Abstract
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.
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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 45:2054–2059
Aarestrup FM (2005) Veterinary drug usage and antimicrobial resistance in bacteria of animal origin. Basic Clin Pharmacol 96:271–281
Aga DS, Goldfish R, Kulshrestha P (2003) Application of ELISA in determining the fate of tetracyclines in land-applied livestock wastes. Analyst 128:658
Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486
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 66:25–37
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 490:440–444
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 188:56
Bouki C, Venieri D, Diamadopoulos E (2013) Detection and fate of antibiotic resistant bacteria in wastewater treatment plants: a review. Ecotox Environ Safe 91:1–9
Boxall ABA, Blackwell P, Cavallo R, Kay P, Tolls J (2002) The sorption and transport of a sulphonamide antibiotic in soil systems. Toxicol Lett 131:19–28
Boxall ABA, Fogg LA, Kay P, Blackwell PA, Pemberton EJ, Croxford A (2003) Prioritisation of veterinary medicines in the UK environment. Toxicol Lett 142:207–218
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 304:18–25
Cruz AT, Cazacu AC, Allen CH (2007) Pantoea agglomerans, a plant pathogen causing human disease. J Clin Microbiol 45:1989–1992
Cully M (2014) Public health: the politics of antibiotics. Nature 509:S16–S17
Davis JG, Truman CC, Kim SC, Ascough JC, Carlson K (2006) Antibiotic transport via runoff and soil loss. J Environ Qual 35:2250–2260
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 26:73–78
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 69:5336–5342
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
Geng Y, Doberstein B (2008) Developing the circular economy in China: challenges and opportunities for achieving ‘leapfrog development’. Int J Sust Dev World 15:231–239
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 37:230–234
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
Hvistendahl M (2012) PUBLIC HEALTH. China takes aim at rampant antibiotic resistance. Science 336:795–795
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 93:267–278
Kumar K, Gupta SC, Baidoo SK, Chander Y, Rosen CJ (2005) Antibiotic uptake by plants from soil fertilized with animal manure. J Environ Qual 34:2082–2085
Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663
Munir M, Xagoraraki I (2011) Levels of antibiotic resistance genes in manure, biosolids, and fertilized soil. J Environ Qual 40:248–255
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–e607
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 46:6382–6390
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 405:377–384
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 24:1047–1052
Rice EW, Messer JW, Johnson CH, Reasoner DJ (1995) Occurrence of high-level aminoglycoside resistance in environmental isolates of enterococci. Appl Environ Microb 61:374–376
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 488:220–227
Smith DD, Kirzinger MW, Stavrinides J (2013) Draft genome sequence of the antibiotic-producing cystic fibrosis isolate Pantoea agglomerans Tx10. Genome Announc 1:e00904–e00913
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 65:9–15
Sukul P, Lamshoft M, Zuhlke S, Spiteller M (2008) Sorption and desorption of sulfadiazine in soil and soil-manure systems. Chemosphere 73:1344–1350
Taylor NG, Verner-Jeffreys DW, Baker-Austin C (2011) Aquatic systems: maintaining, mixing and mobilising antimicrobial resistance? Trends Ecol Evol 26:278–284
Thiele-Bruhn S, Beck IC (2005) Effects of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere 59:457–465
Wright GD (2007) The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 5:175–186
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 45:120–126
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 487:399–406
Zhang Q, Dick WA (2014) Growth of soil bacteria, on penicillin and neomycin, not previously exposed to these antibiotics. Sci Total Environ 493:445–453
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 444:183–195
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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).
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Xu, L., Qian, Y., Su, C. et al. Prevalence of bacterial resistance within an eco-agricultural system in Hangzhou, China. Environ Sci Pollut Res 23, 21369–21376 (2016). https://doi.org/10.1007/s11356-016-7345-2
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DOI: https://doi.org/10.1007/s11356-016-7345-2