Environmental Science and Pollution Research

, Volume 23, Issue 21, pp 21369–21376 | Cite as

Prevalence of bacterial resistance within an eco-agricultural system in Hangzhou, China

  • Like Xu
  • Yanyun Qian
  • Chao Su
  • Weixiao Cheng
  • Jianan Li
  • Mark L. Wahlqvist
  • Hong ChenEmail author
Research Article


The wide use of antibiotics in the animal husbandry and the relevant sustainable industries may promote the emergence of antibiotic-resistant bacteria (ARB), which constitutes a growing threat to human health. The objective of this study was to determine the abundance and diversity of sulfonamide- and tetracycline-resistant bacteria within an eco-agricultural system (EAS) in Hangzhou, China. We investigated samples at every link in the EAS, from livestock manure, to biogas residues and biogas slurry, to vegetable and ryegrass fields, to a fish pond. A combination of culture-based and 16S rRNA gene-based sequencing method was used in this study. Within the studied system, the average rate of bacterial resistance to sulfonamide (46.19 %) was much higher than that of tetracycline (8.51 %) (p < 0.01). There were 224 isolates that were enumerated and sequenced, 108 of which were identified to species level. The genera comprising the sulfamethoxazole-resistant (SMXr) bacteria were generally different from those of tetracycline-resistant (TCr) bacteria. Staphylococcus and Acinetobacter were the most dominant genera of SMXr bacteria (19.30 % of the total resistant bacteria) and TCr bacteria (14.04 % of the total resistant bacteria), respectively. Several strains of resistant opportunistic pathogens (e.g., Pantoea agglomerans) were detected in edible vegetable samples, which may exert a potential threat to both pig production and human health. In general, this study indicates that the EAS is an important reservoir of antibiotic-resistant bacteria, some of which may be pathogenic.


Eco-agricultural system Sulfonamide Tetracycline Antibiotic-resistant bacteria 



This work was supported by the Major Science and Technology Program for Water Pollution Control and Treatment (2014ZX07101-012) and the Natural Science Foundation of China (Nos. 21277117 and 20210008).


  1. Aarestrup FM, Seyfarth AM, Emborg HD, Pedersen K, Hendriksen RS, Bager F (2001) Effect of abolishment of the use of antimicrobial agents for growth promotion on occurrence of antimicrobial resistance in fecal enterococci from food animals in Denmark. Antimicrob Agents Chemother 45:2054–2059CrossRefGoogle Scholar
  2. Aarestrup FM (2005) Veterinary drug usage and antimicrobial resistance in bacteria of animal origin. Basic Clin Pharmacol 96:271–281CrossRefGoogle Scholar
  3. Aga DS, Goldfish R, Kulshrestha P (2003) Application of ELISA in determining the fate of tetracyclines in land-applied livestock wastes. Analyst 128:658CrossRefGoogle Scholar
  4. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486CrossRefGoogle Scholar
  5. Binh CT, Heuer H, Kaupenjohann M, Smalla K (2008) Piggery manure used for soil fertilization is a reservoir for transferable antibiotic resistance plasmids. FEMS Microbiol Ecol 66:25–37CrossRefGoogle Scholar
  6. Birosova L, Mackulak T, Bodik I, Ryba J, Skubak J, Grabic R (2014) Pilot study of seasonal occurrence and distribution of antibiotics and drug resistant bacteria in wastewater treatment plants in Slovakia. Sci Total Environ 490:440–444CrossRefGoogle Scholar
  7. Blaustein RA, Shelton DR, Van Kessel JAS, Karns JS, Stocker MD, Pachepsky YA (2016) Irrigation waters and pipe-based biofilms as sources for antibiotic-resistant bacteria. Environ Monit Assess 188:56CrossRefGoogle Scholar
  8. Bouki C, Venieri D, Diamadopoulos E (2013) Detection and fate of antibiotic resistant bacteria in wastewater treatment plants: a review. Ecotox Environ Safe 91:1–9CrossRefGoogle Scholar
  9. Boxall ABA, Blackwell P, Cavallo R, Kay P, Tolls J (2002) The sorption and transport of a sulphonamide antibiotic in soil systems. Toxicol Lett 131:19–28CrossRefGoogle Scholar
  10. Boxall ABA, Fogg LA, Kay P, Blackwell PA, Pemberton EJ, Croxford A (2003) Prioritisation of veterinary medicines in the UK environment. Toxicol Lett 142:207–218CrossRefGoogle Scholar
  11. Cheng W, Li J, Wu Y, Xu L, Su C, Qian Y, Zhu YG, Chen H (2015) Behavior of antibiotics and antibiotic resistance genes in eco-agricultural system: a case study. J Hazard Mater 304:18–25CrossRefGoogle Scholar
  12. Cruz AT, Cazacu AC, Allen CH (2007) Pantoea agglomerans, a plant pathogen causing human disease. J Clin Microbiol 45:1989–1992CrossRefGoogle Scholar
  13. Cully M (2014) Public health: the politics of antibiotics. Nature 509:S16–S17CrossRefGoogle Scholar
  14. Davis JG, Truman CC, Kim SC, Ascough JC, Carlson K (2006) Antibiotic transport via runoff and soil loss. J Environ Qual 35:2250–2260CrossRefGoogle Scholar
  15. Fernández-Fuentes MA, Ortega Morente E, Abriouel H, Pérez Pulido R, Gálvez A (2012) Isolation and identification of bacteria from organic foods: sensitivity to biocides and antibiotics. Food Control 26:73–78CrossRefGoogle Scholar
  16. Furushita M, Shiba T, Maeda T, Yahata M, Kaneoka A, Takahashi Y, Torii K, Hasegawa T, Ohta M (2003) Similarity of tetracycline resistance genes isolated from fish farm bacteria to those from clinical isolates. Appl Environ Microbiol 69:5336–5342CrossRefGoogle Scholar
  17. 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 46:2355–2364CrossRefGoogle Scholar
  18. Geng Y, Doberstein B (2008) Developing the circular economy in China: challenges and opportunities for achieving ‘leapfrog development’. Int J Sust Dev World 15:231–239CrossRefGoogle Scholar
  19. Hu LF, Chang X, Ye Y, Wang ZX, Shao YB, Shi W, Li X, Li JB (2011) Stenotrophomonas maltophilia resistance to trimethoprim/sulfamethoxazole mediated by acquisition of sul and dfrA genes in a plasmid-mediated class 1 integron. Int J Antimicrob Agents 37:230–234CrossRefGoogle Scholar
  20. 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 158:2992–2998CrossRefGoogle Scholar
  21. Hvistendahl M (2012) PUBLIC HEALTH. China takes aim at rampant antibiotic resistance. Science 336:795–795CrossRefGoogle Scholar
  22. Jjemba PK (2002) The potential impact of veterinary and human therapeutic agents in manure and biosolids on plants grown on arable land: a review. Agric Ecosyst Environ 93:267–278CrossRefGoogle Scholar
  23. Kumar K, Gupta SC, Baidoo SK, Chander Y, Rosen CJ (2005) Antibiotic uptake by plants from soil fertilized with animal manure. J Environ Qual 34:2082–2085CrossRefGoogle Scholar
  24. Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663CrossRefGoogle Scholar
  25. Munir M, Xagoraraki I (2011) Levels of antibiotic resistance genes in manure, biosolids, and fertilized soil. J Environ Qual 40:248–255CrossRefGoogle Scholar
  26. Neela V, Rankouhi SZ, van Belkum A, Goering RV, Awang R (2012) Stenotrophomonas maltophilia in Malaysia: molecular epidemiology and trimethoprim-sulfamethoxazole resistance. Int J Infec Dis 16:e603–e607CrossRefGoogle Scholar
  27. Ozaktas T, Taskin B, Gozen AG (2012) High level multiple antibiotic resistance among fish surface associated bacterial populations in non-aquaculture freshwater environment. Water Res 46:6382–6390CrossRefGoogle Scholar
  28. Phuong Hoa PT, Nonaka L, Hung Viet P, Suzuki S (2008) Detection of the sul1, sul2, and sul3 genes in sulfonamide-resistant bacteria from wastewater and shrimp ponds of north Vietnam. Sci Total Environ 405:377–384CrossRefGoogle Scholar
  29. Qiao M, Chen WD, Su JQ, Zhang B, Zhang C (2012) Fate of tetracyclines in swine manure of three selected swine farms in China. J Environ Sci-China 24:1047–1052CrossRefGoogle Scholar
  30. Rice EW, Messer JW, Johnson CH, Reasoner DJ (1995) Occurrence of high-level aminoglycoside resistance in environmental isolates of enterococci. Appl Environ Microb 61:374–376Google Scholar
  31. Sidrach-Cardona R, Hijosa-Valsero M, Marti E, Balcazar JL, Becares E (2014) Prevalence of antibiotic-resistant fecal bacteria in a river impacted by both an antibiotic production plant and urban treated discharges. Sci Total Environ 488:220–227CrossRefGoogle Scholar
  32. Smith DD, Kirzinger MW, Stavrinides J (2013) Draft genome sequence of the antibiotic-producing cystic fibrosis isolate Pantoea agglomerans Tx10. Genome Announc 1:e00904–e00913Google Scholar
  33. Su JQ, Wei B, Xu CY, Qiao M, Zhu YG (2014) Functional metagenomic characterization of antibiotic resistance genes in agricultural soils from China. Environ Int 65:9–15CrossRefGoogle Scholar
  34. Sukul P, Lamshoft M, Zuhlke S, Spiteller M (2008) Sorption and desorption of sulfadiazine in soil and soil-manure systems. Chemosphere 73:1344–1350CrossRefGoogle Scholar
  35. Taylor NG, Verner-Jeffreys DW, Baker-Austin C (2011) Aquatic systems: maintaining, mixing and mobilising antimicrobial resistance? Trends Ecol Evol 26:278–284CrossRefGoogle Scholar
  36. Thiele-Bruhn S, Beck IC (2005) Effects of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere 59:457–465CrossRefGoogle Scholar
  37. Wright GD (2007) The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 5:175–186CrossRefGoogle Scholar
  38. Wu H, Wang JT, Shiau YR, Wang HY, Lauderdale TLY, Chang SC, Hosp T (2012) A multicenter surveillance of antimicrobial resistance on Stenotrophomonas maltophilia in Taiwan. J Microbiol Immunol 45:120–126Google Scholar
  39. Wu XL, Xiang L, Yan QY, Jiang YN, Li YW, Huang XP, Li H, Cai QY, Mo CH (2014) Distribution and risk assessment of quinolone antibiotics in the soils from organic vegetable farms of a subtropical city, Southern China. Sci Total Environ 487:399–406CrossRefGoogle Scholar
  40. Zhang Q, Dick WA (2014) Growth of soil bacteria, on penicillin and neomycin, not previously exposed to these antibiotics. Sci Total Environ 493:445–453CrossRefGoogle Scholar
  41. Zhou LJ, Ying GG, Liu S, Zhang RQ, Lai HJ, Chen ZF, Pan CG (2013) Excretion masses and environmental occurrence of antibiotics in typical swine and dairy cattle farms in China. Sci Total Environ 444:183–195CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Like Xu
    • 1
  • Yanyun Qian
    • 1
  • Chao Su
    • 1
  • Weixiao Cheng
    • 1
  • Jianan Li
    • 1
  • Mark L. Wahlqvist
    • 2
  • Hong Chen
    • 1
    Email author
  1. 1.Department of Environmental Engineering, College of Environmental and Resource SciencesZhejiang UniversityHangzhouChina
  2. 2.Fuli Institute of Food ScienceZhejiang UniversityHangzhouChina

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