Skip to main content

Advertisement

SpringerLink
Log in

Quantification and characterization of β-lactam resistance genes in 15 sewage treatment plants from East Asia and North America

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The emerging antibiotic resistance genes in the aquatic environment have aroused public concern. As β-lactam is the most widely used group of antibiotics, β-lactam resistance genes were selected to investigate their distribution and diversity in the activated sludge from 15 geographically different sewage treatment plants (STPs) of China, Singapore, USA, and Canada. Specific PCR and quantitative real-time PCR (q-PCR) were used to investigate the occurrence and abundance of nine β-lactam resistance genes. Five genes (OXA-1, OXA-2, OXA-10, ampC, and TEM-1) were detected in most of the sludge collected, while three genes (mecA, CTX-M-1, and SME) were not found in any sludge sample. The total abundances of the six detected β-lactam resistance genes in the 15 STPs varied from 5.34 × 101 copies/ng DNA (ampC) to 5.49 × 104 copies/ng DNA (OXA-1). Overall, OXA-1 had the highest total concentration, followed by IMP and OXA-10. Noticeably, the abundances of TEM-1 in Chinese STPs were generally higher than those in the STPs of other countries, while the abundances of OXA-2 and IMP in the STPs of North America were much greater than those of East Asia. A total of 78 clones carrying β-lactam resistance genes were randomly selected from six clone libraries for phylogenetic diversity analysis; the similarity of these cloned genes to known β-lactam resistance genes with sequence identities ranged from 96% to 100%. Furthermore, OXA-1, ampC, and IMP were found to be more diverse than the other β-lactam resistance genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Reference

  • Auerbach EA, Seyfried EE, McMahon KD (2007) Tetracycline resistance genes in activated sludge wastewater treatment plants. Water Res 41:1143–1151

    Article  CAS  Google Scholar 

  • Bönemann G, Stiens M, Pühler A, Schlüter A (2006) Mobilizable IncQ-related plasmid carrying a new quinolone resistance gene, qnrS2, isolated from the bacterial community of a wastewater treatment plant. Antimicrob Agents Chemother 50:3075–3080

    Article  Google Scholar 

  • Cantón R, Coque T (2006) The CTX-M β-lactamase pandemic. Curr Opin Microbiol 9:466–475

    Article  Google Scholar 

  • Colomer-Lluch M, Jofre J, Muniesa M (2011) Antibiotic resistance genes in the bacteriophage DNA fraction of environmental samples. PLoS One 6(3):e17549. doi:10.1371/journal.pone.0017549

    Article  CAS  Google Scholar 

  • Davies J, Davies D (2010) Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74:417–433

    Article  CAS  Google Scholar 

  • Ding H, Yang YH, Chen Y, Wang Y, Fan SZ, She SZ (2008) Antimicrobial usage in paediatric intensive care units in China. Acta Pediatr 97:100–104

    Article  CAS  Google Scholar 

  • Faria C, Vaz-Moreira I, Serapicos E, Nunes OC, Manaia CM (2009) Antibiotic resistance in coagulase negative staphylococci isolated from wastewater and drinking water. Sci Total Environ 407:3876–3882

    Article  CAS  Google Scholar 

  • Grohskopf LA, Huskins WC, Sinkowitz-Cochran RL, Levine GL, Goldmann DA, Jarvis WR (2005) Use of antimicrobial agents in United States neonatal and pediatric intensive care patients. Pediatr Infect Dis J 24:766–773

    Article  Google Scholar 

  • Hawkey PM, Jones AM (2009) The changing epidemiology of resistance. J Antimicrob Chemother 64:i3–i10

    Article  CAS  Google Scholar 

  • Henriques I, Moura A, Alves A, Saavedra MJ, Correia A (2006) Analysing diversity among β-lactamase encoding genes in aquatic environments. FEMS Microbiol Ecol 56:418–429

    Article  CAS  Google Scholar 

  • Iversen A, Kuhn I, Franklin A, Mollby R (2002) High Prevalence of vancomycin-resistant Enterococci in Swedish sewage. Appl Environ Microbiol 68:2838–2842

    Article  CAS  Google Scholar 

  • Jury KL, Khan SJ, Vancov T, Stuetz RM, Ashbolt NJ (2011) Are sewage treatment plants promoting antibiotic resistance? Crit Rev Env Sci Technol 41:243–270

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Li D, Yang M, Hu J, Zhang J, Liu R, Gu X, Zhang Y, Wang ZY (2009) Antibiotic-resistance profile in environmental bacteria isolated from penicillin production wastewater treatment plant and the receiving river. Environ Microbiol 11:1506–1517

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Livermore DM (1996) Are all beta-lactams created equal? Scand J Infect Dis Suppl 101:33–43

    CAS  Google Scholar 

  • Livermore DM (1998) beta-Lactamase-mediated resistance and opportunities for its control. J Antimicrob Chemother 41:25–41

    Article  CAS  Google Scholar 

  • Moura A, Henriques I, Ribeiro R, Correia A (2007) Prevalence and characterization of integrons from bacteria isolated from a slaughterhouse wastewater treatment plant. J Antimicrob Chemother 60:1243–1250

    Article  CAS  Google Scholar 

  • Poole K (2004) Resistance to β-lactam antibiotics. Cell Mol Life Sci 61:2200–2223

    Article  CAS  Google Scholar 

  • Richardson BJ, Lam PKS, Martin M (2005) Emerging chemicals of concern: Pharmaceuticals and personal care products (PPCPs) in Asia, with particular reference to Southern China. Mar Pollut Bull 50:913–920

    Article  CAS  Google Scholar 

  • Sapkota AR, Curriero FC, Gibson KE, Schwab KJ (2007) Antibiotic-resistant enterococci and fecal indicators in surface water and groundwater impacted by a concentrated swine feeding operation. Environ Health Perspect 115:1040–1045

    Article  CAS  Google Scholar 

  • Schlüter A, Szczepanowski R, Kurz N, Schneiker S, Krahn I, Pühler A (2007a) Erythromycin resistance-conferring plasmid pRSB105, isolated from a sewage treatment plant, harbors a new macrolide resistance determinant, an integron-containing Tn402-like element, and a large region of unknown function. Appl Environ Microbiol 73:1952–1960

    Article  Google Scholar 

  • Schlüter A, Szczepanowski R, Pühler A, Top EM (2007b) Genomics of IncP-1 antibiotic resistance plasmids isolated from wastewater treatment plants provides evidence for a widely accessible drug resistance gene pool. FEMS Microbiol Rev 31:449–477

    Article  Google Scholar 

  • Schwartz T, Kohnen W, Jansen B, Obst U (2003) Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms. FEMS Microbiol Ecol 43:325–335

    Article  CAS  Google Scholar 

  • Szczepanowski R (2004) Antibiotic multiresistance plasmid pRSB101 isolated from a wastewater treatment plant is related to plasmids residing in phytopathogenic bacteria and carries eight different resistance determinants including a multidrug transport system. Microbiology 150:3613–3630

    Article  CAS  Google Scholar 

  • Szczepanowski R, Linke B, Krahn I, Gartemann KH, Gutzkow T, Eichler W, Pühler A, Schlüter 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

    Article  CAS  Google Scholar 

  • Tennstedt T, Szczepanowski R, Braun S, Pühler A, Schlüter A (2003) Occurrence of integron-associated resistance gene cassettes located on antibiotic resistance plasmids isolated from a wastewater treatment plant. FEMS Microbiol Ecol 45:239–252

    Article  CAS  Google Scholar 

  • Vandenesch F, Naimi T, Enright MC, Lina G, Nimmo GR, Heffernan H, Liassine N, Bes M, Greenland T, Reverdy ME, Etienne J (2003) Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 9:978–984

    Article  Google Scholar 

  • Volkmann H (2004) Detection of clinically relevant antibiotic-resistance genes in municipal wastewater using real-time PCR (TaqMan). J Microbiol Methods 56:277–286

    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 

  • Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, Walsh TR (2009) Characterization of a new metallo- -lactamase gene, bla NDM-1 , and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae Sequence Type 14 from India. Antimicrob Agents Chemother 53:5046–5054

    Article  CAS  Google Scholar 

  • Zhanel GG, Wang X, Nichol K, Nikulin A, Wierzbowski AK, Mulvey M, Hoban DJ (2006) Molecular characterisation of Canadian paediatric multidrug-resistant Streptococcus pneumoniae from 1998–2004. Int J Antimicro Ag 28:465–471

    Article  CAS  Google Scholar 

  • Zhang XX, Zhang T (2011) Occurrence, abundance, and diversity of tetracycline resistance genes in 15 sewage treatment plants across China and other global locations. Environ Sci Technol 45:2598–2604

    Article  CAS  Google Scholar 

  • Zhang T, Zhang M, Zhang XX, Fang HHP (2009a) Tetracycline resistance genes and tetracycline resistant lactose-fermenting Enterobacteriaceae in activated sludge of sewage treatment plants. Environ Sci Technol 43:3455–3460

    Article  CAS  Google Scholar 

  • Zhang XX, Zhang T, Fang HHP (2009b) Antibiotic resistance genes in water environment. Appl Microbiol Biotechnol 82:397–414

    Article  CAS  Google Scholar 

Download references

Acknowledgement

The authors wish to thank the Hong Kong Research Grants Council for the financial support of this study (HKU 7201/11E). We would like to thank Prof. Deng BL, Dr. Duan JZ, Mr. Yu K, and Mr. Ye L for the sludge sampling.

Author information

Authors and Affiliations

  1. Environmental Biotechnology Lab, Department of Civil Engineering, The University of Hong Kong, Pokfulam Road, Hong Kong SAR, China

    Ying Yang, Tong Zhang, Xu-Xiang Zhang & Herbert H. P. Fang

  2. School of Chemistry and Environment, Beihang University, Beijing, China

    Da-Wei Liang

  3. School of Resources and Environmental Science, East China Normal University, Shanghai, China

    Ming Zhang

  4. State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology, Harbin, China

    Da-Wen Gao

  5. Cestoil Chemical Inc., Toronto, Canada

    He-Guang Zhu

  6. Department of Crop and Soil Sciences, University of Georgia, Athens, GA, USA

    Qing-Guo Huang

Authors
  1. Ying Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xu-Xiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Da-Wei Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ming Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Da-Wen Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. He-Guang Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Qing-Guo Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Herbert H. P. Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tong Zhang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM. 1

(DOC 184 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yang, Y., Zhang, T., Zhang, XX. et al. Quantification and characterization of β-lactam resistance genes in 15 sewage treatment plants from East Asia and North America. Appl Microbiol Biotechnol 95, 1351–1358 (2012). https://doi.org/10.1007/s00253-011-3810-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-011-3810-5

Keywords

Search

Navigation