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Occurrence and prevalence of antibiotic resistance in landfill leachate

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Abstract

Antibiotic resistance (AR) is extensively present in various environments, posing emerging threat to public and environmental health. Landfill receives unused and unwanted antibiotics through household waste and AR within waste (e.g., activated sludge and illegal clinical waste) and is supposed to serve as an important AR reservoir. In this study, we used culture-dependent methods and quantitative molecular techniques to detect and quantify antibiotic-resistant bacteria (ARB) and antibiotic resistance genes (ARGs) in 12 landfill leachate samples from six geographic different landfills, China. Five tested ARGs (tetO, tetW, bla TEM, sulI, and sulII) and seven kinds of antibiotic-resistant heterotrophic ARB were extensively detected in all samples, demonstrating their occurrence in landfill. The detected high ratio (10−2 to 10−5) of ARGs to 16S ribosomal RNA (rRNA) gene copies implied that ARGs are prevalent in landfill. Correlation analysis showed that ARGs (tetO, tetW, sulI, and sulII) significantly correlated to ambient bacterial 16S rRNA gene copies, suggesting that the abundance of bacteria in landfill leachate may play an important role in the horizontal spread of ARGs.

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References

  • APHA (1998) Standard methods for the evaluation of water and wastewater. American Public Health Association Publishing, Washington

    Google Scholar 

  • Barlaz MA (1997) Microbial studies of landfills and anaerobic refuse decomposition. Man Environ Microbiol 541–557

  • Barlaz MA, Schaefer DM, Ham RK (1989) Bacterial population development and chemical characteristics of refuse decomposition in a simulated sanitary landfill. Appl Environ Microbiol 55:55–65

    CAS  Google Scholar 

  • Bound JP, Voulvoulis N (2005) Household disposal of pharmaceuticals as a pathway for aquatic contamination in the United Kingdom. Environ Health Perspect 1705–1711

  • Chen H, Zhang M (2013) Occurrence and removal of antibiotic resistance genes in municipal wastewater and rural domestic sewage treatment systems in eastern China. Environ Int 55:9–14

    Article  CAS  Google Scholar 

  • China SEPAo (2002) Monitoring and analysis method of water and waste water. China Environmental Science Press, Beijing

    Google Scholar 

  • Courvalin P (1994) Transfer of antibiotic resistance genes between gram-positive and gram-negative bacteria. Antimicrob Agents Chemother 38:1447

    Article  CAS  Google Scholar 

  • Garcia-Armisen T, Vercammen K, Passerat J, Triest D, Servais P, Cornelis P (2011) Antimicrobial resistance of heterotrophic bacteria in sewage-contaminated rivers. Water Res 45:788–796

    Article  CAS  Google Scholar 

  • Graham DW, Olivares-Rieumont S, Knapp CW, Lima L, Werner D, Bowen E (2010) Antibiotic resistance gene abundances associated with waste discharges to the Almendares River near Havana, Cuba. Environ Sci Technol 45:418–424

    Article  Google Scholar 

  • Hammer Ø, Harper D, Ryan P (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontolia Electron 4

  • Huang Z (2014) Study of migration, transformation and removal of antibiotic residues and antibiotic resistance genes in the process of municipal solid waste transfer and landfilling. East China Normal University

  • Institute of Clinical and Laboratory Standards (2006) Performance standards for antimicrobial disk susceptibility tests. 9th ed. Approved standard M2-A9, Clinical and Laboratory Standards Institute, Wayne, PA

  • Kim S, Aga DS (2007) Potential ecological and human health impacts of antibiotics and antibiotic-resistant bacteria from wastewater treatment plants. J Toxicol Env Heal B 10:559–573

    Article  CAS  Google Scholar 

  • Kjeldsen P, Barlaz MA, Rooker AP, Baun A, Ledin A, Christensen TH (2002) Present and long-term composition of MSW landfill leachate: a review. Crit Rev Environ Sci Technol 32:297–336

    Article  CAS  Google Scholar 

  • Knapp CW, Dolfing J, Ehlert PA, Graham DW (2009) Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ Sci Technol 44:580–587

    Article  Google Scholar 

  • Kotchen M, Kallaos J, Wheeler K, Wong C, Zahller M (2009) Pharmaceuticals in wastewater: behavior, preferences, and willingness to pay for a disposal program. J Environ Manag 90:1476–1482

    Article  Google Scholar 

  • Kümmerer K (2003) Significance of antibiotics in the environment. J Antimicrob Chemother 52:5–7

    Article  Google Scholar 

  • Lachmayr KL, Kerkhof LJ, DiRienzo AG, Cavanaugh CM, Ford TE (2009) Quantifying nonspecific TEM β-lactamase (blaTEM) genes in a wastewater stream. Appl Environ Microbiol 75:203–211

    Article  CAS  Google Scholar 

  • Liu L, Liu YH, Wang Z, Liu CX, Huang X, Zhu GF (2014) Behavior of tetracycline and sulfamethazine with corresponding resistance genes from swine wastewater in pilot-scale constructed wetlands. J Hazard Mater 278:304–310

    Article  CAS  Google Scholar 

  • Livermore DM (1995) Beta-lactamases in laboratory and clinical resistance. Clin Microbiol Rev 8:557–584

    CAS  Google Scholar 

  • Luo Y, Mao D, Rysz M, Zhou Q, Zhang H, Xu LJJ, Alvarez P (2010) Trends in antibiotic resistance genes occurrence in the Haihe River, China. Environ Sci Technol 44:7220–7225

    Article  Google Scholar 

  • Mackie RI, Koike S, Krapac I, Chee-Sanford J, Maxwell S, Aminov RI (2006) Tetracycline residues and tetracycline resistance genes in groundwater impacted by swine production facilities. Anim Biotechnol 17:157–176

    Article  CAS  Google Scholar 

  • Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64:795–799

    CAS  Google Scholar 

  • Martinez JL (2009) Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 157:2893–2902

    Article  CAS  Google Scholar 

  • Mazel D (2004) Integrons and the origin of antibiotic resistance gene cassettes-super integrons with thousands of gene cassettes may have set the stage for pathogens to develop antibiotic resistance very rapidly. ASM News-Am Soc Microbiol 70:520–525

    Google Scholar 

  • Metzger J (2004) Drugs in municipal landfills and landfill leachates, Pharmaceuticals in the environment. Springer pp 133–137

  • Michigan Department of Environmental Quality (2007) A remedy for residential drug disposal, Michigan Department of Environmental Quality, Lansing, Michigan

  • 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

    Article  CAS  Google Scholar 

  • Musson SE, Townsend TG (2009) Pharmaceutical compound content of municipal solid waste. J Hazard Mater 162:730–735

    Article  CAS  Google Scholar 

  • Office of National Drug Control Policy (2007) Proper disposal of prescription drugs, executive office of the president of the United States. Office of National Drug Control Policy, Washington

    Google Scholar 

  • Peak N, Knapp CW, Yang RK, Hanfelt MM, Smith MS, Aga DS, Graham DW (2007) Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies. Environ Microbiol 9:143–151

    Article  CAS  Google Scholar 

  • Pei R, Kim S-C, Carlson KH, Pruden A (2006) Effect of river landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Res 40:2427–2435

    Article  CAS  Google Scholar 

  • Pruden A, Pei R, Storteboom H, Carlson KH (2006) Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ Sci Technol 40:7445–7450

    Article  CAS  Google Scholar 

  • Sarmah AK, Meyer MT, Boxall ABA (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65:725–759

    Article  CAS  Google Scholar 

  • Schmitt H, Stoob K, Hamscher G, Smit E, Seinen W (2006) Tetracyclines and tetracycline resistance in agricultural soils: microcosm and field studies. Microb Ecol 51:267–276

    Article  Google Scholar 

  • Scott KP, Melville CM, Barbosa TM, Flint HJ (2000) Occurrence of the new tetracycline resistance gene tet (W) in bacteria from the human gut. Antimicrob Agents Chemother 44:775–777

    Article  CAS  Google Scholar 

  • Sköld O (2000) Sulfonamide resistance: mechanisms and trends. Drug Resist Updat 3:155–160

    Article  Google Scholar 

  • Song LY, Zhao YC, Sun WM, Lou ZY (2009) Hydrophobic organic chemicals (HOCs) removal from biologically treated landfill leachate by powder-activated carbon (PAC), granular-activated carbon (GAC) and biomimetic fat cell (BFC). J Hazard Mater 163:1084–1089

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wu P, Shannon K, Phillips I (1994) Effect of hyperproduction of TEM-1 beta-lactamase on in vitro susceptibility of Escherichia coli to beta-lactam antibiotics. Antimicrob Agents Chemother 38:494–498

    Article  CAS  Google Scholar 

  • Wu N, Qiao M, Zhang B, Cheng W-D, Zhu Y-G (2010) Abundance and diversity of tetracycline resistance genes in soils adjacent to representative swine feedlots in China. Environ Sci Technol 44:6933–6939

    Article  CAS  Google Scholar 

  • Xi C, Zhang Y, Marrs CF, Ye W, Simon C, Foxman B, Nriagu J (2009) Prevalence of antibiotic resistance in drinking water treatment and distribution systems. Appl Environ Microbiol 75:5714–5718

    Article  CAS  Google Scholar 

  • Zhang Y, Marrs CF, Simon C, Xi C (2009) Wastewater treatment contributes to selective increase of antibiotic resistance among Acinetobacter spp. Sci Total Environ 407:3702–3706

    Article  CAS  Google Scholar 

  • Zhu Y-G, Johnson TA, Su J-Q, Qiao M, Guo G-X, Stedtfeld RD, Hashsham SA, Tiedje JM (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci 110:3435–3440

    Article  CAS  Google Scholar 

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Acknowledgments

The authors acknowledge the Chinese Academy of Science, China, for financial support for the research with Contract No KZCX2-XB3-14. We would like to thank the anonymous reviewers for offering valuable suggestions that greatly improved the manuscript.

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Correspondence to Liyan Song.

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Responsible editor: Leif Kronberg

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Wang, Y., Tang, W., Qiao, J. et al. Occurrence and prevalence of antibiotic resistance in landfill leachate. Environ Sci Pollut Res 22, 12525–12533 (2015). https://doi.org/10.1007/s11356-015-4514-7

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  • DOI: https://doi.org/10.1007/s11356-015-4514-7

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