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The residue of tetracycline antibiotics in soil and Brassica juncea var. gemmifera, and the diversity of soil bacterial community under different livestock manure treatments

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Abstract

Tetracycline antibiotics (TCs) are a broad-spectrum antibiotic, widely used in livestock and poultry breeding. Residue of tetracycline antibiotics in animal manure may cause changes in vegetable TCs content and soil microbial community. On the basis of the investigation and analysis of TCs pollution in the soil of main vegetable bases and the livestock manure of major large-scale farms in Chongqing, China, field experiment was conducted to study the residues of tetracycline antibiotics in Brassica juncea var. gemmifera and soil under different kinds and different dosages of livestock manures. Effects of tetracycline antibiotics on the structure and diversity of soil microbial community were also investigated by high-throughput sequencing. TCs content in soil was increased by applying livestock manure. The contents of tetracycline, oxytetracycline (OTC) and chlortetracycline (CTC) in the soil under pig manure treatment were 171.07–660.20 μg kg−1, 25.38–345.78 μg kg−1 and 170.77–707.47 μg kg−1, respectively. The contents of TC, OTC and CTC in the soil under the treatment of chicken manure were 166.62–353.61 μg kg−1, 122.25–251.23 μg kg−1 and 15.12–80.91 μg kg−1, respectively. TCs in edible parts of Brassica juncea var. gemmifera was increased after livestock manure treatment Proteobacteria, Acidobacteria, Actinobacteria, Chioroflexi and Bacteroidetes under livestock manure treatment were the dominant phyla, accounting for 85.2–92.4% of the total abundance of soil bacteria. The soil OTUs under the treatment of pig manure was higher than that under the treatment of chicken manure. Biogas residue (Livestock manure after fermentation treatment) can effectively reduce the environmental and ecological risks caused by antibiotic residues.

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Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Bonanomi, G., Filippis, D. F., Cesarano, G., Storia, A. L., Ercolini, D., & Scala, F. (2016). Organic farming induces changes in soil microbiota that affect agro-ecosystem functions. Soil Biology and Biochemistry, 103, 327–336. https://doi.org/10.1016/j.soilbio.2016.09.005

    Article  CAS  Google Scholar 

  • Calleja-Cervantes, M. E., Fernández-González, A. J., Irigoyen, I., Fernández-López, M., Aparicio-Tejo, P. M., & Menéndez, S. (2015). Thirteen years of continued application of composted organic wastes in a vineyard modify soil quality characteristics. Soil Biology and Biochemistry, 90, 241–254. https://doi.org/10.1016/j.soilbio.2015.07.002

    Article  CAS  Google Scholar 

  • Chen, Y. S., Zhang, H. B., Luo, Y. M., & Song, J. (2012). Occurrence and assessment of veterinary antibiotics in swine manures: A case study in East China. Chinese Science Bulletin, 57, 606–614. https://doi.org/10.1007/s11434-011-4830-3

    Article  CAS  Google Scholar 

  • Chi, S. L., Wang, W. Z., Xu, W. H., Li, T., & Zhang, C. L. (2018). Effects of tetracycline antibiotics on growth and characteristics of enrichment and transformation in two vegetables. Environmental Science, 39, 935–943.

    Google Scholar 

  • Chung, H. S., Lee, Y. J., Rahman, M. M., Abd, A. M., Lee, H. S., Kabir, M. H., Kim, S. W., Park, B. J., Kim, J. E., Hacımüftüoğlu, F., Nahar, N., Shin, H. C., & Shim, J. H. (2017). Uptake of the veterinary antibiotics chlortetracycline, enrofloxacin, and sulphathiazole from soil by radish. The Science of the total environment, 605, 322–331. https://doi.org/10.1016/j.scitotenv.2017.06.231

    Article  CAS  Google Scholar 

  • Duan, M. L., Li, H. C., Gu, J., Tuo, X. X., Sun, W., Qian, X., & Wang, X. J. (2017). Effects of biochar on reducing the abundance of oxytetracycline, antibiotic resistance genes, and human pathogenic bacteria in soil and lettuce. Environmental Pollution, 224, 787–795. https://doi.org/10.1016/j.envpol.2017.01.021

    Article  CAS  Google Scholar 

  • European Medicines Agency (EMEA). (2008). Guideline on Environmental Impact Assessment for Veterinary Medicinal Products. In Support of the VICH Guideline GL6 and GL38. https://www.EMEA/CVMP/ERA/418282/2005-Rev.1.

  • Francioli, D., Schulz, E., Lentendu, G., Wubet, T., Buscot, F., & Reitz, T. (2016). Mineral versus Organic amendments: microbial community structure, activity and abundance of agriculturally relevant microbes are driven by long-term fertilization strategies. Frontiers in Microbiology, 17, 1446.

    Google Scholar 

  • Goldstein, M., Shenker, M., & Chefetz, B. (2014). Insights into the uptake processes of wastewater-borne pharmaceuticals by vegetables. Environmental Science & Technology, 48, 5593–5600. https://doi.org/10.1021/es5008615

    Article  CAS  Google Scholar 

  • Hartmann, M., Frey, B., Mayer, J., Mäder, P., & Widmer, F. (2015). Distinct soil microbial diversity under long-term organic and conventional farming. The ISME Journal, 9, 1177–1194. https://doi.org/10.1038/ismej.2014.210

    Article  Google Scholar 

  • Hess, M., Sczyrba, A., & Egan, R. (2011). Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science (New York, N.Y.). Science, 331, 463–467. https://doi.org/10.1126/science.1200387

    Article  CAS  Google Scholar 

  • Hu, X. G., Zhou, Q. X., & Luo, Y. (2010). Occurrence and source analysis of typical veterinary antibiotics in manure, soil, vegetables and groundwater from organic vegetable bases, Northern China. Environmental Pollution, 158, 2992–2998. https://doi.org/10.1016/j.envpol.2010.05.023

    Article  CAS  Google Scholar 

  • Jacobsen, A. M., Halling-Sørensen, B., Ingerslev, F., & Hansen, S. H. (2004). Simultaneous extraction of tetracycline, macrolide and sulfonamide antibiotics from agricultural soils using pressurised liquid extraction, followed by solid-phase extraction and liquid chromatography–tandem mass spectrometry. Journal of Chromatography A, 1038, 157–170. https://doi.org/10.1016/j.chroma.2004.03.034

    Article  CAS  Google Scholar 

  • Kong, W. D., Zhu, Y. G., Liang, Y. C., Zhang, J., Smith, F. A., & Yang, M. (2007). Uptake of oxytetracycline and its phytotoxicity to alfalfa (Medicago sativa L.). Environmental Pollution, 147, 187–193. https://doi.org/10.1016/j.envpol.2006.08.016

    Article  CAS  Google Scholar 

  • Lladó, S., López-Mondéjar, R., & Baldrian, P. (2018). Drivers of microbial community structure in forest soils. Applied Microbiology and Biotechnology, 102, 4331–4338. https://doi.org/10.1007/s00253-018-8950-4

    Article  CAS  Google Scholar 

  • Miller, E. L., Nason, S. L., Karthikeyan, K. G., & Pedersen, J. A. (2016). Root uptake of pharmaceuticals and personal care product ingredients. Environmental Science & Technology, 50, 525–541. https://doi.org/10.1021/acs.est.5b01546

    Article  CAS  Google Scholar 

  • Ninh, H. T., Grandy, A. S., Wickings, K., Snapp, S. S., Kirk, W., & Hao, J. (2015). Organic amendment effects on potato productivity and quality are related to soil microbial activity. Plant and Soil, 386, 223–236. https://doi.org/10.1007/s11104-014-2223-5

    Article  CAS  Google Scholar 

  • Pan, M., & Chu, L. M. (2017). Fate of antibiotics in soil and their uptake by edible crops. Science of the Total Environment, 599–600, 500–512. https://doi.org/10.1016/j.scitotenv.2017.04.214

    Article  CAS  Google Scholar 

  • Prosser, R. S., & Sibley, P. K. (2015). Human health risk assessment of pharmaceuticals and personal care products in plant tissue due to biosolids and manure amendments, and wastewater irrigation. Environment International, 75, 223–233. https://doi.org/10.1016/j.envint.2014.11.020

    Article  CAS  Google Scholar 

  • Quaik, S., Embrandiri, A., Ravindran, B., Hossain, K., Al-Dhabi, N. A., Arasu, M. V., Ignacimuthu, S., & Ismail, N. (2020). Veterinary antibiotics in animal manure and manure laden soil: Scenario and challenges in Asian countries. Journal of King Saud University - Science, 32, 1300–1305. https://doi.org/10.1016/J.JKSUS.2019.11.015

    Article  Google Scholar 

  • Sun, R., Zhang, X. X., Guo, X., Wang, D., & Chu, H. (2015). Bacterial diversity in soils subjected to long-term chemical fertilization can be more stably maintained with the addition of livestock manure than wheat straw. Soil Biology and Biochemistry, 88, 9–18. https://doi.org/10.1016/j.soilbio.2015.05.007

    Article  CAS  Google Scholar 

  • Tamminen, M., Karkman, A., Lõhmus, A., Muziasari, W. I., Takasu, H., Wada, S., Suzuki, S., & Virta, M. (2011). Tetracycline resistance genes persist at aquaculture farms in the absence of selection pressure. Environmental Science & Technology, 45, 386–391. https://doi.org/10.1021/es102725n

    Article  CAS  Google Scholar 

  • Tasho, R. P., & Cho, J. Y. (2016). Veterinary antibiotics in animal waste, its distribution in soil and uptake by plants: A review. Science of the Total Environment, 563–564, 366–376. https://doi.org/10.1016/j.scitotenv.2016.04.140

    Article  CAS  Google Scholar 

  • Wang, H., Jiang, W. J., Yu, H. J., & Yang, X. Y. (2011). Antibiotics in livestock wastes and its enrichment in vegetable crops. China Vegetables, 12, 10–15.

    Google Scholar 

  • Wang, W. Z., Chi, S. L., Xu, W. H., & Zhang, C. L. (2018). Influence of long-term chicken manure application on the concentration of soil tetracycline antibiotics and resistant bacteria variations. Applied Ecology and Environmental Research, 16(2), 1143–1153.

    Article  Google Scholar 

  • Wu, X., Wei, Y., Zheng, J., Zhao, X., & Zhong, W. (2011). The behavior of tetracyclines and their degradation products during swine manure composting. Bioresource Technology, 102(10), 5924–5931. https://doi.org/10.1016/j.biortech.2011.03.007

    Article  CAS  Google Scholar 

  • Wu, X., Dodgen, L. K., Conkle, J. L., & Gan, J. (2015). Plant uptake of pharmaceutical and personal care products from recycled water and biosolids: A review. Science of the Total Environment, 536, 655–666. https://doi.org/10.1016/j.scitotenv.2015.07.129

    Article  CAS  Google Scholar 

  • Xiong, W., Wang, M., Dai, J., Sun, Y., & Zeng, Z. (2018). Application of manure containing tetracyclines slowed down the dissipation of tet resistance genes and caused changes in the composition of soil bacteria. Ecotoxicology and environmental safety, 147, 455–460. https://doi.org/10.1016/j.ecoenv.2017.08.061

    Article  CAS  Google Scholar 

  • Xu, L. S., Wang, W. Z., & Xu, W. H. (2021). Effects of tetracycline antibiotics in chicken manure on soil microbes and resistance genes (ARGs). Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-021-01004-y/EGAH-D-20-01065

    Article  Google Scholar 

  • Yang, Q., Zhang, J., Zhu, K., & Zhang, H. (2009). Influence 0f oxytetracycline on the structure and activity of microbial community in wheat rhizosphere soil. Journal of Environmental Sciences, 21(7), 954–959.

    Article  CAS  Google Scholar 

  • Zhang, Z., Li, C., Huang, S., Gao, W., & Tang, J. (2013). Optimization of residual tetracyclines analysis in soils and manure using SPE-HPLC and pilot survey in Tianjin. Journal of Plant Nutrition and Fertilizers, 19, 713–726.

    CAS  Google Scholar 

  • Zhang, C., Xue, J. M., Cheng, D. M., Feng, Y., Liu, Y., Aly, H. M., & Li, Z. (2019). Uptake, translocation and distribution of three veterinary antibiotics in Zea mays L. Environmental Pollution, 110, 47–57. https://doi.org/10.1016/j.envpol.2019.03.110

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to express our gratitude to the reviewers of this manuscript; their insight was instrumental to improving this paper. Finally, we also thank Ministry of Agriculture and Rural Affairs of the People's Republic of China for the financial support necessary to make all of this work possible.

Funding

This study was funded by Fund of China Agriculture Research System (CARS-23-13B), and the National Key Research and Development Program of China (2018YFD0201200).

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LSX and WHX conceived the study. WZW collected the data presented in the manuscript. LSX, WZW and JBD performed statistical analyses. All authors contributed to the writing and revision of the final manuscript. All authors read and approved the final manuscript.

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Correspondence to W. H. Xu.

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The sampling of soil and vegetable did not require permission and the species are not classified as endangered, and are not under any protection in any of the sampled areas.

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Xu, L.S., Wang, W.Z., Deng, J.B. et al. The residue of tetracycline antibiotics in soil and Brassica juncea var. gemmifera, and the diversity of soil bacterial community under different livestock manure treatments. Environ Geochem Health 45, 7–17 (2023). https://doi.org/10.1007/s10653-022-01213-z

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