to selected antibiotics. Microbiology 155:2306–2319 Tao CW, Hsu BM, Ji WT, Hsu TK, Kao PM, Hsu CP, Shen SM, Shen TY, Wan TJ, Huang YL (2014) Evaluation of five antibiotic resistance genes in wastewater treatment systems of swine farms by real-time PCR. Sci Total Environ 496:116–121 Threedeach S, Chiemchaisri W, Watanabe T, Chiemchaisri C, Honda R, Yamamoto K (2012) Antibiotic resistance of Escherichia coli in leachates from municipal solid waste landfills: comparison between semi-aerobic and anaerobic operations. Bioresour Technol 113:253–258 Wang J, Mao D, Mu Q, Luo Y (2015) Fate and proliferation of typical antibiotic resistance genes in five full-scale pharmaceutical wastewater treatment plants. Sci Total Environ 526:366– 373 Yang D, Wang J, Qiu Z, Jin M, Shen Z, Chen Z, Wang X, Zhang B, Li JW (2013) Horizontal transfer of antibiotic resistance genes in a membrane bioreactor. J Biotechnol 167:441–447 Yang CW, Chang YT, Chao WL, Shiung II, Lin HS, Chen H, Ho SH, Lu MJ, Lee PH, Fan SN (2014) An investigation of total bacterial communities, culturable antibiotic-resistant bacterial communities and integrons in the river water environments of Taipei city. J Hazard Mater 277:159–168 Yuan QB, Guo MT, Yang J (2014) Monitoring and assessing the impact of wastewater treatment on release of both antibiotic-resistant bacteria and their typical genes in a Chinese municipal wastewater treatment plant. Environ Sci Process Impacts 16:1930–1937 Yuan QB, Guo MT, Yang J (2015a) Fate of antibiotic resistant bacteria and genes during wastewater chlorination: implication for antibiotic resistance control. PLoS One 10:e0119403 Yuan QB, Guo MT, Yang J (2015b) The sludge loading rate regulates the growth and release of heterotrophic bacteria resistant to six types of

Environ Sci Pollut Res (2016) 23:19495–19503 antibiotics in wastewater activated sludge. Environ Sci Process Impacts 17:206–212 Zhang XX, Zhang T, Fang HH (2009) Antibiotic resistance genes in water environment. Appl Microbiol Biotechnol 82:397–414

19503 Zhang Y, Zhuang Y, Geng J, Ren H, Zhang Y, Ding L, Xu K (2015) Inactivation of antibiotic resistance genes in municipal wastewater effluent by chlorination and sequential UV/chlorination disinfection. Sci Total Environ 512-513:125–132

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