Effects of chicken manure-modified biochar on the adsorption capacity of tetracycline and abundance of antibiotic resistance genes in soil
Fangyu Hu
Key Laboratory of Pollution Ecology and Environmental Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China
University of Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorChengcheng Gao
Key Laboratory of Pollution Ecology and Environmental Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China
University of Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorBaoyu Wang
Key Laboratory of Pollution Ecology and Environmental Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China
University of Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorZiming Ding
Key Laboratory of Pollution Ecology and Environmental Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China
University of Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorLijie Zhang
Department of Chemistry and Environmental Science, New Jersey Institute of Technology, New Jersey, USA
Search for more papers by this authorShuhe Wei
Key Laboratory of Pollution Ecology and Environmental Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China
Search for more papers by this authorCorresponding Author
Jing An
Key Laboratory of Pollution Ecology and Environmental Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China
National-Local Joint Engineering Laboratory of Contaminated Soil Remediation by Bio-physicochemical Synergistic Process, Shenyang, China
Correspondence
Jing An, Institute of Applied Ecology, Chinese Academy of Sciences, No. 72, Wenhua Road, Shenyang 110016, China.
Email: [email protected]
Search for more papers by this authorFangyu Hu
Key Laboratory of Pollution Ecology and Environmental Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China
University of Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorChengcheng Gao
Key Laboratory of Pollution Ecology and Environmental Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China
University of Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorBaoyu Wang
Key Laboratory of Pollution Ecology and Environmental Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China
University of Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorZiming Ding
Key Laboratory of Pollution Ecology and Environmental Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China
University of Chinese Academy of Sciences, Beijing, China
Search for more papers by this authorLijie Zhang
Department of Chemistry and Environmental Science, New Jersey Institute of Technology, New Jersey, USA
Search for more papers by this authorShuhe Wei
Key Laboratory of Pollution Ecology and Environmental Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China
Search for more papers by this authorCorresponding Author
Jing An
Key Laboratory of Pollution Ecology and Environmental Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China
National-Local Joint Engineering Laboratory of Contaminated Soil Remediation by Bio-physicochemical Synergistic Process, Shenyang, China
Correspondence
Jing An, Institute of Applied Ecology, Chinese Academy of Sciences, No. 72, Wenhua Road, Shenyang 110016, China.
Email: [email protected]
Search for more papers by this authorFangyu Hu and Chengcheng Gao should be considered joint first authorship.
Abstract
Large quantities of livestock manure not only occupy farmland but also serve as the primary source of antibiotics and antibiotic resistance genes (ARGs) in agricultural soil. To enhance the resource utilization of animal manure and mitigate ecological risks associated with antibiotics in agroecosystems, chicken manure was used as a raw material for biochar production. The manure derived biochar (MB) was modified with an alkali–acid two-step modification process. The results showed that the total pore volume and surface area of alkali–acid modified MB (AMMB) was significantly increased about three and five times, respectively after modification. The SEM images showed that the surface of AMMB had a more regular and clearer structure with fewer impurities. The improvement of surface properties of AMMB significantly increased its adsorbing capacity of tetracycline in the soil. The adsorption kinetics of tetracycline by AMMB were better fitted by the pseudo-second-order kinetic model, suggesting that the adsorption of tetracycline on biochar followed the process of chemisorption. The adsorption mechanisms mainly involved the pore filling, hydrophobic effect, and π–π EDA interaction. Moreover, after a 60 days amendment of AMMB, the total relative abundances (RAs) of tested tetracycline resistance genes (TRGs) in soil decreased significantly, which suggested that AMMB can be a potential material to reduce risks of antibiotics and its resistance genes.
CONFLICT OF INTEREST STATEMENT
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Supporting Information
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| ldr4983-sup-0001-Supinfo.docxWord 2007 document , 125 KB | Appendix S1. Supporting information |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Acosta, R., Fierro, V., De Yuso, A. M., Nabarlatz, D., & Celzard, A. (2016). Tetracycline adsorption onto activated carbons produced by KOH activation of tyre pyrolysis char. Chemosphere, 149, 168–176.
- Ai, T., Jiang, X., Liu, Q., Lv, L., & Wu, H. (2019). Daptomycin adsorption on magnetic ultra-fine wood-based biochars from water: Kinetics, isotherms, and mechanism studies. Bioresource Technology, 273, 8–15.
- An, J., Chen, H., Wei, S., & Gu, J. (2015). Antibiotic contamination in animal manure, soil, and sewage sludge in Shenyang, Northeast China. Environment and Earth Science, 74, 5077–5086.
- Beaber, J. W., Hochhut, B., & Waldor, M. K. (2004). SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature, 427, 72–74.
- Chen, T. W., Luo, L., Deng, S. H., Shi, G. Z., Zhang, S. R., Zhang, Y. Z., Deng, O. P., Wang, L. L., Zhang, J., & Wei, L. Y. (2018). Sorption of tetracycline on H3PO4 modified biochar derived from rice straw and swine manure. Bioresource Technology, 267, 431–437.
- Conde-Cid, M., Álvarez-Esmorís, C., Paradelo-Núñez, R., Nóvoa-Muñoz, J. C., Arias-Estévez, M., Álvarez-Rodríguez, E., Fernández-Sanjurjo, M. J., & Núñez-Delgado, A. (2018). Occurrence of tetracyclines and sulfonamides in manures, agricultural soils and crops from different areas in Galicia (NW Spain). Journal of Cleaner Production, 197, 491–500.
- 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.
- 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.
- Czekala, W., Malinska, K., Caceres, R., Janczak, D., Dach, J., & Lewicki, A. (2016). Co-composting of poultry manure mixtures amended with biochar—The effect of biochar on temperature and C-CO2 emission. Bioresource Technology, 200, 921–927.
- Duan, M., Li, H., Gu, J., Tuo, X., Sun, W., Qian, X., & Wang, X. (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.
- Feng, Z., & Zhu, L. (2018). Sorption of phenanthrene to biochar modified by base. Frontiers of Environmental Science & Engineering, 12, 1–11.
- Gu, Z., & Wang, X. (2013). Carbon materials from high ash bio-char: A nanostructure similar to activated graphene. American Transactions on Engineering & Applied Sciences, 2, 15–34.
- Guo, C., Wang, M., Xiao, H., Huai, B., Wang, F., Pan, G., Liao, X., & Liu, Y. (2016). Development of a modified QuEChERS method for the determination of veterinary antibiotics in swine manure by liquid chromatography tandem mass spectrometry. Journal of Chromatography B, 1027, 110–118.
- Kumar, A., Bhattacharya, T., Shaikh, W. A., Chakraborty, S., Sarkar, D., & Biswas, J. K. (2022). Biochar modification methods for augmenting sorption of contaminants. Current Pollution Reports, 8, 519–555.
- Kumar, R. R., Park, B. J., & Cho, J. Y. (2013). Application and environmental risks of livestock manure. Journal of the Korean Society for Applied Biological Chemistry, 56, 497–503.
10.1007/s13765-013-3184-8 Google Scholar
- Li, H., Hu, J., Meng, Y., Su, J., & Wang, X. (2017). An investigation into the rapid removal of tetracycline using multilayered graphene-phase biochar derived from waste chicken feather. Science of The Total Environment, 603-604, 39–48.
- Li, M., Liu, Q., Guo, L., Zhang, Y., Lou, Z., Wang, Y., & Qian, G. (2013). Cu(II) removal from aqueous solution by Spartina alterniflora derived biochar. Bioresource Technology, 141, 83–88.
- Li, Y., Wang, X., Li, J., Wang, Y., Song, J., Xia, S., Jing, H., & Zhao, J. (2019). Effects of struvite-humic acid loaded biochar/bentonite composite amendment on Zn(II) and antibiotic resistance genes in manure-soil. Chemical Engineering Journal, 375, 122013.
- Li, H., Wang, X., Tan, L., Li, Q., Zhang, C., Wei, X., Wang, Q., Zheng, X., & Xu, Y. (2022). Coconut shell and its biochar as fertilizer amendment applied with organic fertilizer: Efficacy and course of actions on eliminating antibiotic resistance genes in agricultural soil. Journal of Hazardous Materials, 437, 129322.
- Liu, W. J., Jiang, H., & Yu, H. Q. (2015). Development of biochar-based functional materials: Toward a sustainable platform carbon material. Chemical Reviews, 115, 12251–12285.
- Liu, S., Xu, W. H., Liu, Y. G., Tan, X. F., Zeng, G. M., Li, X., Liang, J., Zhou, Z., Yan, Z. L., & Cai, X. X. (2017). Facile synthesis of Cu(II) impregnated biochar with enhanced adsorption activity for the removal of doxycycline hydrochloride from water. Science of the Total Environment, 592, 546–553.
- Lundstrom, S. V., Ostman, M., Bengtsson-Palme, J., Rutgersson, C., Thoudal, M., Sircar, T., Blanck, H., Eriksson, K. M., Tysklind, M., Flach, C. F., & Larsson, D. G. J. (2016). Minimal selective concentrations of tetracycline in complex aquatic bacterial biofilms. Science of the Total Environment, 553, 587–595.
- National Bureau of Statistics of China. (2021). China rural statistical yearbook. China Statistics Press.
- Oliveira, F. R., Patel, A. K., Jaisi, D. P., Adhikari, S., Lu, H., & Khanal, S. K. (2017). Environmental application of biochar: Current status and perspectives. Bioresource Technology, 246, 110–122.
- Peiris, C., Gunatilake, S. R., Mlsna, T. E., Mohan, D., & Vithanage, M. (2017). Biochar based removal of antibiotic sulfonamides and tetracyclines in aquatic environments: A critical review. Bioresource Technology, 246, 150–159.
- Peng, H., Gao, P., Chu, G., Pan, B., Peng, J., & Xing, B. (2017). Enhanced adsorption of Cu(II) and Cd(II) by phosphoric acid-modified biochars. Environmental Pollution, 229, 846–853.
- Rathnayake, D., Creber, H., Van Poucke, R., Sohi, S., Meers, E., Mašek, O., & Ronsse, F. (2021). Biochar from sawmill residues: Characterization and evaluation for its potential use in the horticultural growing media. Biochar, 3, 201–212.
- Shentu, J., Li, X., Han, R., Chen, Q., Shen, D., & Qi, S. (2022). Effect of site hydrological conditions and soil aggregate sizes on the stabilization of heavy metals (Cu, Ni, Pb, Zn) by biochar. Science of the Total Environment, 802, 149949.
- Sizmur, T., Fresno, T., Akgül, G., Frost, H., & Moreno-Jiménez, E. (2017). Biochar modification to enhance sorption of inorganics from water. Bioresource Technology, 246, 34–47.
- Sun, M., Ye, M., Jiao, W., Feng, Y., Yu, P., Liu, M., Jiao, J., He, X., Liu, K., Zhao, Y., Wu, J., Jiang, X., & Hu, F. (2018). Changes in tetracycline partitioning and bacteria/phage-comediated ARGs in microplastic-contaminated greenhouse soil facilitated by sophorolipid. Journal of Hazardous Materials, 345, 131–139.
- Taheran, M., Naghdi, M., Brar, S. K., Knystautas, E. J., Verma, M., Ramirez, A. A., Surampalli, R. Y., & Valero, J. R. (2016). Adsorption study of environmentally relevant concentrations of chlortetracycline on pinewood biochar. Science of the Total Environment, 571, 772–777.
- Tang, L., Yu, J., Pang, Y., Zeng, G. M., Deng, Y. C., Wang, J. J., Ren, X. Y., Ye, S. J., Peng, B., & Feng, H. P. (2018). Sustainable efficient adsorbent: Alkali-acid modified magnetic biochar derived from sewage sludge for aqueous organic contaminant removal. Chemical Engineering Journal, 336, 160–169.
- Tien, Y. C., Li, B., Zhang, T., Scott, A., Murray, R., Sabourin, L., Marti, R., & Topp, E. (2017). Impact of dairy manure pre-application treatment on manure composition, soil dynamics of antibiotic resistance genes, and abundance of antibiotic-resistance genes on vegetables at harvest. Science of the Total Environment, 581-582, 32–39.
- Uchimiya, M., Bannon, D. I., & Wartelle, L. H. (2012). Retention of heavy metals by carboxyl functional groups of biochars in small arms range soil. Journal of Agricultural and Food Chemistry, 60, 1798–1809.
- Urra, J., Alkorta, I., Lanzén, A., Mijangos, I., & Garbisu, C. (2019). The application of fresh and composted horse and chicken manure affects soil quality, microbial composition and antibiotic resistance. Applied Soil Ecology, 135, 73–84.
- Wang, Y., Li, X., Fu, Y., Chen, Y., Wang, Y., Ye, D., Wang, C., Hu, X., Zhou, L., Du, J., Shen, J., & Xia, X. (2020). Association of florfenicol residues with the abundance of oxazolidinone resistance genes in livestock manures. Journal of Hazardous Materials, 399, 123059.
- Wang, H., Yang, J., Yu, X., Zhao, G., Zhao, Q., Wang, N., Jiang, Y., Jiang, F., He, G., Chen, Y., Zhou, Z., & Jiang, Q. (2018). Exposure of adults to antibiotics in a Shanghai suburban area and health risk assessment: A biomonitoring-based study. Environmental Science & Technology, 52, 13942–13950.
- Xiong, J., Zhou, M., Qu, C., Yu, D., Chen, C., Wang, M., & Tan, W. (2021). Quantitative analysis of Pb adsorption on sulfhydryl-modified biochar. Biochar, 3, 37–49.
- Yan, J., Zuo, X., Yang, S., Chen, R., Cai, T., & Ding, D. (2022). Evaluation of potassium ferrate activated biochar for the simultaneous adsorption of copper and sulfadiazine: Competitive versus synergistic. Journal of Hazardous Materials, 424, 127435.
- Ye, M., Sun, M., Feng, Y., Wan, J., Xie, S., Tian, D., Zhao, Y., Wu, J., Hu, F., Li, H., & Jiang, X. (2016). Effect of biochar amendment on the control of soil sulfonamides, antibiotic-resistant bacteria, and gene enrichment in lettuce tissues. Journal of Hazardous Materials, 309, 219–227.
- Yue, Y., Shen, C., & Ge, Y. (2019). Biochar accelerates the removal of tetracyclines and their intermediates by altering soil properties. Journal of Hazardous Materials, 380, 120821.
- Zama, E. F., Zhu, Y. G., Reid, B. J., & Sun, G. X. (2017). The role of biochar properties in influencing the sorption and desorption of Pb(II), Cd(II) and As(III) in aqueous solution. Journal of Cleaner Production, 148, 127–136.
- Zeng, H., Zeng, H., Zhang, H., Shahab, A., Zhang, K., Lu, Y., Nabi, I., Naseem, F., & Ullah, H. (2021). Efficient adsorption of Cr (VI) from aqueous environments by phosphoric acid activated eucalyptus biochar. Journal of Cleaner Production, 286, 124964.
- Zhang, X., Gang, D. D., Zhang, J., Lei, X., Lian, Q., Holmes, W. E., Zappi, M. E., & Yao, H. (2022). Insight into the activation mechanisms of biochar by boric acid and its application for the removal of sulfamethoxazole. Journal of Hazardous Materials, 424, 127333.
- Zhang, J. H., Huang, B., Chen, L., Li, Y., Li, W., & Luo, Z. X. (2018). Characteristics of biochar produced from yak manure at different pyrolysis temperatures and its effects on the yield and growth of highland barley. Chemical Speciation & Bioavailability, 30, 57–67.
- Zhang, H., Wang, T., Sui, Z., Zhang, Y., Sun, B., & Pan, W. P. (2019). Enhanced mercury removal by transplanting sulfur-containing functional groups to biochar through plasma. Fuel, 253, 703–712.
- Zhang, Q., Ying, G., & Pan, C. (2015). A comprehensive evaluation of antibiotics emission and fate in the river basins of China: Source analysis, multimedia modelling, and linkage to bacterial resistance. Environmental Science & Technology, 49, 6772–6782.
- Zheng, J., Chen, T., & Chen, H. (2018). Antibiotic resistome promotion in drinking water during biological activated carbon treatment: Is it influenced by quorum sensing? Science of the Total Environment, 612, 1–8.
- Zhou, Y., Liu, X., Xiang, Y., Wang, P., Zhang, J., Zhang, F., Wei, J., Luo, L., Lei, M., & Tang, L. (2017). Modification of biochar derived from sawdust and its application in removal of tetracycline and copper from aqueous solution: Adsorption mechanism and modelling. Bioresource Technology, 245, 266–273.
- Zhu, X., Liu, Y., Qian, F., Zhou, C., Zhang, S., & Chen, J. (2014). Preparation of magnetic porous carbon from waste hydrochar by simultaneous activation and magnetization for tetracycline removal. Bioresource Technology, 154, 209–214.
- Zhu, S., Zhao, J., Zhao, N., Yang, X., Chen, C., & Shang, J. (2020). Goethite modified biochar as a multifunctional amendment for cationic Cd(II), anionic As(III), roxarsone, and phosphorus in soil and water. Journal of Cleaner Production, 247, 119579.
- Zuo, L., Ai, J., Fu, H., Chen, W., Zheng, S., Xu, Z., & Zhu, D. (2016). Enhanced removal of sulfonamide antibiotics by KOH-activated anthracite coal: Batch and fixed-bed studies. Environmental Pollution, 211, 425–434.
