Skip to main content
SpringerLink
Log in

Abundance and distribution of antibiotic resistance genes in a full-scale anaerobic–aerobic system alternately treating ribostamycin, spiramycin and paromomycin production wastewater

  • Original Paper
  • Published:
Environmental Geochemistry and Health Aims and scope Submit manuscript

Abstract

The occurrence of antibiotic-resistant bacteria and antibiotic resistance genes (ARGs) has been intensively investigated for wastewater treatment systems treating single class of antibiotic in recent years. However, the impacts of alternately occurring antibiotics in antibiotic production wastewater on the behavior of ARGs in biological treatment systems were not well understood yet. Herein, techniques including high-capacity quantitative PCR and quantitative PCR (qPCR) were used to investigate the behavior of ARGs in an anaerobic–aerobic full-scale system. The system alternately treated three kinds of antibiotic production wastewater including ribostamycin, spiramycin and paromomycin, which referred to stages 1, 2 and 3. The aminoglycoside ARGs (52.1–79.3%) determined using high-capacity quantitative PCR were the most abundant species in all sludge samples of the three stages. The total relative abundances of macrolide–lincosamide–streptogramin (MLS) resistance genes and aminoglycoside resistance genes measured using qPCR were significantly higher (P < 0.05) in aerobic sludge than in sewage sludge. However, the comparison of ARGs acquired from three alternate stages revealed that MLS genes and the aminoglycoside ARGs did not vary significantly (P > 0.05) in both aerobic and anaerobic sludge samples. In aerobic sludge, one acetyltransferase gene (aacA4) and the other three nucleotidyltransferase genes (aadB, aadA and aadE) exhibited positive correlations with intI1 (r 2 = 0.83–0.94; P < 0.05), implying the significance of horizontal transfer in their proliferation. These results and facts will be helpful to understand the abundance and distribution of ARGs from antibiotic production wastewater treatment systems.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aydin, S., Ince, B., & Ince, O. (2015). Development of antibiotic resistance genes in microbial communities during long-term operation of anaerobic reactors in the treatment of pharmaceutical wastewater. Water Research, 83, 337–344.

    Article  CAS  Google Scholar 

  • Ben Said, L., Klibi, N., Lozano, C., Dziri, R., Ben Slama, K., Boudabous, A., et al. (2015). Diversity of enterococcal species and characterization of high-level aminoglycoside resistant enterococci of samples of wastewater and surface water in Tunisia. Science of the Total Environment, 530–531, 11–17.

    Article  Google Scholar 

  • Chen, J., Ying, G. G., Wei, X. D., Liu, Y. S., Liu, S. S., Hu, L. X., et al. (2016). Removal of antibiotics and antibiotic resistance genes from domestic sewage by constructed wetlands: Effect of flow configuration and plant species. Science of the Total Environment, 571, 974–982.

    Article  CAS  Google Scholar 

  • Chen, J., Yu, Z., Michel, F. C., Wittum, T., & Morrison, M. (2007). Development and application of real-time PCR assays for quantification of erm genes conferring resistance to macrolides–lincosamides–streptogramin B in livestock manure and manure management systems. Applied and Environmental Microbiology, 73(14), 4407–4416.

    Article  CAS  Google Scholar 

  • Devarajan, N., Laffite, A., Graham, N. D., Meijer, M., Prabakar, K., Mubedi, J. I., et al. (2015). Accumulation of clinically relevant antibiotic-resistance genes, bacterial load, and metals in freshwater lake sediments in Central Europe. Environmental Science and Technology, 49(11), 6528–6537.

    Article  CAS  Google Scholar 

  • Fernandez-Martinez, M., Miro, E., Ortega, A., Bou, G., Gonzalez-Lopez, J. J., Oliver, A., et al. (2015). Molecular identification of aminoglycoside-modifying enzymes in clinical isolates of Escherichia coli resistant to amoxicillin/clavulanic acid isolated in Spain. International Journal of Antimicrobial Agents, 46(2), 157–163.

    Article  CAS  Google Scholar 

  • Gillings, M., Boucher, Y., Labbate, M., Holmes, A., Krishnan, S., Holley, M., et al. (2008). The evolution of class 1 integrons and the rise of antibiotic resistance. Journal of Bacteriology, 190(14), 5095–5100.

    Article  CAS  Google Scholar 

  • Harb, M., Wei, C. H., Wang, N., Amy, G., & Hong, P. Y. (2016). Organic micropollutants in aerobic and anaerobic membrane bioreactors: Changes in microbial communities and gene expression. Bioresource Technology, 218, 882–891.

    Article  CAS  Google Scholar 

  • Koike, S., Aminov, R. I., Yannarell, A. C., Gans, H. D., Krapac, I. G., Chee-Sanford, J. C., et al. (2010). Molecular ecology of macrolide–lincosamide–streptogramin B methylases in waste lagoons and subsurface waters associated with swine production. Microbial Ecology, 59(3), 487–498.

    Article  CAS  Google Scholar 

  • Li, D., Yu, T., Zhang, Y., Yang, M., Li, Z., Liu, M. M., et al. (2010). Antibiotic resistance characteristics of environmental bacteria from an oxytetracycline production wastewater treatment plant and the receiving river. Applied and Environmental Microbiology, 76(11), 3444–3451.

    Article  CAS  Google Scholar 

  • Liu, M., Ding, R., Zhang, Y., Gao, Y., Tian, Z., Zhang, T., et al. (2014). Abundance and distribution of Macrolide–Lincosamide–Streptogramin resistance genes in an anaerobic–aerobic system treating spiramycin production wastewater. Water Research, 63, 33–41.

    Article  Google Scholar 

  • Liu, M., Zhang, Y., Yang, M., Tian, Z., Ren, L., & Zhang, S. (2012). Abundance and distribution of tetracycline resistance genes and mobile elements in an oxytetracycline production wastewater treatment system. Environmental Science and Technology, 46(14), 7551–7557.

    Article  CAS  Google Scholar 

  • Luby, E. M., Moorman, T. B., & Soupir, M. L. (2016). Fate and transport of tylosin-resistant bacteria and macrolide resistance genes in artificially drained agricultural fields receiving swine manure. Science of the Total Environment, 550, 1126–1133.

    Article  CAS  Google Scholar 

  • Ma, Y., Wilson, C. A., Novak, J. T., Riffat, R., Aynur, S., Murthy, S., et al. (2011). Effect of various sludge digestion conditions on sulfonamide, macrolide, and tetracycline resistance genes and class I integrons. Environmental Science and Technology, 45(18), 7855–7861.

    Article  CAS  Google Scholar 

  • Marti, E., Jofre, J., & Balcazar, J. L. (2013). Prevalence of antibiotic resistance genes and bacterial community composition in a river influenced by a wastewater treatment plant. PLoS ONE, 8(10), 1–8.

    Article  Google Scholar 

  • Mingeot-Leclercq, M. P., Glupczynski, Y., & Tulkens, P. M. (1999). Aminoglycosides: Activity and resistance. Antimicrobial Agents and Chemotherapy, 43(4), 727–737.

    CAS  Google Scholar 

  • Ramirez, M. S., & Tolmasky, M. E. (2010). Aminoglycoside modifying enzymes. Drug Resistance Updates: Reviews and Commentaries in Antimicrobial and Anticancer Chemotherapy, 13(6), 151–171.

    Article  CAS  Google Scholar 

  • Roberts, M. C., Sutcliffe, J., Courvalin, P., Jensen, L. B., Rood, J., & Seppala, H. (1999). Nomenclature for macrolide and macrolide–lincosamide–streptogramin B resistance determinants. Antimicrobial Agents and Chemotherapy, 43(12), 2823–2830.

    CAS  Google Scholar 

  • Schmittgen, T. D., & Livak, K. J. (2008). Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3(6), 1101–1108.

    Article  CAS  Google Scholar 

  • Schönfeld, W., & Kirst, H. A. (2002). Macrolide antibiotics (pp. 281–305). Berlin: Springer Basel AG.

  • Sidrach-Cardona, R., Hijosa-Valsero, M., Marti, E., Balcazar, J. L., & Becares, E. (2014). Prevalence of antibiotic-resistant fecal bacteria in a river impacted by both an antibiotic production plant and urban treated discharges. The Science of the Total Environment, 488–489, 220–227.

    Article  Google Scholar 

  • Su, J. Q., Wei, B., Ou-Yang, W. Y., Huang, F. Y., Zhao, Y., Xu, H. J., et al. (2015). Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environmental Science and Technology, 49(12), 7356–7363.

    Article  CAS  Google Scholar 

  • Tian, Z., Zhang, Y., Yu, B., & Yang, M. (2016). Changes of resistome, mobilome and potential hosts of antibiotic resistance genes during the transformation of anaerobic digestion from mesophilic to thermophilic. Water Research, 98, 261–269.

    Article  CAS  Google Scholar 

  • Topp, E., Renaud, J., Sumarah, M., & Sabourin, L. (2016). Reduced persistence of the macrolide antibiotics erythromycin, clarithromycin and azithromycin in agricultural soil following several years of exposure in the field. Science of the Total Environment, 562, 136–144.

    Article  CAS  Google Scholar 

  • Vakulenko, S. B., & Mobashery, S. (2003). Versatility of aminoglycosides and prospects for their future. Clinical Microbiology Reviews, 16(3), 430–450.

    Article  CAS  Google Scholar 

  • Wang, J. L., Mao, D. Q., Mu, Q. H., & Luo, Y. (2015). Fate and proliferation of typical antibiotic resistance genes in five full-scale pharmaceutical wastewater treatment plants. Science of the Total Environment, 526, 366–373.

    Article  CAS  Google Scholar 

  • Wang, F. H., Qiao, M., Su, J. Q., Chen, Z., Zhou, X., & Zhu, Y. G. (2014). High throughput profiling of antibiotic resistance genes in urban park soils with reclaimed water irrigation. Environmental Science and Technology, 48(16), 9079–9085.

    Article  CAS  Google Scholar 

  • Wei, F. S. (2002). Monitoring and analysis methods of water and wastewater, 4th ed. (pp. 210–213). Beijing: China Environmental Science Press.

  • Yu, X., Zuo, J., Li, R., Gan, L., Li, Z., & Zhang, F. (2014). A combined evaluation of the characteristics and acute toxicity of antibiotic wastewater. Ecotoxicology and Environmental Safety, 106, 40–45.

    Article  CAS  Google Scholar 

  • Zhai, W. C., Yang, F. X., Mao, D. Q., & Luo, Y. (2016). Fate and removal of various antibiotic resistance genes in typical pharmaceutical wastewater treatment systems. Environmental Science and Pollution Research, 23(12), 12030–12038.

    Article  CAS  Google Scholar 

  • Zhang, Y., Xie, J., Liu, M., Tian, Z., He, Z., van Nostrand, J. D., et al. (2013). Microbial community functional structure in response to antibiotics in pharmaceutical wastewater treatment systems. Water Research, 47(16), 6298–6308.

    Article  CAS  Google Scholar 

  • Zhang, H., Zhang, Y., Yang, M., & Liu, M. (2015). Evaluation of residual antibacterial potency in antibiotic production wastewater using a real-time quantitative method. Environmental Science Processes and Impacts, 17(11), 1923–1929.

    Article  CAS  Google Scholar 

  • Zhu, Y. G., Johnson, T. A., Su, J. Q., Qiao, M., Guo, G. X., Stedtfeld, R. D., et al. (2013). Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proceedings of the National Academy of Sciences of the United States of America, 110(9), 3435–3440.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This project is supported by National Natural Scientific Foundation of China (No. 21437005) and special fund of State Key Joint Laboratory of Environmental Simulation and Pollution Control (15L03ESPC).

Author information

Authors and Affiliations

  1. State Key Laboratory of Environmental Aquatic Chemistry, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100085, China

    Mei Tang, Chunyan Wang, Zhe Tian, Min Yang & Yu Zhang

  2. College of Environmental Science and Engineering, Beijing Forestry University, Beijing, 100083, China

    Xiaomin Dou

  3. Department of Biology and Chemical Engineering, Nanyang Institute of Technology, Nanyang, 473004, China

    Chunyan Wang

  4. University of Chinese Academy of Sciences, Beijing, 100049, China

    Mei Tang, Zhe Tian, Min Yang & Yu Zhang

Authors
  1. Mei Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaomin Dou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chunyan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhe Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Min Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xiaomin Dou or Yu Zhang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 126 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tang, M., Dou, X., Wang, C. et al. Abundance and distribution of antibiotic resistance genes in a full-scale anaerobic–aerobic system alternately treating ribostamycin, spiramycin and paromomycin production wastewater. Environ Geochem Health 39, 1595–1605 (2017). https://doi.org/10.1007/s10653-017-9987-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10653-017-9987-5

Keywords

Search

Navigation