Skip to main content

Antibiotic resistance genes in surface water of eutrophic urban lakes are related to heavy metals, antibiotics, lake morphology and anthropic impact

Ecotoxicology volume 26, pages 831–840 (2017)Cite this article

Abstract

Urban lakes are impacted by heavy human activities and represent potential reservoirs for antibiotic resistance genes. In this study, six urban lakes in Wuhan, central China were selected to analyze the distribution of sulfonamide resistance (sul) genes, tetracycline resistance (tet) genes and quinolone resistance (qnr) genes and their relationship with heavy metals, antibiotics, lake morphology and anthropic impact. sul1 and sul2 were detected in all six lakes and dominated the types of antibiotic resistance genes, which accounted for 86.28–97.79% of the total antibiotic resistance gene abundance. For eight tested tet genes, antibiotic efflux pumps (tetA, tetB, tetC, and tetG) genes were all observed in six lakes and had higher relative abundance than ribosomal protection protein genes (tetM and tetQ). For 4 plasmid mediated quinolone resistance genes, only qnrD is found in all six lakes. The class I integron (intI1) is also found to be a very important media for antibiotic resistance gene propagation in urban lakes. The results of redundancy analysis and variation partitioning analysis showed that antibiotic and co-selection with heavy metals were the major factors driving the propagation of antibiotic resistance genes in six urban lakes. The heavily eutrophic Nanhu Lake and Shahu Lake which located in a high density building area with heavy human activities had the higher relative abundance of total antibiotic resistance genes. Our study could provide a useful reference for antibiotic resistance gene abundance in urban lakes with high anthropic impact.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Aminov RI (2009) The role of antibiotics and antibiotic resistance in nature. Environ Microbiol 11:2970–2988

    CAS  Article  Google Scholar 

  • Aminov RI, Garrigues-Jeanjean N, Mackie RI (2001) Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Appl Environ Microbiol 67:22–32

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Bengtsson-Palme J, Boulund F, Fick J, Kristiansson E, Larsson J (2014) Shotgun metagenomics reveals a wide array of antibiotic resistance genes and mobile elements in a polluted lake in India. Front Microbiol 5:e648

    Article  Google Scholar 

  • Berg J, Thorsen MK, Holm PE, Jensen J, Nybroe O, Brandt KK (2010) Cu Exposure under field conditions coselects for antibiotic resistance as determined by a novel cultivation-independent bacterial community tolerance assay. Environ Sci Technol 44:8724–8728

    CAS  Article  Google Scholar 

  • Chen H, Zhang MM (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

    CAS  Article  Google Scholar 

  • Cummings DE, Archer KF, Arriola DJ, Baker PA, Faucett KG, Laroya JB, Pfeil KL, Ryan CR, Ryan KRU, Zuill DE (2010) Broad dissemination of plasmid-mediated quinolone resistance genes in sediments of two urban coastal wetlands. Environ Sci Technol 45:447–454

    Article  Google Scholar 

  • Czekalski N, Gascon Diez E, Burgmann H (2014) Wastewater as a point source of antibiotic-resistance genes in the sediment of a freshwater lake. ISME J 8:1381–1390

    CAS  Article  Google Scholar 

  • Czekalski N, Sigdel R, Birtel J, Matthews B, Bürgmann H (2015) Does human activity impact the natural antibiotic resistance background? Abundance of antibiotic resistance genes in 21 Swiss lakes. Environ Int 81:45–55

    CAS  Article  Google Scholar 

  • Devarajan N, Laffite A, Graham ND, Meijer M, Prabakar K, Mubedi JI, Elongo V, Mpiana PT, Ibelings BW, Wildi W, Pote J (2015) Accumulation of clinically relevant antibiotic-resistance genes, bacterial load, and metals in freshwater lake sediments in Central Europe. Environ Sci Technol 49:6528–6537

    CAS  Article  Google Scholar 

  • Di Cesare A, Eckert EM, D’Urso S, Bertoni R, Gillan DC, Wattiez R, Corno G (2016) Co-occurrence of integrase 1, antibiotic and heavy metal resistance genes in municipal wastewater treatment plants. Water Res 94:208–214

    Article  Google Scholar 

  • Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MOA, Dantas G (2012) The shared antibiotic resistome of soil bacteria and human pathogens. Science 337:1107–1111

    CAS  Article  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • Gaze WH, Zhang L, Abdouslam NA, Hawkey PM, Calvo-Bado L, Royle J, Brown H, Davis S, Kay P, Boxall ABA, Wellington EMH (2011) Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. ISME J 5:1253–1261

    CAS  Article  Google Scholar 

  • Gillings MR, Gaze WH, Pruden A, Smalla K, Tiedje JM, Zhu YG (2015) Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J 9:1269–1279

    CAS  Article  Google Scholar 

  • Hemme CL, Deng Y, Gentry TJ, Fields MW, Wu L, Barua S, Barry K, Tringe SG, Watson DB, He Z, Hazen TC, Tiedje JM, Rubin EM, Zhou J (2010) Metagenomic insights into evolution of a heavy metal-contaminated groundwater microbial community. ISME J 4:660–672

    CAS  Article  Google Scholar 

  • Huerta B, Marti E, Gros M, Lopez P, Pompeo M, Armengol J, Barcelo D, Balcazar JL, Rodriguez-Mozaz S, Marce R (2013) Exploring the links between antibiotic occurrence, antibiotic resistance, and bacterial communities in water supply reservoirs. Sci Total Environ 456:161–170

    Article  Google Scholar 

  • Ji X, Shen Q, Liu F, Ma J, Xu G, Wang Y, Wu M (2012) Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai; China. J Hazard Mater 235–236:178–185

    Article  Google Scholar 

  • Khan GA, Berglund B, Khan KM, Lindgren PE, Fick J (2013) Occurrence and abundance of antibiotics and resistance genes in rivers, canal and near drug formulation facilities--a study in Pakistan. PLoS ONE 8:e62712

    CAS  Article  Google Scholar 

  • Kim SC, Carlson K (2007) Quantification of human and veterinary antibiotics in water and sediment using SPE/LC/MS/MS. Anal Bioanal Chem 387:1301–1315

    CAS  Article  Google Scholar 

  • Li JA, Cheng WX, Xu LK, Strong PJ, Chen H (2015) Antibiotic-resistant genes and antibiotic-resistant bacteria in the effluent of urban residential areas, hospitals, and a municipal wastewater treatment plant system. Environ Sci Pollut Res 22:4587–4596

    CAS  Article  Google Scholar 

  • Ling Z, Yang Y, Huang Y, Zou S, Luan T (2013) A preliminary investigation on the occurrence and distribution of antibiotic resistance genes in the Beijiang River, South China. J Environ Sci 25:1656–1661

    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. Environ Sci Technol 46:7551–7557

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  • Mao DQ, Yu S, Rysz M, Luo Y, Yang FX, Li FX, Hou J, Mu QH, Alvarez PJJ (2015) Prevalence and proliferation of antibiotic resistance genes in two municipal wastewater treatment plants. Water Res 85:458–466

    CAS  Article  Google Scholar 

  • Marti E, Variatza E, Balcazar JL (2014) The role of aquatic ecosystems as reservoirs of antibiotic resistance. Trends Microbiol 22:36–41

    CAS  Article  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • Ng L-K, Martin I, Alfa M, Mulvey M (2001) Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probe 15:209–215

    CAS  Article  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

    CAS  Article  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

    CAS  Article  Google Scholar 

  • Rosas I, Salinas E, Martinez L, Cruz-Cordova A, Gonzalez-Pedrajo B, Espinosa N, Amabile-Cuevas CF (2015) Characterization of Escherichia coli isolates from an urban lake receiving water from a wastewater treatment plant in Mexico City: fecal pollution and antibiotic resistance. Curr Microbiol 71:490–495

    CAS  Article  Google Scholar 

  • Sayah RS, Kaneene JB, Johnson Y, Miller R (2005) Patterns of antimicrobial resistance observed in Escherichia coli isolates obtained from domestic- and wild-animal fecal samples, human septage, and surface water. Appl Environ Microbiol 71:1394–1404

    CAS  Article  Google Scholar 

  • Seiler C, Berendonk TU (2012) Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol. 3:e399

    Article  Google Scholar 

  • Stalder T, Barraud O, Casellas M, Dagot C, Ploy MC (2012) Integron involvement in environmental spread of antibiotic resistance. Front Microbiol. 3:e119

    Article  Google Scholar 

  • Suzuki S, Hoa PTP (2012) Distribution of quinolones, sulfonamides, tetracyclines in aquatic environment and antibiotic resistance in Indochina. Front Microbiol. 3:e67

    Google Scholar 

  • Tamminen M, Karkman A, Lõhmus A, Muziasari WI, Takasu H, Wada S, Suzuki S, Virta M (2010) Tetracycline resistance genes persist at aquaculture farms in the absence of selection pressure. Environ Sci Technol 45:386–391

    Article  Google Scholar 

  • Wang D, Sui Q, Zhao W, Shuguang LU, Qiu Z, Yu G (2014) Pharmaceutical and personal care products in the surface water of China: a review. Chinese Sci Bull 59:743–751

    Article  Google Scholar 

  • Xing Z, Chua LH, Imberger J (2014) Evaluation of management scenarios for controlling eutrophication in a shallow tropical urban lake. Int J Environ Pollut Rem 2:66–72

    CAS  Google Scholar 

  • Yang Y, Cao X, Lin H, Wang J (2016) Antibiotics and antibiotic resistance genes in sediment of Honghu Lake and East Dongting Lake, China. Microb Ecol 72:791–801

    CAS  Article  Google Scholar 

  • Yang Y, Liu W, Xu C, Wei B, Wang J (2017) Antibiotic resistance genes in lakes from middle and lower reaches of the Yangtze River, China: Effect of land use and sediment characteristics. Chemosphere 178:19–25

    CAS  Article  Google Scholar 

  • Zhang X-X, 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

    CAS  Article  Google Scholar 

  • Zhou T, Lu JJ, Tong YB, Li SM, Wang XL (2014) Distribution of antibiotic resistance genes in Bosten Lake, Xinjiang, China. Water Sci Technol 70:925–931

    CAS  Article  Google Scholar 

Download references

Funding

This project is supported in part by National Natural Science Foundation of China (NO. 31400113, 41401542), Funding Project of Sino-Africa Joint Research Center, Chinese Academy of Sciences (Y623321K01), Knowledge Innovation Program of the Chinese Academy of Sciences (NO. Y455436K02), Youth Innovation Promotion Association of Chinese Academy of Sciences (NO. 2015282), and the Hundred Talents Program of the Chinese Academy of Sciences (Y329671K01).

Author information

Affiliations

  1. Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, 430074, China

    Yuyi Yang, Chen Xu, Xinhua Cao & Jun Wang

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

    Chen Xu & Xinhua Cao

  3. Institute of Environmental Resources and Soil Fertilizers, Zhejiang Academy of Agricultural Sciences, Hangzhou, 310021, China

    Hui Lin

  4. Sino-Africa Joint Research Center, Chinese Academy of Sciences, Wuhan, 430074, China

    Jun Wang

Authors
  1. Yuyi Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chen Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xinhua Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hui Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jun Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yang, Y., Xu, C., Cao, X. et al. Antibiotic resistance genes in surface water of eutrophic urban lakes are related to heavy metals, antibiotics, lake morphology and anthropic impact. Ecotoxicology 26, 831–840 (2017). https://doi.org/10.1007/s10646-017-1814-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-017-1814-3

Keywords

  • Urban lakes
  • Antibiotic resistance genes (ARGs)
  • Heavy metals
  • Antibiotics
  • Redundancy analysis