Abstract
Purpose
The treated antibiotic fermentation residues free of antibiotics but containing a high level of nutrients might be used as organic fertilizers. However, their impact on the development of antibiotic resistance in the soil and plant tissue has not been explored.
Methods
In this study, the effects of thermally treated oxytetracycline fermentation residue (OFR) free of antibiotics on the dissemination of antibiotic resistance in the rhizosphere of spinach (Spinacia oleracea), changes in the rhizobacterial communities, and contamination of plant tissue were investigated in a pot experiment under greenhouse condition. Raw OFR, animal manure-based compost sourced from a commercial company, and untreated soil (control) were used as control. The experiment was conducted over a period of 2 months, and soil samples were collected at intervals of 15 days. Plant tissues were analyzed at harvest for the presence of tet genes and the concentration of antibiotics.
Results
The quantification of tet genes including tetA, tetL, tetQ, and tetX indicated that treated OFR did not significantly promote these genes over the control. The accumulation of antibiotics and tet genes in spinach tissues was not significantly different from the control (untreated soil), suggesting the potentiality of the treated OFR as an organic source for agricultural application.
Conclusion
The findings of this study indicated that hydrothermally treated OFR can be used as an organic fertilizer in agricultural applications without the promotion of antibiotic resistance in the soil and plant tissue.
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References
Anderson M, Habiger J (2012) Characterization and identification of productivity-associated rhizobacteria in wheat. Appl Environ Microbiol 78:4434–4446. https://doi.org/10.1128/AEM.07466-11
Awad M, Tian Z, Zhang Y et al (2020) Hydrothermal pretreatment of oxytetracycline fermentation residue: removal of oxytetracycline and increasing the potential for anaerobic digestion. Environmental Engineering Research. https://doi.org/10.4491/eer.2020.258
Azanu D, Mortey C, Darko G et al (2016) Uptake of antibiotics from irrigation water by plants. Chemosphere 157:107–114. https://doi.org/10.1016/j.chemosphere.2016.05.035
Bais HP, Weir TL, Perry LG et al (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. https://doi.org/10.1146/annurev.arplant.57.032905.105159
Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. https://doi.org/10.13140/2.1.1341.1520
Berlemont R, Martiny AC (2015) Genomic potential for polysaccharide deconstruction in bacteria. Appl Environ Microbiol 81:1513–1519. https://doi.org/10.1128/AEM.03718-14
Cai C, Liu H, Dai X, Whalen JK (2019) Multiple selection of resistance genes in arable soil amended with cephalosporin fermentation residue. Soil Biol Biochem 136:107538. https://doi.org/10.1016/j.soilbio.2019.107538
Carter LJ, Harris E, Williams M et al (2014) Fate and uptake of pharmaceuticals in soil–plant systems. J Agric Food Chem 62:816–825. https://doi.org/10.1021/jf404282y
Chee-Sanford JC, Mackie RI, Koike S et al (2009) Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J Environ Qual 38:1086–1108. https://doi.org/10.2134/jeq2008.0128
Chen Q-L, Cui H-L, Su J-Q et al (2019) Antibiotic resistomes in plant microbiomes. Trends Plant Sci 24:530–541. https://doi.org/10.1016/j.tplants.2019.02.010
Deng W, Wang Y, Liu Z et al (2014) HemI: a toolkit for illustrating heatmaps. PLoS One 9:e111988. https://doi.org/10.1371/journal.pone.0111988
Ding C, Pan J, Jin M et al (2016) Enhanced uptake of antibiotic resistance genes in the presence of nanoalumina. Nanotoxicology 10:1051–1060. https://doi.org/10.3109/17435390.2016.1161856
Du B, Yang Q, Wang R et al (2019) Evolution of antibiotic resistance and the relationship between the antibiotic resistance genes and microbial compositions under long-term exposure to tetracycline and sulfamethoxazole. IJERPH 16:4681. https://doi.org/10.3390/ijerph16234681
Gamalero E, Glick BR (2015) Bacterial modulation of plant ethylene levels. Plant Physiol 169:13–22. https://doi.org/10.1104/pp.15.00284
Gong P, Liu H, Wang M et al (2020) Characteristics of hydrothermal treatment for the disintegration of oxytetracycline fermentation residue and inactivation of residual antibiotics. Chem Eng J. https://doi.org/10.1016/j.cej.2020.126011
Gros M, Rodríguez-Mozaz S, Barceló D (2013) Rapid analysis of multiclass antibiotic residues and some of their metabolites in hospital, urban wastewater and river water by ultra-high-performance liquid chromatography coupled to quadrupole-linear ion trap tandem mass spectrometry. J Chromatogr A 1292:173–188. https://doi.org/10.1016/j.chroma.2012.12.072
Guo B, Gong L, Duan E et al (2012) Characteristics of penicillin bacterial residue. J Air Waste Manag Assoc 62:485–488. https://doi.org/10.1080/10962247.2012.658956
Guo H, Xue S, Nasir M et al (2018) Role of bentonite on the mobility of antibiotic resistance genes, and microbial community in oxytetracycline and cadmium contaminated soil. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.02722
Guo M-T, Yuan Q-B, Yang J (2015) Distinguishing effects of ultraviolet exposure and chlorination on the horizontal transfer of antibiotic resistance genes in municipal wastewater. Environ Sci Technol 49:5771–5778. https://doi.org/10.1021/acs.est.5b00644
Heuer H, Schmitt H, Smalla K (2011) Antibiotic resistance gene spread due to manure application on agricultural fields. Curr Opin Microbiol 14:236–243. https://doi.org/10.1016/j.mib.2011.04.009
Ismail BS, Farihah K, Khairiah J (2005) Bioaccumulation of heavy metals in vegetables from selected agricultural areas. Bull Environ Contam Toxicol 74:320–327. https://doi.org/10.1007/s00128-004-0587-6
Karkman A, Pärnänen K, Larsson DGJ (2019) Fecal pollution can explain antibiotic resistance gene abundances in anthropogenically impacted environments. Nat Commun 10:80. https://doi.org/10.1038/s41467-018-07992-3
Li C, Zhang G, Zhang Z et al (2015) Hydrothermal pretreatment for biogas production from anaerobic digestion of antibiotic mycelial residue. Chem Eng J 279:530–537. https://doi.org/10.1016/j.cej.2015.05.073
Li D, Yu T, Zhang Y et al (2010) Antibiotic resistance characteristics of environmental bacteria from an oxytetracycline production wastewater treatment plant and the receiving river. Appl Environ Microbiol 76:3444–3451. https://doi.org/10.1128/AEM.02964-09
Li Z, Tian B, Zuo J, Yu X, Shen H, Wang Y, Zhao X (2012) Progress in treatment and disposal technology of antibiotic bacterial residues. Environ Eng 30:72–75
Liao H, Zhao Q, Cui P et al (2019) Efficient reduction of antibiotic residues and associated resistance genes in tylosin antibiotic fermentation waste using hyperthermophilic composting. Environ Int 133:105203. https://doi.org/10.1016/j.envint.2019.105203
Liu M, Zhang Y, Yang M et al (2012) Abundance and distribution of tetracycline resistance genes and mobile elements in an oxytetracycline production wastewater treatment system. Environ Sci Technol 46:7551–7557. https://doi.org/10.1021/es301145m
Ma D, Zhang G, Zhao P et al (2015) Hydrothermal treatment of antibiotic mycelial dreg: more understanding from fuel characteristics. Chem Eng J 273:147–155. https://doi.org/10.1016/j.cej.2015.01.041
Marti R, Scott A, Tien Y-C et al (2013) Impact of manure fertilization on the abundance of antibiotic-resistant bacteria and frequency of detection of antibiotic resistance genes in soil and on vegetables at harvest. Appl Environ Microbiol 79:5701–5709. https://doi.org/10.1128/AEM.01682-13
Micallef SA, Shiaris MP, Colón-Carmona A (2009) Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J Exp Bot 60:1729–1742. https://doi.org/10.1093/jxb/erp053
Ministry of Environmental Protection (MEP), PRC, No. 2008–81.Discharge standard of water pollutants for pharmaceutical industry—chemical synthesis products.category. http://kjs.mep.gov.cn/hjbhbz/bzwb/shjbh/swrwpfbz/200807/t20080701_124700.htm
Mishra M, Arukha AP, Patel AK et al (2018) Multi-drug resistant coliform: water sanitary standards and health hazards. Front Pharmacol 9:311. https://doi.org/10.3389/fphar.2018.00311
Muhammad J, Khan S, Su JQ et al (2020) Antibiotics in poultry manure and their associated health issues: a systematic review. J Soils Sediments 20:486–497. https://doi.org/10.1007/s11368-019-02360-0
Nesme J, Simonet P (2015) The soil resistome: a critical review on antibiotic resistance origins, ecology and dissemination potential in telluric bacteria. Environ Microbiol 17(4):913–930. https://doi.org/10.1111/1462-2920.12631
Pei J, Yao H, Wang H et al (2016) Comparison of ozone and thermal hydrolysis combined with anaerobic digestion for municipal and pharmaceutical waste sludge with tetracycline resistance genes. Water Res. https://doi.org/10.1016/j.watres.2016.04.058
Pérez-Jaramillo JE, Carrión VJ, de Hollander M, Raaijmakers JM (2018) The wild side of plant microbiomes. Microbiome 6:143. https://doi.org/10.1186/s40168-018-0519-z
Qiu Z, Yu Y, Chen Z et al (2012) Nanoalumina promotes the horizontal transfer of multiresistance genes mediated by plasmids across genera. Proc Natl Acad Sci 109:4944–4949. https://doi.org/10.1073/pnas.1107254109
Roberts JL, Moreau R (2016) Functional properties of spinach (Spinacia oleracea L.) phytochemicals and bioactives. Food Funct 7:3337–3353. https://doi.org/10.1039/C6FO00051G
Seiler C, Berendonk TU (2012) Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbio 3. https://doi.org/10.3389/fmicb.2012.00399
Shen Y, Zhuan R, Chu L et al (2019) Inactivation of antibiotic resistance genes in antibiotic fermentation residues by ionizing radiation: exploring the development of recycling economy in antibiotic pharmaceutical factory. Waste Manage 84:141–146. https://doi.org/10.1016/j.wasman.2018.11.039
Szekeres E, Baricz A, Chiriac CM et al (2017) Abundance of antibiotics, antibiotic resistance genes and bacterial community composition in wastewater effluents from different Romanian hospitals. Environ Pollut 225:304–315. https://doi.org/10.1016/j.envpol.2017.01.054
Thomas F, Hehemann J-H, Rebuffet E et al (2011) Environmental and gut Bacteroidetes: the food connection. Front Microbio 2. https://doi.org/10.3389/fmicb.2011.00093
Tian Z, Zhang Y, Yu B, Yang M (2016) Changes of resistome, mobilome and potential hosts of antibiotic resistance genes during the transformation of anaerobic digestion from mesophilic to thermophilic. Water Res 98:261–269. https://doi.org/10.1016/j.watres.2016.04.031
Vacheron J, Desbrosses G, Bouffaud M-L et al (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4. https://doi.org/10.3389/fpls.2013.00356
van Elsas JD, Turner S, Bailey MJ (2003) Horizontal gene transfer in the phytosphere. New Phytol 157:525–537. https://doi.org/10.1046/j.1469-8137.2003.00697.x
Van Hoek AH, Mevius D, Guerra B, Mullany P, Roberts AP, Aarts HJ (2011) Acquired antibiotic resistance genes: an overview. Frontiers in microbiology. Front Microbio 2. https://doi.org/10.3389/fmicb.2011.00203
Wan Y, Bao Y, Zhou Q (2010) Simultaneous adsorption and desorption of cadmium and tetracycline on cinnamon soil. Chemosphere 80:807–812. https://doi.org/10.1016/j.chemosphere.2010.04.066
Wang R, Liu TZ, Wang T (2006) The fate of antibiotics in environment and its ecotoxicology: a review. Acta Ecol Sin 26:265–270
Wester AL, Gopinathan U, Gjefle K, Solberg SØ, Røttingen J-A (2017) Antimicrobial resistance in a one health and one world perspective – mechanisms and solutions. International Encyclopedia of Public Health 140–153. https://doi.org/10.1016/b978-0-12-803678-5.00022-9
Xiong J, Liu Y, Lin X et al (2012) Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau: bacterial biogeography in alkaline sediments. Environ Microbiol 14:2457–2466. https://doi.org/10.1111/j.1462-2920.2012.02799.x
Xue G, Diao R, Jiang M et al (2021) Significant effect of pH on tetracycline resistance genes reduction during sludge thermal hydrolysis treatment. Waste Manage. https://doi.org/10.1016/j.wasman.2021.01.019
Yang J-F, Ying G-G, Zhao J-L et al (2010) Simultaneous determination of four classes of antibiotics in sediments of the Pearl Rivers using RRLC–MS/MS. Sci Total Environ 408:3424–3432. https://doi.org/10.1016/j.scitotenv.2010.03.049
Yang L, Zhang S, Chen Z et al (2016) Maturity and security assessment of pilot-scale aerobic co-composting of penicillin fermentation dregs (PFDs) with sewage sludge. Biores Technol 204:185–191. https://doi.org/10.1016/j.biortech.2016.01.004
Yin X, Jiang X, Chai B et al (2018) ARGs-OAP v2.0 with an expanded SARG database and hidden Markov models for enhancement characterization and quantification of antibiotic resistance genes in environmental metagenomes. Bioinformatics 34:2263–2270
Zhang B, Wang MM, Wang B et al (2018) The effects of bio-available copper on macrolide antibiotic resistance genes and mobile elements during tylosin fermentation dregs co-composting. Biores Technol 251:230–237. https://doi.org/10.1016/j.biortech.2017.12.051
Zhang G, Ma D, Peng C et al (2014) Process characteristics of hydrothermal treatment of antibiotic residue for solid biofuel. Chem Eng J 252:230–238. https://doi.org/10.1016/j.cej.2014.04.092
Zhang M, Meng J, Liu Q et al (2019a) Corn stover–derived biochar for efficient adsorption of oxytetracycline from wastewater. J Mater Res. https://doi.org/10.1557/jmr.2019.198
Zhang Y-J, Hu H-W, Chen Q-L et al (2019b) Transfer of antibiotic resistance from manure-amended soils to vegetable microbiomes. Environ Int 130:104912. https://doi.org/10.1016/j.envint.2019.104912
Zhong W, Li Z, Yang J et al (2014) Effect of thermal–alkaline pretreatment on the anaerobic digestion of streptomycin bacterial residues for methane production. Biores Technol 151:436–440. https://doi.org/10.1016/j.biortech.2013.10.100
Zhu Y-G, Johnson TA, Su JQ et al (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1222743110
Acknowledgements
We thank Prof. Xiaomin Dou from the Beijing Forestry University for providing the greenhouse. This study was supported by the National Natural Scientific Foundation of China (No. 51978645) and the Project of International Cooperation and Exchanges NSFC (No. 31861143049).
Funding
National Natural Science Foundation of China, 51978645, Zhe Tian, 31861143049, Min Yang
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Awad, M., Tian, Z., Han, Z. et al. Application of the hydrothermally treated oxytetracycline fermentation residue in agriculture: concentrations of antibiotic and resistance genes in soil and plant. J Soils Sediments 22, 1095–1104 (2022). https://doi.org/10.1007/s11368-021-03123-6
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DOI: https://doi.org/10.1007/s11368-021-03123-6