Skip to main content
SpringerLink
Log in

Increasing prevalence of antibiotic resistance genes in manured agricultural soils in northern China

  • Research Article
  • Published:
Frontiers of Environmental Science & Engineering Aims and scope Submit manuscript

Abstract

Land application of manure tends to result in the dissemination of antibiotic resistance in the environment. In this study, the influence of long-term manure application on the enrichment of antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs) in agricultural soils was investigated. All the analyzed eight ARGs (tetA, tetW, tetX, sulI, sulII, ermF, aac(6′)-Ib-cr and blaTEM) and two MGEs (intI1 and Tn916/1545) were detected in both the manured and control soils, with relative abundances ranging from 10−6 to 10−2. Compared with the control soil, the relative abundances of ARGs and MGEs in manured soils were enriched 1.0–18.1 fold and 0.6–69.1 fold, respectively. High-throughput sequencing analysis suggested that at the phylum level, the bacteria carrying intI1 and ermF might be mainly affiliated with Proteobacteria and Bacteroides, respectively. The dominant genera carrying intI1 and ermF could be Pseudomonas and Bacteroides, independent of manure application. Correlation analysis revealed that ARGs had strong links with soil physicochemical properties (TC, TN, and OM), heavy metals (Cu, Zn and Pb) and MGEs, indicating that the profile and spread of ARGs might be driven by the combined impacts of multiple factors. In contrast, soil pH and C/N exhibited no significant relationships with ARGs. Our findings provide evidence that long-term manure application could enhance the prevalence and stimulate the propagation of antibiotic resistance in agricultural soils.

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

Similar content being viewed by others

References

  • Agersø Y, Sandvang D (2005). Class 1 integrons and tetracycline resistance genes in Alcaligenes, Arthrobacter, and Pseudomonas spp. isolated from pigsties and manured soil. Applied and Environmental Microbiology, 71(12)): 7941–7947

    Article  CAS  Google Scholar 

  • Aminov R I, Garrigues-Jeanjean N, Mackie R I (2001). Molecular ecology of tetracycline resistance: Development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Applied and Environmental Microbiology, 67(1)): 22–32

    Article  CAS  Google Scholar 

  • Brenciani A, Tiberi E, Bacciaglia A, Petrelli D, Varaldo P E, Giovanetti E (2011). Two distinct genetic elements are responsible for erm(TR)-mediated erythromycin resistance in tetracycline-susceptible and tetracycline-resistant strains of Streptococcus pyogenes. Antimicrobial Agents and Chemotherapy, 55(5)): 2106–2112

    Article  CAS  Google Scholar 

  • Byrne-Bailey K G, Gaze W H, Zhang L, Kay P, Boxall A, Hawkey P M, Wellington E M (2011). Integron prevalence and diversity in manured soil. Applied and Environmental Microbiology, 77(2)): 684–687

    Article  CAS  Google Scholar 

  • Chen J, Yu Z, Michel F C Jr, Wittum T, Morrison M (2007). Development and application of real-time PCR assays for quantification of erm genes conferring resistance to macrolides-lincosamides-streptogramin B in livestock manure and manure management systems. Applied and Environmental Microbiology, 73(14)): 4407–4416

    Article  CAS  Google Scholar 

  • Chen Q, An X, Li H, Su J, Ma Y, Zhu Y G (2016). Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil. Environment International, 92–93: 1–10

    Article  CAS  Google Scholar 

  • Chung W O, Werckenthin C, Schwarz S, Roberts M C (1999). Host range of the ermF rRNA methylase gene in bacteria of human and animal origin. Journal of Antimicrobial Chemotherapy, 43(1)): 5–14

    Article  CAS  Google Scholar 

  • Cui E, Wu Y, Zuo Y, Chen H (2016). Effect of different biochars on antibiotic resistance genes and bacterial community during chicken manure composting. Bioresource Technology, 203): 11–17

    Article  CAS  Google Scholar 

  • Eitel Z, Sóki J, Urbán E, Nagy E (2013). The prevalence of antibiotic resistance genes in Bacteroides fragilis group strains isolated in different European countries. Anaerobe, 21): 43–49

    Article  CAS  Google Scholar 

  • Forsberg K J, Reyes A, Wang B, Selleck E M, Sommer M O, Dantas G (2012). The shared antibiotic resistome of soil bacteria and human pathogens. Science, 337(6098)): 1107–1111

    Article  CAS  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 Research, 46(7)): 2355–2364

    Article  CAS  Google Scholar 

  • Gillings M R, Gaze W H, Pruden A, Smalla K, Tiedje J M, Zhu Y G (2015). Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME Journal, 9(6)): 1269–1279

    Article  CAS  Google Scholar 

  • Guo A, Gu J, Wang X, Zhang R, Yin Y, Sun W, Tuo X, Zhang L (2017). Effects of superabsorbent polymers on the abundances of antibiotic resistance genes, mobile genetic elements, and the bacterial community during swine manure composting. Bioresource Technology, 244(Pt 1)): Pt 1

    Google Scholar 

  • Guo T, Lou C, Zhai W, Tang X, Hashmi M Z, Murtaza R, Li Y, Liu X, Xu J (2018). Increased occurrence of heavy metals, antibiotics and resistance genes in surface soil after long-term application ofmanure. Science of the Total Environment, 635): 995–1003

    Article  CAS  Google Scholar 

  • Hardwick S A, Stokes H W, Findlay S, Taylor M, Gillings M R (2008). Quantification of class 1 integron abundance in natural environments using real-time quantitative PCR. FEMS Microbiology Letters, 278(2)): 207–212

    Article  CAS  Google Scholar 

  • Heuer H, Schmitt H, Smalla K (2011). Antibiotic resistance gene spread due to manure application on agricultural fields. Current Opinion in Microbiology, 14(3)): 236–243

    Article  CAS  Google Scholar 

  • Hvistendahl M (2012). China takes aim at rampant antibiotic resistance. Science, 336(6083): 795

    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. Journal of Hazardous Materials, 235–236(20): 178–185

    Article  CAS  Google Scholar 

  • Johnsen B O, Handal N, Meisal R, Bjørnholt J V, Gaustad P, Leegaard T M (2017). erm gene distribution among Norwegian Bacteroides isolates and evaluation of phenotypic tests to detect inducible clindamycin resistance in Bacteroides species. Anaerobe, 47): 226–232

    Article  CAS  Google Scholar 

  • Liu P, Jia S, He X, Zhang X, Ye L (2017). Different impacts of manure and chemical fertilizers on bacterial community structure and antibiotic resistance genes in arable soils. Chemosphere, 188): 455–464

    Article  CAS  Google Scholar 

  • Lu R K (2000). Analysis Methods of Soil and Agricultural Chemistry. Beijing: Chinese Agriculture and Technology Press (in Chinese)

    Google Scholar 

  • Luo G, Rensing C, Chen H, Liu M Q, Wang M, Guo S W, Ling N, Shen Q R (2018). Deciphering the associations between soil microbial diversity and ecosystem multifunctionality driven by long-term fertilization management. Functional Ecology, 32(4)): 1103–1116

    Article  Google Scholar 

  • Negreanu Y, Pasternak Z, Jurkevitch E, Cytryn E (2012). Impact of treated wastewater irrigation on antibiotic resistance in agricultural soils. Environmental Science & Technology, 46(9)): 4800–4808

    Article  CAS  Google Scholar 

  • Ng L K, Martin I, Alfa M, Mulvey M (2001). Multiplex PCR for the detection of tetracycline resistant genes. Molecular and Cellular Probes, 15(4)): 209–215

    Article  CAS  Google Scholar 

  • Nguyen C C, Hugie C N, Kile M L, Navab-Daneshmand T (2019). Association between heavy metals and antibiotic-resistant human pathogens in environmental reservoirs: A review. Frontiers of Environmental Science & Engineering, 13(3): 46

    Article  CAS  Google Scholar 

  • Peng S, Feng Y, Wang Y, Guo X, Chu H, Lin X (2017). Prevalence of antibiotic resistance genes in soils after continually applied with different manure for 30 years. Journal of Hazardous Materials, 340): 16–25

    Article  CAS  Google Scholar 

  • Pruden A, Pei R, Storteboom H, Carlson K H (2006). Antibiotic resistance genes as emerging contaminants: Studies in northern Colorado. Environmental Science & Technology, 40(23)): 7445–7450

    Article  CAS  Google Scholar 

  • Pu C, Liu H, Ding G, Sun Y, Yu X, Chen J, Ren J, Gong X (2018). Impact of direct application of biogas slurry and residue in fields: In situ analysis of antibiotic resistance genes from pig manure to fields. Journal of Hazardous Materials, 344): 441–449

    Article  CAS  Google Scholar 

  • Rosewarne C P, Pettigrove V, Stokes H W, Parsons Y M (2010). Class 1 integrons in benthic bacterial communities: Abundance, association with Tn402-like transposition modules and evidence for coselection with heavy-metal resistance. FEMS Microbiology Ecology, 72(1)): 35–46

    Article  CAS  Google Scholar 

  • Sharma V K, Johnson N, Cizmas L, McDonald T J, Kim H (2016). A review of the influence of treatment strategies on antibiotic resistant bacteria and antibiotic resistance genes. Chemosphere, 150): 702–714

    Article  CAS  Google Scholar 

  • Sharma V K, Yu X, McDonald T J, Jinadatha C, Dionysiou D D, Feng M (2019). Elimination of antibiotic resistance genes and control of horizontal transfer risk by UV-based treatment of drinking water: A mini review. Frontiers of Environmental Science & Engineering, 13(3): 37

    Article  CAS  Google Scholar 

  • Shi J, Yu X, Zhang M, Lu S, Wu W, Wu J, Xu J (2011). Potential risks of copper, zinc, and cadmium pollution due to pig manure application in a soil-rice system under intensive farming: a case study of Nanhu, China. Journal of Environmental Quality, 40(6)): 1695–1704

    Article  CAS  Google Scholar 

  • Suzuki M T, Taylor L T, DeLong E F (2000). Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5′-nuclease assays. Applied and Environmental Microbiology, 66(11)): 4605–4614

    Article  CAS  Google Scholar 

  • Udikovic-Kolic N, Wichmann F, Broderick N A, Handelsman J (2014). Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proceedings of the National Academy of Sciences of the United States of America, 111(42)): 15202–15207

    Article  CAS  Google Scholar 

  • Wang F H, Qiao M, Lv Z E, Guo G X, Jia Y, Su Y H, Zhu Y G (2014). Impact of reclaimed water irrigation on antibiotic resistance in public parks, Beijing, China. Environmental Pollution, 184): 247–253

    Article  CAS  Google Scholar 

  • Wang M, Liu P, Xiong W, Zhou Q, Wangxiao J, Zeng Z, Sun Y (2018). Fate of potential indicator antimicrobial resistance genes (ARGs) and bacterial community diversity in simulated manure-soil microcosms. Ecotoxicology and Environmental Safety, 147): 817–823

    Article  CAS  Google Scholar 

  • Wu N, Qiao M, Zhang B, Cheng W D, Zhu Y G (2010). Abundance and diversity of tetracycline resistance genes in soils adjacent to representative swine feedlots in China. Environmental Science & Technology, 44(18)): 6933–6939

    Article  CAS  Google Scholar 

  • Xie W Y, Yuan S T, Xu M G, Yang X P, Shen Q R, Zhang W W, Su J Q, Zhao F J (2018). Long-term effects ofmanure and chemical fertilizers on soil antibiotic resistome. Soil Biology & Biochemistry, 122): 111–119

    Article  CAS  Google Scholar 

  • Xiong W, Sun Y, Ding X, Zhang Y, Zhong X, Liang W, Zeng Z (2015). Responses of plasmid-mediated quinolone resistance genes and bacterial taxa to (fluoro)quinolones-containing manure in arable soil. Chemosphere, 119): 473–478

    Article  CAS  Google Scholar 

  • Xu Y, Yu W, Ma Q, Zhou H (2015). Occurrence of (fluoro)quinolones and (fluoro)quinolone resistance in soil receiving swine manure for 11 years. Science of the Total Environment, 530–531: 191–197

    Article  CAS  Google Scholar 

  • Yang F, Zhang K, Zhi S, Li J, Tian X, Gu Y, Zhou J (2019). High prevalence and dissemination of β-lactamase genes in swine farms in northern China. Science of the Total Environment, 651(Pt 2)): Pt 2

    Google Scholar 

  • Zhang A N, Li L G, Ma L, Gillings M R, Tiedje J M, Zhang T (2018a). Conserved phylogenetic distribution and limited antibiotic resistance of class 1 integrons revealed by assessing the bacterial genome and plasmid collection. Microbiome, 6(1): 130

    Article  Google Scholar 

  • Zhang J, Chen M, Sui Q, Tong J, Jiang C, Lu X, Zhang Y, Wei Y (2016). Impacts of addition of natural zeolite or a nitrification inhibitor on antibiotic resistance genes during sludge composting. Water Research, 91): 339–349

    Article  CAS  Google Scholar 

  • Zhang L, Gu J, Wang X, Zhang R, Tuo X, Guo A, Qiu L (2018b). Fate of antibiotic resistance genes and mobile genetic elements during anaerobic co-digestion of Chinese medicinal herbal residues and swine manure. Bioresource Technology, 250: 799–805

    Article  CAS  Google Scholar 

  • Zhang S, Zhang F, Liu X, Wang Y, Zou S, He X (2005). Determination and analysis on main harmful composition in excrement of scale livestock and poultry feedlots. Plant Nutrition and Fertilizing Science, 11(6)): 822–829 (in Chinese)

    Google Scholar 

  • Zhang X, Wu B, Zhang Y, Zhang T, Yang L, Fang H H P, Ford T, Cheng S (2009). Class 1 integronase gene and tetracycline resistance genes tetA and tetC in different water environments of Jiangsu Province, China. Ecotoxicology (London, England), 18(6)): 652–660

    Article  CAS  Google Scholar 

  • Zhang Y J, Hu H W, Gou M, Wang J T, Chen D, He J Z (2017). Temporal succession of soil antibiotic resistance genes following application of swine, cattle and poultry manures spiked with or without antibiotics. Environmental Pollution, 231(Pt 2)): Pt 2

    Google Scholar 

  • Zhao Z, Wang J, Han Y, Chen J, Liu G, Lu H, Yan B, Chen S (2017). Nutrients, heavy metals and microbial communities co-driven distribution of antibiotic resistance genes in adjacent environment of mariculture. Environmental Pollution, 220(Pt B)): Pt B

    Google Scholar 

  • Zhou X, Qiao M, Wang F H, Zhu Y G (2017). Use of commercial organic fertilizer increases the abundance of antibiotic resistance genes and antibiotics in soil. Environmental Science and Pollution Research International, 24(1)): 701–710

    Article  CAS  Google Scholar 

  • Zhu B, Chen Q, Chen S, Zhu Y G (2017). Does organically produced lettuce harbor higher abundance of antibiotic resistance genes than conventionally produced? Environment International, 98: 152–159

    Article  CAS  Google Scholar 

  • Zhu Y G, Johnson T A, Su J Q, Qiao M, Guo G X, Stedtfeld R D, Hashsham S A, Tiedje J M (2013). Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proceedings of the National Academy of Sciences of the United States of America, 110(9)): 3435–3440

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the National Natural Science Foundation of China (Grant No. 21607114) and Science and Technology Correspondent Project of Tianjin (No. 18JCTPJC55100). We also appreciated the help from Professors Xiaomei Wang and Xiaodong Xie during sample analysis. Thanks to Chunjie Li and Fahui Liang for sample collection.

Author information

Authors and Affiliations

  1. College of Engineering and Technology, Tianjin Agricultural University, Tianjin, 300384, China

    Nan Wu, Weiyu Zhang, Shiyu Xie, Xinyuan Liu & Fan Yang

  2. College of Marine and Environmental Sciences, Tianjin University of Science & Technology, Tianjin, 300457, China

    Ming Zeng

  3. Laboratory of Agricultural Analysis, Tianjin Agricultural University, Tianjin, 300384, China

    Haixue Liu

  4. College of Horticulture and Landscape, Tianjin Agricultural University, Tianjin, 300384, China

    Jinghui Yang

Authors
  1. Nan Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Weiyu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shiyu Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ming Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Haixue Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jinghui Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xinyuan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Fan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ming Zeng.

Additional information

Highlights

• Manure application increased the abundances of ARGs and MGEs in agricultural soils.

• Five classes of ARGs and two MGEs were prevalent in manured and unfertilized soils.

• Genera Pseudomonas and Bacteroidetes might be the dominant hosts of intIl and ermF.

• The abundances of ARGs positively correlated with TC, TN, OM, Cu, Zn, Pb and MGEs.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, N., Zhang, W., Xie, S. et al. Increasing prevalence of antibiotic resistance genes in manured agricultural soils in northern China. Front. Environ. Sci. Eng. 14, 1 (2020). https://doi.org/10.1007/s11783-019-1180-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11783-019-1180-x

Keywords

Search

Navigation