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Prevalence of antibiotic resistance genes of wastewater and surface water in livestock farms of Jiangsu Province, China

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Abstract

The overuse of antibiotics in livestock farms is general, leading to a wide distribution of antibiotic resistance genes (ARGs) in aquatic environment adjacent to livestock farms. However, researches of the distribution and types of ARGs in aquatic environment of China are still in the initial stage. In this study, wastewater and surface water samples were collected from 12 livestock farms (four pig farms, four cattle farms, and four chicken farms) in Jiangsu Province of China. The prevalence, abundance, and distribution of 22 ARGs were investigated, which were categorized into six groups, including nine tetracyclin resistance genes, three sulfonamides resistance genes, three quinolone resistance genes, two macrolide resistance genes, three aminoglycoside resistance genes, and two multidrug resistance genes, employing quantitative real-time PCR (qPCR). The results suggested that all of the 22 ARGs were detected in samples. Sul1, sul2, and tetM were the most abundant with the average concentration of 3.84 × 101 copies/16S recombinant RNA (rRNA) gene copies, 1.62 × 101 copies/16S rRNA gene copies, 2.33 × 101 copies/16S rRNA gene copies, respectively. Principle component analysis revealed that the comprehensive pollution of ARGs in northern Jiangsu was more serious. ARGs in wastewater were more abundant when compared to that in surface water. A preliminary study regarding the fate of ARGs after an aerobiotic process showed that tetA, tetC, sul1, sul2, oqxB, and qnrS were significantly increased. And, among the tetracycline resistance genes, the efflux pump genes were enriched while the ribosomal protection protein encoding genes were decreased in the aerobiotic process. The prevalance of ARGs in water environment is of concern; more surveillance is required to determine the pollution level and pattern of antibiotic resistance genes.

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References

  • Adachi F, Yamamoto A, Takakura K-I, Kawahara R (2013) Occurrence of fluoroquinolones and fluoroquinolone-resistance genes in the aquatic environment. Sci Total Environ 444:508–514

    Article  CAS  Google Scholar 

  • Andam CP, Fournier GP, Gogarten JP (2011) Multilevel populations and the evolution of antibiotic resistance through horizontal gene transfer. FEMS Microbiol Rev 35:756–767

    Article  CAS  Google Scholar 

  • Baquero F, Martínez J-L, Cantón R (2008) Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol 19:260–265

    Article  CAS  Google Scholar 

  • Blackwell PA, Kay P, Ashauer R, Boxall ABA (2009) Effects of agricultural conditions on the leaching behaviour of veterinary antibiotics in soils. Chemosphere 75:13–19

    Article  CAS  Google Scholar 

  • Chan Y (2008) Low prevalence of vancomycin- and bifunctional aminoglycoside-resistant enterococci isolated from poultry farms in Malaysia. Int J Food Microbiol 122:221–226

    Article  CAS  Google Scholar 

  • Chen F, Ying G-G, Kong L-X, Wang L, Zhao J-L, Zhou L-J, Zhang L-J (2011) Distribution and accumulation of endocrine-disrupting chemicals and pharmaceuticals in wastewater irrigated soils in Hebei, China. Environ Pollut 159:1490–1498

    Article  CAS  Google Scholar 

  • Chen C, Li J, Chen P, Ding R, Zhang P, Li X (2014) Occurrence of antibiotics and antibiotic resistances in soils from wastewater irrigation areas in Beijing and Tianjin, China, Environmental Pollution, pp. 94–101

  • Cheng W, Chen H, Su C, Yan S (2013) Abundance and persistence of antibiotic resistance genes in livestock farms: a comprehensive investigation in eastern China. Environ Int 61:1–7

    Article  CAS  Google Scholar 

  • Chopra I, Roberts M (2001) Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65:232–260

    Article  CAS  Google Scholar 

  • Dobiasova H, Kutilova I, Piackova V (2014) Ornamental fish as a source of plasmid-mediated quinolone resistance genes and antibiotic resistance plasmids. Vet Microbiol 171:413–421

    Article  CAS  Google Scholar 

  • Ghotaslou R, Aghazadeh M, Ahangarzadeh Rezaee M, Moshafi MH, Forootanfar H, Hojabri Z, Saffari F (2014) The prevalence of aminoglycoside-modifying enzymes among coagulase negative staphylococci in Iranian pediatric patients. J Infect Chemother 20:569–573

    Article  CAS  Google Scholar 

  • Harrison E, Brockhurst MA (2012) Plasmid-mediated horizontal gene transfer is a coevolutionary process. Trends Microbiol 20:262–267

    Article  CAS  Google Scholar 

  • Heuer H, Solehati Q, Zimmerling U, Kleineidam K (2011) Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine. Appl Environ Microbiol 77:2527–2530

    Article  CAS  Google Scholar 

  • Hu F-Y, He L-M, Yang J-W, Bian K, Wang Z-N, Yang H-C, Liu Y-H (2014) Determination of 26 veterinary antibiotics residues in water matrices by lyophilization in combination with LC–MS/MS. J Chromatogr B 949–950:79–86

    Article  Google Scholar 

  • Hung S-W, Wang S-L, Tu C-Y, Tsai Y-C, Chuang S-T, Shieh M-T, Liu P-C, Wang W-S (2008) Antibiotic susceptibility and prevalence of erythromycin ribosomal methylase gene, erm(B) in Streptococcus spp. Vet J 176:197–204

    Article  CAS  Google Scholar 

  • Huovinen P (1995) Trimethoprim and sulfonamide resistance. Antimicrob Agents Chemother 39:279–289

    Article  CAS  Google Scholar 

  • Jensen LB, Agersø Y, Sengeløv G (2002) Presence of erm genes among macrolide-resistant Gram-positive bacteria isolated from Danish farm soil. Environ Int 28:487–491

    Article  CAS  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 

  • Jiang X, Yu T, Jiang X, Zhang W, Zhang L, Ma J (2014a) Emergence of plasmid-mediated quinolone resistance genes in clinical isolates of Acinetobacter baumannii and Pseudomonas aeruginosa in Henan, China. Diagn Microbiol Infect Dis 79:381–383

    Article  CAS  Google Scholar 

  • Jiang Y, Li M, Guo C, An D, Xu J, Zhang Y, Xi B (2014b) Distribution and ecological risk of antibiotics in a typical effluent-receiving river (Wangyang River) in north China. Chemosphere 112:267–274

    Article  CAS  Google Scholar 

  • Kay P, Blackwell PA, Boxall ABA (2005) Column studies to investigate the fate of veterinary antibiotics in clay soils following slurry application to agricultural land. Chemosphere 60:497–507

    Article  CAS  Google Scholar 

  • Kemper N (2008) Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indic 8:1–13

    Article  CAS  Google Scholar 

  • Knapp CW, Zhang W, Sturm BSM, Graham DW (2010) Differential fate of erythromycin and beta-lactam resistance genes from swine lagoon waste under different aquatic conditions. Environ Pollut 158:1506–1512

    Article  CAS  Google Scholar 

  • Li WC (2014) Occurrence, sources, and fate of pharmaceuticals in aquatic environment and soil. Environ Pollut 187:193–201

    Article  CAS  Google Scholar 

  • Liu L, Y-h L, Wang Z, C-x L, Huang X, G-f Z (2014a) 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 

  • Liu M, Ding R, Zhang Y, Gao Y (2014b) Abundance and distribution of Macrolide-Lincosamide-Streptogramin resistance genes in an anaerobic-aerobic system treating spiramycin production wastewater. Water Res 63:33–41

    Article  Google Scholar 

  • Marshall BM, Levy SB (2011) Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev 24:718–733

    Article  CAS  Google Scholar 

  • Martina K, Jir J, Alica C (2013) Cow excrements enhance the occurrence of tetracycline resistance genes in soil regardless of their oxytetracycline content. Chemosphere 10:2413–2418

    Google Scholar 

  • Masi M, Pagès J-M, Pradel E (2003) Overexpression and purification of the three components of the Enterobacter aerogenes AcrA–AcrB–TolC multidrug efflux pump. J Chromatogr B 786:197–205

    Article  CAS  Google Scholar 

  • Montanari MP, Cochetti I, Mingoia M, Varaldo PE (2003) Phenotypic and molecular characterization of tetracycline- and erythromycin-resistant strains of Streptococcus pneumoniae. Antimicrob Agents Chemother 47:2236–2241

    Article  CAS  Google Scholar 

  • Na G, Zhang W, Zhou S, Gao H, Lu Z, Wu X, Li R, Qiu L, Cai Y, Yao Z (2014) Sulfonamide antibiotics in the Northern Yellow Sea are related to resistant bacteria: implications for antibiotic resistance genes. Mar Pollut Bull 84:70–75

    Article  CAS  Google Scholar 

  • Nandi S, Maurer JJ, Hofacre C, Summers AO (2004) Gram-positive bacteria are a major reservoir of Class 1 antibiotic resistance integrons in poultry litter. Proc Natl Acad Sci 101:7118–7122

    Article  CAS  Google Scholar 

  • Nikaido H (2009) Multidrug resistance in bacteria. Annu Rev Biochem 78:119–146

    Article  CAS  Google Scholar 

  • Piddock LJV (2006) Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin Microbiol Rev 19:382–402

    Article  CAS  Google Scholar 

  • Ramirez MS, Tolmasky ME (2010) Aminoglycoside modifying enzymes. Drug Resist Updat 13:151–171

    Article  CAS  Google Scholar 

  • Redgrave LS, Sutton SB, Webber MA, Piddock LJV (2014) Fluoroquinolone resistance: mechanisms, impact on bacteria, and role in evolutionary success. Trends Microbiol 22:438–445

    Article  CAS  Google Scholar 

  • Roberts MC (2005) Update on acquired tetracycline resistance genes. FEMS Microbiol Lett 245:195–203

    Article  CAS  Google Scholar 

  • Rodríguez-Rojas A, Rodríguez-Beltrán J, Couce A, Blázquez J (2013) Antibiotics and antibiotic resistance: a bitter fight against evolution. Int J Med Microbiol 303:293–297

    Article  Google Scholar 

  • Salyers A, Gupta A, Wang Y (2004) Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol 12:412–416

    Article  CAS  Google Scholar 

  • Shi Y, Gao L, Li W, Liu J, Cai Y (2012) Investigation of fluoroquinolones, sulfonamides and macrolides in long-term wastewater irrigation soil in Tianjin, China. Bull Environ Contam Toxicol 89:857–861

    Article  CAS  Google Scholar 

  • Shoemaker NB, Vlamakis H, Hayes K, Salyers AA (2001) Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon. Appl Environ Microbiol 67:561–568

    Article  CAS  Google Scholar 

  • Stokes HW, Gillings MR (2011) Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into Gram-negative pathogens. FEMS Microbiol Rev 35:790–819

    Article  CAS  Google Scholar 

  • Su H-C, Pan C-G, Ying G-G, Zhao J-L, Zhou L-J, Liu Y-S, Tao R, Zhang R-Q, He L-Y (2014) Contamination profiles of antibiotic resistance genes in the sediments at a catchment scale. Sci Total Environ 490:708–714

    Article  CAS  Google Scholar 

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

  • Tao C-W, Hsu B-M, Ji W-T, Hsu T-K, Kao P-M, Hsu C-P, Shen S-M, Shen T-Y, Wan T-J, Huang Y-L (2014) Evaluation of five antibiotic resistance genes in wastewater treatment systems of swine farms by real-time PCR. Sci Total Environ 496:116–121

    Article  CAS  Google Scholar 

  • Udikovic-Kolic N, Wichmann F, Broderick NA, Handelsman J (2014) Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proc Natl Acad Sci 111:15202–15207

    Article  CAS  Google Scholar 

  • Vinué L, Sáenz Y, Rojo-Bezares B, Olarte I, Undabeitia E, Somalo S, Zarazaga M, Torres C (2010) Genetic environment of sul genes and characterisation of integrons in Escherichia coli isolates of blood origin in a Spanish hospital. Int J Antimicrob Agents 35:492–496

    Article  Google Scholar 

  • Wei R, Ge F, Huang S, Chen M, Wang R (2011) Occurrence of veterinary antibiotics in animal wastewater and surface water around farms in Jiangsu Province, China. Chemosphere 82:1408–1414

    Article  CAS  Google Scholar 

  • Wright GD (2010) Antibiotic resistance in the environment: a link to the clinic? Curr Opin Microbiol 13:589–594

    Article  CAS  Google Scholar 

  • Xu J, Zhang Y, Zhou C, Guo C, Wang D, Du P, Luo Y, Wan J, Meng W (2014) Distribution, sources and composition of antibiotics in sediment, overlying water and pore water from Taihu Lake, China. Sci Total Environ 497–498:267–273

    Article  Google Scholar 

  • Yang Y, Li B, Zou S, Fang HHP, Zhang T (2014) Fate of antibiotic resistance genes in sewage treatment plant revealed by metagenomic approach. Water Res 62:97–106

    Article  CAS  Google Scholar 

  • Zhao L, Dong YH, Wang H (2010) Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Sci Total Environ 408:1069–1075

    Article  CAS  Google Scholar 

  • Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, 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 would like to acknowledge the financial support from 2011 Commonwealth and Environmental Protection Project granted by the MEP “The health risk assessment and management technology of veterinary medicine” (201109038) and “Study of determination method, pollution level, and pollution control strategy of antibiotic-resistant gene in China” (201309031).

I certify that this manuscript is original and has not been published and will not be submitted elsewhere for publication while being considered. And the study is not split up into several parts to increase the quantity of submissions and submitted to various journals or to one journal over time. No data have been fabricated or manipulated (including images) to support your conclusions. No data, text, or theories by others are presented as if they were our own.The submission has been received explicitly from all co-authors. And authors whose names appear on the submission have contributed sufficiently to the scientific work and therefore share collective responsibility and accountability for the results.

Conflict of interest

The authors declare that they have no conflict of interest. This article does not contain any studies with human participants or animals performed by any of the authors. Informed consent was obtained from all individual participant included in the study.

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Correspondence to Na Wang or Boping Ye.

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Responsible editor: Robert Duran

Biao Chen, Lijun Hao, Na Wang and Boping Ye contributed equally to this work.

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Chen, B., Hao, L., Guo, X. et al. Prevalence of antibiotic resistance genes of wastewater and surface water in livestock farms of Jiangsu Province, China. Environ Sci Pollut Res 22, 13950–13959 (2015). https://doi.org/10.1007/s11356-015-4636-y

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