Skip to main content

Advertisement

Springer Nature Link
Log in

Antibiotic resistance genes in manure-amended paddy soils across eastern China: Occurrence and influencing factors

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

Abstract

Pig manure, rich in antibiotics and metals, is widely applied in paddy fields as a soil conditioner, triggering the proliferation of antibiotic resistance genes (ARGs) in soil. However, comprehensive studies on the effects of manure fertilization on the abundance of ARGs and their influencing factors are still insufficient. Here, pig manure and manure-amended and inorganic-amended soils were collected from 11 rice-cropping regions in eastern China, and the accumulation of antibiotics, metals, and ARGs was assessed simultaneously. The results showed that manure fertilization led to antibiotic residues and increased the metal content (i.e., Zn, Cu, Ni, and Cr). Tetracycline and sulfonamide resistance genes (tetM, tetO, sul1, and sul2) were also significantly enhanced with manure fertilization. According to variance partitioning analysis, the most important factors that individually influenced ARGs were soil physicochemical properties, accounting for 12% of the variation. Significant correlations between soil nutrients and ARGs indicated that manure application enhanced the growth of resistant microorganisms by supplying more nutrients. Metals and antibiotics contributed 9% and 5% to the variations in ARGs, respectively. Their co-occurrence also increased the enrichment of ARGs, as their interactions accounted for 2% of the variation in ARGs. Interestingly, Cu was significantly related to most ARGs in the soil (r = 0.26–0.52, p < 0.05). Sulfapyridine was significantly related to sul2, and tetracycline resistance genes were positively related to doxycycline. This study highlighted the risks of antibiotic and ARG accumulation with manure fertilization and shed light on the essential influencing factors of ARGs in paddy soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • An J, Chen H, Wei S, Gu J (2015). Antibiotic contamination in animal manure, soil, and sewage sludge in Shenyang, Northeast China. Environmental Earth Sciences, 74(6): 5077–5086

    Article  CAS  Google Scholar 

  • Baker-Austin C, Wright M S, Stepanauskas R, McArthur J V (2006). Co-selection of antibiotic and metal resistance. Trends in Microbiology, 14(4): 176–182

    Article  CAS  Google Scholar 

  • Berg J, Tom-Petersen A, Nybroe O (2005). Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field. Letters in Applied Microbiology, 40(2): 146–151

    Article  CAS  Google Scholar 

  • Chopra I, Roberts M (2001). Tetracycline antibiotics: Mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiology and Molecular Biology Reviews, 65(2): 232–260

    Article  CAS  Google Scholar 

  • Cui E P, Gao F, Liu Y, Fan X Y, Li Z Y, Du Z J, Hu C, Neal A L (2018). Amendment soil with biochar to control antibiotic resistance genes under unconventional water resources irrigation: Proceed with caution. Environmental Pollution, 240: 475–484

    Article  CAS  Google Scholar 

  • Deng W, Zhang A, Chen S, He X, Jin L, Yu X, Yang S, Li B, Fan L, Ji L, Pan X, Zou L (2020). Heavy metals, antibiotics and nutrients affect the bacterial community and resistance genes in chicken manure composting and fertilized soil. Journal of Environmental Management, 257: 109980

    Article  CAS  Google Scholar 

  • González-Alcaraz M N, van Gestel C A M (2015). Climate change effects on enchytraeid performance in metal-polluted soils explained from changes in metal bioavailability and bioaccumulation. Environmental Research, 142: 177–184

    Article  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 of manure. Science of the Total Environment, 635: 995–1003

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Heuer H, Solehati Q, Zimmerling U, Kleineidam K, Schloter M, Müller T, Focks A, Thiele-Bruhn S, Smalla K (2011b). Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine. Applied and Environmental Microbiology, 77(7): 2527–2530

    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: 178–185

    Article  Google Scholar 

  • Johnsen P J, Townsend J P, Bøhn T, Simonsen G S, Sundsfjord A, Nielsen K M (2009). Factors affecting the reversal of antimicrobial-drug resistance. Lancet. Infectious Diseases, 9(6): 357–364

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kim S Y, Kuppusamy S, Kim J H, Yoon Y E, Kim K R, Lee Y B (2016). Occurrence and diversity of tetracycline resistance genes in the agricultural soils of Korea. Environmental Science and Pollution Research International, 23(21): 22190–22196

    Article  CAS  Google Scholar 

  • Knapp C W, McCluskey S M, Singh B K, Campbell C D, Hudson G, Graham D W (2011). Antibiotic resistance gene abundances correlate with metal and geochemical conditions in archived Scottish soils. PLoS One, 6(11): e27300

    Article  CAS  Google Scholar 

  • Kolz A C, Moorman T B, Ong S K, Scoggin K D, Douglass E A (2005). Degradation and metabolite production of tylosin in anaerobic and aerobic swine-manure lagoons. Water Environment Research, 77(1): 49–56

    Article  CAS  Google Scholar 

  • Li Y X, Zhang X L, Li W, Lu X F, Liu B, Wang J (2013). The residues and environmental risks of multiple veterinary antibiotics in animal faeces. Environmental Monitoring and Assessment, 185(3): 2211–2220

    Article  CAS  Google Scholar 

  • Liang Y, Pei M, Wang D, Cao S, Xiao X, Sun B (2017). Improvement of soil ecosystem multifunctionality by dissipating Manure-Induced antibiotics and resistance genes. Environmental Science & Technology, 51(9): 4988–4998

    Article  CAS  Google Scholar 

  • Liu W, Zeng D, She L, Su W, He D, Wu G, Ma X, Jiang S, Jiang C, Ying G (2020). Comparisons of pollution characteristics, emission situations, and mass loads for heavy metals in the manures of different livestock and poultry in China. Science of the Total Environment, 734: 139023

    Article  CAS  Google Scholar 

  • Lu R (1999). Soil Agricultural Chemical Analysis. Nanjing: China Agricultural Science and Technology Press (in Chinese)

    Google Scholar 

  • Luo L, Ma Y, Zhang S, Wei D, Zhu Y G (2009). An inventory of trace element inputs to agricultural soils in China. Journal of Environmental Management, 90(8): 2524–2530

    Article  CAS  Google Scholar 

  • Mahmoud M A M, Abdel-Mohsein H S (2019). Hysterical tetracycline in intensive poultry farms accountable for substantial gene resistance, health and ecological risk in Egypt- manure and fish. Environmental Pollution, 255(Pt 1): 113039

    Article  CAS  Google Scholar 

  • Martínez-Carballo E, González-Barreiro C, Scharf S, Gans O (2007). Environmental monitoring study of selected veterinary antibiotics in animal manure and soils in Austria. Environmental Pollution, 148(2): 570–579

    Article  Google Scholar 

  • Pan X, Qiang Z, Ben W, Chen M (2011). Residual veterinary antibiotics in swine manure from concentrated animal feeding operations in Shandong Province, China. Chemosphere, 84(5): 695–700

    Article  CAS  Google Scholar 

  • Pan M, Chu L M (2016). Adsorption and degradation of five selected antibiotics in agricultural soil. Science of the Total Environment, 545–546: 48–56

    Article  Google Scholar 

  • Pei R, Cha J, Carlson K H, Pruden A (2007). Response of antibiotic resistance genes (ARG) to biological treatment in dairy lagoon water. Environmental Science & Technology, 41(14): 5108–5113

    Article  CAS  Google Scholar 

  • Rahman M M, Shan J, Yang P, Shang X, Xia Y, Yan X (2018). Effects of long-term pig manure application on antibiotics, abundance of antibiotic resistance genes (ARGs), anammox and denitrification rates in paddy soils. Environmental Pollution, 240: 368–377

    Article  CAS  Google Scholar 

  • Tang X, Lou C, Wang S, Lu Y, Liu M, Hashmi M Z, Liang X, Li Z, Liao Y, Qin W, Fan F, Xu J, Brookes P C (2015). Effects of long-term manure applications on the occurrence of antibiotics and antibiotic resistance genes (ARGs) in paddy soils: Evidence from four field experiments in south of China. Soil Biology and Biochemistry, 90: 179–187

    Article  CAS  Google Scholar 

  • Van den Meersche T, Rasschaert G, Haesebrouck F, Van Coillie E, Herman L, Van Weyenberg S, Daeseleire E, Heyndrickx M (2019). Presence and fate of antibiotic residues, antibiotic resistance genes and zoonotic bacteria during biological swine manure treatment. Ecotoxicology and Environmental Safety, 175: 29–38

    Article  CAS  Google Scholar 

  • Van den Meersche T, Rasschaert G, Vanden Nest T, Haesebrouck F, Herman L, Van Coillie E, Van Weyenberg S, Daeseleire E, Heyndrickx M (2020). Longitudinal screening of antibiotic residues, antibiotic resistance genes and zoonotic bacteria in soils fertilized with pig manure. Environmental Science and Pollution Research International, 27(22): 28016–28029

    Article  CAS  Google Scholar 

  • Wang L, Wang J, Wang J, Zhu L, Conkle J L, Yang R (2020). Soil types influence the characteristic of antibiotic resistance genes in greenhouse soil with long-term manure application. Journal of Hazardous Materials, 392: 122334

    Article  CAS  Google Scholar 

  • Wang L, Zhao X, Wang J, Wang J, Zhu L, Ge W (2019). Macrolide- and quinolone-resistant bacteria and resistance genes as indicators of antibiotic resistance gene contamination in farmland soil with manure application. Ecological Indicators, 106: 105456

    Article  CAS  Google Scholar 

  • Yang S, Qu Y, Ma J, Liu L, Wu H, Liu Q, Gong Y, Chen Y, Wu Y (2020). Comparison of the concentrations, sources, and distributions of heavy metal(loid)s in agricultural soils of two provinces in the Yangtze River Delta, China. Environmental Pollution, 264: 114688

    Article  CAS  Google Scholar 

  • Zhang Q Q, Tian G M, Jin R C (2018). The occurrence, maintenance, and proliferation of antibiotic resistance genes (ARGs) in the environment: influencing factors, mechanisms, and elimination strategies. Applied Microbiology and Biotechnology, 102(19): 8261–8274

    Article  CAS  Google Scholar 

  • Zhang R, Tang J, Li J, Zheng Q, Liu D, Chen Y, Zou Y, Chen X, Luo C, Zhang G (2013). Antibiotics in the offshore waters of the Bohai Sea and the Yellow Sea in China: Occurrence, distribution and ecological risks. Environmental Pollution, 174: 71–77

    Article  CAS  Google Scholar 

  • Zhou B, Wang C, Zhao Q, Wang Y, Huo M, Wang J, Wang S (2016). Prevalence and dissemination of antibiotic resistance genes and coselection of heavy metals in Chinese dairy farms. Journal of Hazardous Materials, 320: 10–17

    Article  CAS  Google Scholar 

  • Zhou J, Bruns M A, Tiedje J M (1996). DNA recovery from soils of diverse composition. Applied and Environmental Microbiology, 62(2): 316–322

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by National Natural Science Foundation of China (Grant Nos. 41877060 and 42007027), Youth Innovation Promotion Association of Chinese Academy of Sciences (No. 2016284), Scholar Program of the Jiangsu Province (China) (No. BRA2019333), and Top — Notch Young Talents Program of China (No. W03070089).

Author information

Authors and Affiliations

  1. School of Environmental and Safety Engineering, Changzhou University, Changzhou, 213164, China

    Yuwei Guo, Xian Xiao, Yuan Zhao & Jianguo Liu

  2. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China

    Yuwei Guo, Bo Sun & Yuting Liang

  3. Institute for Environmental Genomics, Department of Microbiology and Plant Biology, and School of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK, 73019, USA

    Jizhong Zhou

  4. State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, 100084, China

    Jizhong Zhou

  5. Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, 94270, USA

    Jizhong Zhou

Authors
  1. Yuwei Guo
    View author publications

    Search author on:PubMed Google Scholar

  2. Xian Xiao
    View author publications

    Search author on:PubMed Google Scholar

  3. Yuan Zhao
    View author publications

    Search author on:PubMed Google Scholar

  4. Jianguo Liu
    View author publications

    Search author on:PubMed Google Scholar

  5. Jizhong Zhou
    View author publications

    Search author on:PubMed Google Scholar

  6. Bo Sun
    View author publications

    Search author on:PubMed Google Scholar

  7. Yuting Liang
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Yuting Liang.

Additional information

Highlights

• Manure fertilization resulted in antibiotic residues and increased metal contents.

• The tet and sul genes were significantly enhanced with manure fertilization.

• Soil physicochemical properties contributed to 12% of the variations in ARGs.

• Soil metals and antibiotics co-select for ARGs.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, Y., Xiao, X., Zhao, Y. et al. Antibiotic resistance genes in manure-amended paddy soils across eastern China: Occurrence and influencing factors. Front. Environ. Sci. Eng. 16, 91 (2022). https://doi.org/10.1007/s11783-021-1499-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11783-021-1499-y

Keywords