Skip to main content
SpringerLink
Log in

Influence of Tetracycline on Tetracycline-Resistant Heterotrophs and tet Genes in Activated Sludge Process

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

The concentrations of tetracycline-intermediate resistant, tetracycline-resistant heterotrophic bacteria, and total heterotrophic bacteria were examined to assess the influence of tetracycline on tetracycline-resistant heterotrophs by the R2A agar cultivation method in the tetracycline fortified activated sludge process and in the natural background. Results showed that the percentages of both tetracycline-intermediate resistant and tetracycline-resistant heterotrophic bacteria in total heterotrophic bacteria were significantly increased, after tetracycline was fed to activated sludge for a 3 months period under four different operating conditions, as compared with the background. In order to investigate the mechanism of activated sludge resistance to tetracycline, polymerase chain reaction experiments were carried out to analyze the existence and evolution of tet genes in the presence of tetracycline. Results revealed that only tet A and tet B genes out of the 11 target tet genes were observed in tetracycline treated activated sludge while no tet gene was detected in background. This indicated that tet A gene could accumulate in activated sludge with slower and continuous influent, while the accumulation of tet B gene could be attributed to shorter hydraulic retention time. Therefore, it was proposed in this study that tetracycline-resistant genes created by efflux pumps spread earlier and quicker to encode resistance to tetracycline, which facilitated the increase in tetracycline-resistance.

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

  1. Al-Ahmad A, Haiß A, Unger J, Brunswick-Tietze A, Wiethan J, Kümmerer K (2009) Effects of a realistic mixture of antibiotics on resistant and nonresistant sewage sludge bacteria in laboratory-scale treatment plants. Arch Environ Contam Toxicol 57:264–273

    Article  CAS  PubMed  Google Scholar 

  2. Association APH (1994) Water Environment Federation (1998). Standard methods for the examination of water and wastewater. APHA, Washington, DC

  3. Brodisch KE, Joyner SJ (1983) The role of micro-organisms other than acinetobacter in biological phosphate removal in activated sludge processes. Water Sci Technol 15:117–125

    CAS  Google Scholar 

  4. Chen Y, Zhang H, Luo Y, Song J (2012) Occurrence and dissipation of veterinary antibiotics in two typical swine wastewater treatment systems in east China. Environ Monit Assess 184:2205–2217

    Article  CAS  PubMed  Google Scholar 

  5. Dang H, Ren J, Song L, Sun S, An L (2008) Diverse tetracycline resistant bacteria and resistance genes from coastal waters of Jiaozhou Bay. Microb Ecol 55:237–246

    Article  CAS  PubMed  Google Scholar 

  6. Gao P, Mao D, Luo Y, Wang L, Xu B, Xu L (2012) Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment. Water Res 46:2355–2364

    Article  CAS  PubMed  Google Scholar 

  7. Gibs J, Heckathorn HA, Meyer MT, Klapinski FR, Alebus M, Lippincott RL (2013) Occurrence and partitioning of antibiotic compounds found in the water column and bottom sediments from a stream receiving two wastewater treatment plant effluents in northern New Jersey, 2008. Sci Total Environ 458:107–116

    Article  PubMed  Google Scholar 

  8. Gulkowska A, Leung H, So M et al (2008) Removal of antibiotics from wastewater by sewage treatment facilities in Hong Kong and Shenzhen, China. Water Res 42:395–403

    Article  CAS  PubMed  Google Scholar 

  9. Halling-Sørensen B, Nors Nielsen S, Lanzky P, Ingerslev F, Holten Lützhøft H, Jørgensen S (1998) Occurrence, fate and effects of pharmaceutical substances in the environment-a review. Chemosphere 36:357–393

    Article  PubMed  Google Scholar 

  10. Henriques IS, Fonseca F, Alves A, Saavedra MJ, Correia A (2008) Tetracycline-resistance genes in gram-negative isolates from estuarine waters. Lett Appl Microbiol 47:526–533

    Article  CAS  PubMed  Google Scholar 

  11. Hu X, Zhou Q, Luo Y (2010) Occurrence and source analysis of typical veterinary antibiotics in manure, soil, vegetables and groundwater from organic vegetable bases, northern China. Environ Pollut 158:2992–2998

    Article  CAS  PubMed  Google Scholar 

  12. Huang JJ, Hu HY, Lu SQ, Li Y, Tang F, Lu Y, Wei B (2012) Monitoring and evaluation of antibiotic-resistant bacteria at a municipal wastewater treatment plant in China. Environ Int 42:31–36

    Article  CAS  PubMed  Google Scholar 

  13. 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

    Article  CAS  PubMed  Google Scholar 

  14. Kim S, Aga DS, Jensen JN, Weber AS (2007) Effect of sequencing batch reactor operation on presence and concentration of tetracycline-resistant organisms. Water Environ Res 79:2287–2297

    Article  CAS  PubMed  Google Scholar 

  15. Kim S, Jensen JN, Aga DS, Weber AS (2007) Tetracycline as a selector for resistant bacteria in activated sludge. Chemosphere 66:1643–1651

    Article  CAS  PubMed  Google Scholar 

  16. Kűmmerer K (2004) Pharmaceuticals in the environment: sources, fate, effects and risks. Springer, Heidelberg

    Book  Google Scholar 

  17. Li B, Zhang T (2010) Biodegradation and adsorption of antibiotics in the activated sludge process. Environ Sci Technol 44:3468–3473

    Article  CAS  PubMed  Google Scholar 

  18. Li B, Zhang X, Guo F, Wu W, Zhang T (2013) Characterization of tetracycline resistant bacterial community in saline activated sludge using batch stress incubation with high-throughput sequencing analysis. Water Res 47:4207–4216

    Article  CAS  PubMed  Google Scholar 

  19. Li Y-W, Wu X-L, Mo C-H, Tai Y-P, Huang X-P, Xiang L (2011) Investigation of sulfonamide, tetracycline, and quinolone antibiotics in vegetable farmland soil in the Pearl River Delta area, southern China. J Agric Food Chem 59:7268–7276

    Article  PubMed  Google Scholar 

  20. Luo Y, Mao DQ, Rysz M, Zhou DX, Zhang HJ, Xu L, Alvarez PJJ (2010) Trends in antibiotic resistance genes occurrence in the Haihe River, China. Environ Sci Technol 44:7220–7225

    Article  PubMed  Google Scholar 

  21. Luo Y, Xu L, Rysz M, Wang Y, Zhang H, Alvarez PJJ (2011) Occurrence and transport of tetracycline, sulfonamide, quinolone, and macrolide antibiotics in the Haihe River basin, China. Environ Sci Technol 45:1827–1833

    Article  CAS  PubMed  Google Scholar 

  22. Martins da Costa P, Vaz-Pires P, Bernardo F (2006) Antimicrobial resistance in Enterococcus spp. isolated in inflow, effluent and sludge from municipal sewage water treatment plants. Water Res 40:1735–1740

    Article  CAS  PubMed  Google Scholar 

  23. Massa S, Caruso M, Trovatelli F, Tosques M (1998) Comparison of plate count agar and R2A medium for enumeration of heterotrophic bacteria in natural mineral water. World J Microbiol Biotechnol 14:727–730

    Article  Google Scholar 

  24. McKinney CW, Loftin KA, Meyer MT, Davis JG, Pruden A (2010) tet and sul antibiotic resistance genes in livestock lagoons of various operation type, configuration, and antibiotic occurrence. Environ Sci Technol 44:6102–6109

    Article  CAS  PubMed  Google Scholar 

  25. Prado N, Ochoa J, Amrane A (2009) Biodegradation and biosorption of tetracycline and tylosin antibiotics in activated sludge system. Process Biochem 44:1302–1306

    Article  CAS  Google Scholar 

  26. Prado N, Ochoa J, Amrane A (2009) Biodegradation by activated sludge and toxicity of tetracycline into a semi-industrial membrane bioreactor. Bioresour Technol 100:3769–3774

    Article  CAS  PubMed  Google Scholar 

  27. 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  PubMed  Google Scholar 

  28. Schwartz T, Hoffmann S, Obst U (1998) Formation and bacterial composition of young, natural biofilms obtained from public bank-filtered drinking water systems. Water Res 32:2787–2797

    Article  CAS  Google Scholar 

  29. Server BB Antibioresistance Archive. http://www.antibioresistance.be/Tetracycline/Tetdescription/default.html. Accessed 12 Aug 2013

  30. Seyfried EE, Newton RJ, Rubert KF, Pedersen JA, McMahon KD (2010) Occurrence of tetracycline resistance genes in aquaculture facilities with varying use of oxytetracycline. Microb Ecol 59:799–807

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Srinivasan V, Nam H-M, Sawant AA, Headrick SI, Nguyen LT, Oliver SP (2008) Distribution of tetracycline and streptomycin resistance genes and class 1 integrons in Enterobacteriaceae isolated from dairy and nondairy farm soils. Microbial Ecol. 55:184–193

    Article  CAS  Google Scholar 

  32. System NARM (2001) National Antimicrobial Resistance Monitoring System Annual Report, Center for Disease Control and Prevention. Department of Health and Human Services. http://www.cdc.gov/narms/annual/2001/2001.pdf. Accessed 15 July 2013

  33. Wu N, Qiao M, Zhang B, Cheng WD, Zhu YG (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  PubMed  Google Scholar 

  34. Yang H, Byelashov OA, Geornaras I, Goodridge LD, Nightingale KK, Belk KE, Smith GC, Sofos JN (2010) Presence of antibiotic-resistant commensal bacteria in samples from agricultural, city, and national park environments evaluated by standard culture and real-time PCR methods. Can J Microbiol 56:761–770

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  36. 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  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the National water pollution control and treatment technological Project (No. 2008ZX07314-002) and the National Natural Science Foundation of China (No. 50908117). Thanks to Dr. Edward C. Mignot, Shandong University, for linguistic advice.

Author information

Authors and Affiliations

  1. The College of Environmental Science and Engineering, Nankai University, Wei Jin Road 94, Tianjin, 300071, China

    Jie Yu, Dongfang Liu & Kexun Li

  2. School of Electrical Engineering and Automation, Tianjin Polytechnic University, West Binshui Road 399, Tianjin, 300387, China

    Jie Yu

Authors
  1. Jie Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dongfang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kexun Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jie Yu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 32 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, J., Liu, D. & Li, K. Influence of Tetracycline on Tetracycline-Resistant Heterotrophs and tet Genes in Activated Sludge Process. Curr Microbiol 70, 415–422 (2015). https://doi.org/10.1007/s00284-014-0731-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-014-0731-4

Keywords

Search

Navigation