Abstract
Residual antibiotics (ABs) and heavy metals (HMs) are continuously released from soil, reflecting their intensive use and contamination of water and soil, posing an environmental problem of great concern. Relatively few studies exist of the functional diversity of soil microorganisms under the combined action of ABs and HMs. To address this deficiency, BIOLOG ECO microplates and the Integrated Biological Responses version 2 (IBRv2) method were used to comprehensively explore the effects of single and combined actions of copper (Cu) and enrofloxacin (ENR), oxytetracycline (OTC), and sulfadimidine (SM2) on the soil microbial community. The results showed that the high concentration (0.80 mmol/kg) compound group had a significant effect on average well color development (AWCD) and OTC showed a dose–response relationship. The results of IBRv2 analysis showed that the single treatment group of ENR or SM2 had a significant effect on soil microbial communities, and the IBRv2 of E1 was 5.432. Microbes under ENR, SM2, and Cu stress had more types of available carbon sources, and all treatment groups were significantly more enriched with microorganisms having D-mannitol and L-asparagine as carbon sources. This study confirms that the combined effects of ABs and HMs can inhibit or promote the function of soil microbial communities. In addition, this paper will provide new insights into IBRv2 as an effective method to evaluate the impacts of contaminants on soil health.
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References
Aarestrup, F. M. (2015). The livestock reservoir for antimicrobial resistance: A personal view on changing patterns of risks, effects of interventions and the way forward. Philosophical Transactions of the Royal Society B: Biological Sciences., 370, 20140085. https://doi.org/10.1098/rstb.2014.0085
Allen, H. K., Donato, J., Wang, H. H., Cloud-Hansen, K. A., Davies, J., & Handelsman, J. (2010). Call of the wild: Antibiotic resistance genes in natural environments. Nature Reviews. Microbiology, 8, 251–259. https://doi.org/10.1038/nrmicro2312
Antoniadis, V., Levizou, E., Shaheen, S. M., Ok, Y. S., Sebastian, A., Baum, C., Prasad, M. N. V., Wenzel, W. W., & Rinklebe, J. (2017). Trace elements in the soil-plant interface: Phytoavailability, translocation, and phytoremediatione-A review. Earth-Science Reviews, 171, 621–645. https://doi.org/10.1016/j.earscirev.2017.06.005
Auerbach, E. A., Seyfried, E. E., & McMahon, K. D. (2006). Tetracycline resistance genes in activated sludge wastewater treatment plants. Proceeding of the Water Environment Federation, 12, 1478–1493. https://doi.org/10.2175/193864706783749495
Beaber, J. W., Hochhut, B., & Waldor, M. K. (2004). SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature, 427(6969), 72–74.
Beliaeff, B., & Burgeot, T. (2002). Integrated biomarker response: A useful tool for ecological risk assessment. Environmental Toxicology and Chemistry, 21, 1316–1322.
Berendsen, R. L., Pieterse, C. M. J., & Bakker, P. A. H. M. (2012). The rhizosphere microbiome and plant health. Trends in Plant Science, 17(8), 478–486. https://doi.org/10.1016/j.tplants.2012.04.001
Carvalho, I. T., & Santos, L. (2016). Antibiotics in the aquatic environments: A review of the European scenario. Environment International, 94, 736–757. https://doi.org/10.1016/j.envint.2016.06.025
Chao, H. Z., Zheng, X. X., Xia, R., Sun, M. M., & Feng, H. (2021). Incubation trial indicated the earthworm intestinal bacteria as promising biodigestor for mitigating tetracycline resistance risk in anthropogenic disturbed forest soil. Science of The Total Environment, 798(9), 149337. https://doi.org/10.1016/j.scitotenv.2021.149337
Chen, S. X., Wang, J., Feng, H. J., Shen, D. S., He, S. C., & Xu, Y. F. (2020). Quantitative study on the fate of antibiotic emissions in China. Environmental Geochemistry and Health, 42(10), 3471–3479. https://doi.org/10.1007/s10653-020-00563-w
Chen, W. R., & Huang, C. H. (2009). Transformation of tetracyclines mediated by Mn(II) and Cu(II) ions in the presence of oxygen. Environmental Science and Technology, 43(2), 401–407. https://doi.org/10.1021/es802295r
Choi, K. H., & Dobbs, F. C. (1999). Comparison of two kinds of biolog microplates (GEN and ECO) in their ability to distinguish among aquatic microbial communities. Journal of Microbiology Methods, 36, 203–213. https://doi.org/10.1016/S0167-7012(99)00034-2
Dala-Paula, B. M., Custodio, F. B., Knupp, E. A. N., Palmieri, H. E. L., Silva, J. B. B., & Glória, M. B. A. (2018). Cadmium, copper and lead levels in different cultivars of lettuce and soil from urban agriculture. Environmental Pollution, 242, 383–389. https://doi.org/10.1016/j.envpol.2018.04.101
de Souza, M. J. M., Kogawa, A. C., & Salgado, H. R. N. (2019). New and miniaturized method for analysis of enrofloxacin in palatable tablets. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, 209, 1–7. https://doi.org/10.1016/j.saa.2018.10.014
Egli, M., Sartori, G., Mirabella, A., Giaccai, D., Favilli, F., Scherrer, D., Krebs, R., & Delbos, E. (2010). The influence of weathering and organic matter on heavy metals lability in silicatic, Alpine soils. Science of the Total Environment, 408(4), 931–946. https://doi.org/10.1016/j.scitotenv.2009.10.005
Fall, D., Diouf, D., Zoubeirou, A. M., Bakhoum, N., Faye, A., & Sall, S. N. (2012). Effect of distance and depth on microbial biomass and mineral nitrogen content under Acacia senegal (L.) Willd. trees. Journal of Environmental Management, 95, S260–S264. https://doi.org/10.1016/j.jenvman.2011.03.038
Feigl, V., Ujaczki, É., Vaszita, E., & Molnár, M. (2017). Influence of red mud on soil microbial communities: Application and comprehensive evaluation of the Biolog EcoPlate approach as a tool in soil microbiological studies. Science of the Total Environment, 595, 903–911. https://doi.org/10.1016/j.scitotenv.2017.03.266
Gao, M. L., Song, W. H., Zhou, Q., Ma, X. J., & Chen, X. Y. (2013). Interactive effect of oxytetracycline and lead on soil enzymatic activity and microbial biomass. Environmental Toxicology and Pharmacology, 36, 667–674. https://doi.org/10.1016/j.etap.2013.07.003
Ge, Z. W., Du, H. J., Gao, Y. L., & Qiu, W. F. (2018). Analysis on metabolic functions of stored rice microbial communities by BIOLOG ECO microplates. Frontiers in Microbiology, 9, 1375. https://doi.org/10.3389/fmicb.2018.01375
Ghirardini, A., & Verlicchi, P. (2019). A review of selected microcontaminants and microorganisms in land runoff and tile drainage in treated sludge-amended soils. Science of the Total Environment, 655, 939–957. https://doi.org/10.1016/j.scitotenv.2018.11.249
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. The ISME Journal, 9, 1269–1279. https://doi.org/10.1038/ismej.2014.226
Grass, G., Rensing, C., & Solioz, M. (2011). Metallic copper as an antimicrobial surface. Applied and Environmental Microbiology, 77, 1541–1547. https://doi.org/10.1128/aem.02766-10
Gryta, A., Frąc, M., & Oszust, K. (2014). The application of the Biolog EcoPlate approach in ecotoxicological evaluation of dairy sewage sludge. Applied Biochemistry and Biotechnology, 174, 1434–1443. https://doi.org/10.1007/s12010-014-1131-8
Guo, T., Lou, C. L., Zhai, W. W., Tang, X. J., Hashmi, M. Z., Murtaza, R., Li, Y., Liu, X. M., & Xu, J. M. (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. https://doi.org/10.1016/j.scitotenv.2018.04.194
He, X. L., Xu, Y. B., Chen, J. L., Ling, J. Y., Li, Y. F., Huang, L., Zhou, X., Zheng, L., & Xie, G. (2017). Evolution of corresponding resistance genes in the water of fish tanks with multiple stresses of antibiotics and heavy metals. Water Research, 124, 39–48. https://doi.org/10.1016/j.watres.2017.07.048
Hernández, A. F., Parrón, T., Tsatsakis, A. M., Requena, M., Alarcón, R., & López-Guarnido, O. (2013). Toxic effects of pesticide mixtures at a molecular level: Their relevance to human health. Toxicology, 307, 136–145. https://doi.org/10.1016/j.tox.2012.06.009
Hooban, B., Fitzhenry, K., O’Connor, L., Miliotis, G., Joyce, A., Chueiri, A., Farrell, M. L., Delappe, N., Tuohy, A., Cormican, M., & Morris, D. (2022). A longitudinal survey of antibiotic-resistant enterobacterales in the Irish environment, 2019–2020. Science of the Total Environment, 828, 154488. https://doi.org/10.1016/j.scitotenv.2022.154488
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(9), 2992–2998. https://doi.org/10.1016/j.envpol.2010.05.023
Huang, B. C., Long, J., Li, J., & Ai, Y. W. (2021). Effects of antimony contamination on bioaccumulation and gut bacterial community of earthworm Eisenia fetida. Journal of Hazardous Materials, 416(24), 126110. https://doi.org/10.1016/j.jhazmat.2021.126110
Huang, F. Y., An, Z. Y., Moran, M. J., & Liu, G. (2020). Recognition of typical antibiotic residues in environmental media related to groundwater in China (2009–2019). Journal of Hazardous Materials, 399, 122813. https://doi.org/10.1016/j.jhazmat.2020.122813
Jia, D. A., Zhou, D. M., Wang, Y. J., Zhu, H. W., & Chen, J. L. (2008). Adsorption and cosorption of Cu(II) and tetracycline on two soils with different characteristics. Geoderma, 146, 224–230. https://doi.org/10.1016/j.geoderma.2008.05.023
Jonker, M. J., Svendsen, C., Bedaux, J. J. M., Bongers, M., & Kammenga, J. E. (2005). Significance testing of synergistic/antagonistic, dose level-dependent, or dose ratio-dependent effects in mixture dose-response analysis. Environmental Toxicology and Chemistry, 24(10), 2701–2713. https://doi.org/10.1897/04-431r.1
Khan, Z. I., Ahmad, K., Rehman, S., Siddique, S., Bashir, H., Zafar, A., Sohail, M., Ali, S. A., Cazzato, E., & Mastro, G. D. (2017). Health risk assessment of heavy metals in wheat using different water qualities: Implication for human health. Environmental Science and Pollution Research, 24(1), 947–955. https://doi.org/10.1007/s11356-016-7865-9
Kumar, U., Shahid, M., Tripathi, R., Mohanty, S., Kumar, A., Bhattacharyya, P., Lal, B., Gautam, P., Raja, R., Panda, B. B., Jambhulkar, N. N., Shukla, A. K., & Jambhulkar, N. N. (2017). Variation of functional diversity of soil microbial community in sub-humid tropical rice-rice cropping system under long-term organic and inorganic fertilization. Ecological Indicators, 73, 536–543. https://doi.org/10.1016/j.ecolind.2016.10.014
Kümmerer, K. (2009). Antibiotics in the aquatic environment-A review-part I. Chemosphere, 75(4), 417–434.
Li, C., Liu, X., Meng, M. J., Zhai, L., Zhang, B., Jia, Z. H., Gu, Z. Y., Liu, Q. Q., Zhang, Y. L., & Zhang, J. C. (2021). The use of Biolog Eco microplates to compare the effects of sulfuric and nitric acid rain on the metabolic functions of soil microbial communities in a subtropical plantation within the Yangtze River Delta region. CATENA, 198, 105039. https://doi.org/10.1016/j.catena.2020.105039
Li, J., Zheng, T. T., Yuan, D., Gao, C. Z., & Liu, C. G. (2020). Probing the single and combined toxicity of PFOS and Cr(VI) to soil bacteria and the interaction mechanisms. Chemosphere, 249, 126039. https://doi.org/10.1016/j.chemosphere.2020.126039
Li, N., Kang, Y., Pan, W. J., Zeng, L. X., Zhang, Q. Y., & Luo, J. W. (2015). Concentration and transportation of heavy metals in vegetables and risk assessment of human exposure to bioaccessible heavy metals in soil near a waste-incinerator site, South China. Science of the Total Environment, 521–522, 144–151. https://doi.org/10.1016/j.scitotenv.2015.03.081
Li, S. G., Lv, T. X., Zhang, X. X., Gu, G. G., & Niu, Y. C. (2013). Effect of Trichoderma longbrachiatum T2 on functional diversity of cucumber rhizomicrobes. Journal of Environmental Biology, 34, 293–299.
Li, X. N., Qu, C. S., Bian, Y. R., Gu, C. G., Jiang, X., & Song, Y. (2019). New insights into the responses of soil microorganisms to polycyclic aromatic hydrocarbon stress by combining enzyme activity and sequencing analysis with metabolomics. Environmental Pollution, 255, 113312. https://doi.org/10.1016/j.envpol.2019.113312
Li, Y. S., Tang, H., Hu, Y. X., Wang, X. H., Ai, X. J., Tang, L., Matthew, C., Cavanagh, J., & Qiu, J. P. (2016). Enrofloxacin at environmentally relevant concentrations enhances uptake and toxicity of cadmium in the earthworm Eisenia fetida in farm soils. Journal of Hazardous Materials, 308, 312–320. https://doi.org/10.1016/j.jhazmat.2016.01.057
Lin, H., Jiang, L. T., Li, B., Dong, Y. B., He, Y. H., & Qiu, Y. (2019). Screening and evaluation of heavy metals facilitating antibiotic resistance gene transfer in a sludge bacterial community. Science of The Total Environment, 695, 133862. https://doi.org/10.1016/j.scitotenv.2019.133862
Liu, H. L., Li, M., Zhou, J., Zhou, D. M., & Wang, Y. J. (2018). Effects of soil properties and aging process on the acute toxicity of cadmium to earthworm Eisenia fetida. Environmental Science and Pollution Research, 25, 3708–3717. https://doi.org/10.1007/s11356-017-0739-y
Liu, M., Liu, J., Jiang, C. Y., Wu, M., Song, R. S., Gui, R. Y., Jia, J. X., & Li, Z. P. (2017). Improved nutrient status affects soil microbial biomass, respiration, and functional diversity in a Lei bamboo plantation under intensive management. Journal of Soil & Sediments, 17, 917–926. https://doi.org/10.1007/s11368-016-1603-2
Liu, Z. F., Fu, B. J., Zheng, X. X., & Liu, G. H. (2010). Plant biomass, soil water content and soil N: P ratio regulating soil microbial functional diversity in a temperate steppe: A regional scale study. Soil Biology and Biochemistry, 42, 445–450. https://doi.org/10.1016/j.soilbio.2009.11.027
Ma, J., Zhu, D., Chen, Q. L., Ding, J., Zhu, Y. G., Sheng, G. D., & Qiu, Y. P. (2019). Exposure to tetracycline perturbs the microbiome of soil oligochaete Enchytraeus crypticus. Science of the Total Environment, 654, 643–650. https://doi.org/10.1016/j.scitotenv.2018.11.154
Ma, Y. P., Li, M., Wu, M. M., Li, Z., & Liu, X. (2015). Occurrences and regional distributions of 20 antibiotics in water bodies during groundwater recharge. Science of the Total Environment, 518–519, 498–506. https://doi.org/10.1016/j.scitotenv.2015.02.100
Min, X. B., Wang, Y. Y., Chai, L. Y., Yang, Z. H., & Liao, Q. (2017). High-resolution analyses reveal structural diversity patterns of microbial communities in Chromite Ore Processing Residue (COPR) contaminated soils. Chemosphere, 183, 266–276. https://doi.org/10.1016/j.chemosphere.2017.05.105
O'Neill, J. (2016). The review on antimicrobial resistance. Tacking Drug-Resistant Infections Globally: Final Report and Recommendations.
Pan, M., & Chu, L. M. (2017). Occurrence of antibiotics and antibiotic resistance genes in soils from wastewater irrigation areas in the Pearl River Delta region, southern China. Science of the Total Environment., 624, 145–152.
Passos, L. S., Gnocchi, K. G., Pereira, T. M., Coppo, G. C., Cabral, D. S., & Gomes, L. C. (2020). Is the Doce River elutriate or its water toxic to Astyanax lacustris (Teleostei: Characidae) three years after the Samarco mining dam collapse? Science of The Total Environment, 736, 139644. https://doi.org/10.1016/j.scitotenv.2020.139644
Pei, Z. G., Yang, S., Li, L. Y., Li, C. M., Zhang, S. Z., Shan, X. Q., Wen, B., & Guo, B. Y. (2014). Effects of copper and aluminum on the adsorption of sulfathiazole and tylosin on peat and soil. Environmental Pollution, 184, 579–585. https://doi.org/10.1016/j.envpol.2013.09.038
Poole, K. (2017). At the Nexus of antibiotics and metals: The impact of Cu and Zn on antibiotic activity and resistance. Trends in Microbiology, 25, 820–832. https://doi.org/10.1016/j.tim.2017.04.010
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, 35–46. https://doi.org/10.1136/bmj.o1551
Ruma, K., Shefali, B., & Hariprasad, P. (2019). Convergent evolution in bacteria from multiple origins under antibiotic and heavy metal stress, and endophytic conditions of host plant. Science of the Total Environment, 650, 858–867. https://doi.org/10.1016/j.scitotenv.2018.09.078
Sala, M. M., Arrieta, J. M., Boras, J. A., Duarte, C. M., & Vaque, D. (2010). The impact of ice melting on bacterioplankton in the Arctic Ocean. Polar Biology, 33, 1683–1694. https://doi.org/10.1007/s00300-010-0808-x
Sanchez, W., Burgeot, T., & Porcher, J. M. (2013). A novel “Integrated Biomarker Response” calculation based on reference deviation concept. Environmental Science and Pollution Research, 20, 2721–2725. https://doi.org/10.1007/s11356-012-1359-1
Schathauser, B. H., Kristofco, L. A., Ribas de Oliveira, C. M., & Brooks, B. W. (2018). Global review and analysis of erythromycin in the environment: Occurrence, bioaccumulation and antibiotic resistance hazards. Environmental Pollution, 238, 440–451. https://doi.org/10.1016/j.envpol.2018.03.052
Serafim, A., Company, R., Lopes, B., Fonseca, V. F., França, S., Vasconcelos, R. P., Bebianno, M. J., & Cabral, H. N. (2012). Application of an integrated biomarker response index (IBR) to assess temporal variation of environmental quality in two Portuguese aquatic systems. Ecological Indicators, 19, 215–225. https://doi.org/10.1016/j.ecolind.2011.08.009
Shahid, M., Dumat, C., Khalid, S., Schreck, E., Xiong, T. T., & Niazi, N. K. (2017). Foliar heavy metal uptake, toxicity and detoxification in plants: A comparison of foliar and root metal uptake. Journal of Hazardous Materials, 325, 36–58. https://doi.org/10.1016/j.jhazmat.2016.11.063
Shawver, S., Wepking, C., Ishii, S., Strickland, M. S., & Badgley, B. D. (2021). Application of manure from cattle administered antibiotics has sustained multi-year impacts on soil resistome and microbial community structure. Soil Biology and Biochemistry, 157, 108252. https://doi.org/10.1016/j.soilbio.2021.108252
Shen, Y. K., Ryser, E. T., Li, H., & Zhang, W. (2021). Bacterial community assembly and antibiotic resistance genes in the lettuce-soil system upon antibiotic exposure. Science of The Total Environment, 778, 146255. https://doi.org/10.1016/j.scitotenv.2021.146255
Shrestha, P., Gautam, R., & Ashwath, N. (2019). Effects of agronomic treatments on functional diversity of soil microbial community and microbial activity in a revegetated coal mine spoil. Geoderma, 338, 40–47. https://doi.org/10.1016/j.geoderma.2018.11.038
Singh, R., Singh, A. P., Kumar, S., Giri, B. S., & Kim, K. H. (2019). Antibiotic resistance in major rivers in the world: A systematic review on occurrence, emergence and management strategies. Journal of Cleaner Production, 234, 1484–1505. https://doi.org/10.1016/j.jclepro.2019.06.243
Song, J. X., Rensing, C., Holm, P. E., Virta, M., & Brandt, K. K. (2017). Comparison of metals and tetracycline as selective agents for development of tetracycline resistant bacterial communities in agricultural soil. Environmental Science and Technology, 51, 3040–3047. https://doi.org/10.1021/acs.est.6b05342
Su, Y. H., Zhu, Y. G., Lin, A. J., & Zhang, X. H. (2005). Interaction between cadmium and atrazine during uptake by rice seedlings (Oryza sativa L.). Chemosphere, 60(6), 802–809. https://doi.org/10.1016/j.chemosphere.2005.04.022
Sui, Q., Zhang, J., Chen, M., Wang, R., Wang, Y., & Wei, Y. (2019). Fate of microbial pollutants and evolution of antibiotic resistance in three types of soil amended with swine slurry. Environmental Pollution, 245, 353–362. https://doi.org/10.1016/j.envpol.2018.11.003
Tan, H. H., Cao, Y. S., Tang, T., Qian, K., Chen, W. L., & Li, J. Q. (2008). Biodegradation and chiral stability of fipronil in aerobic and flooded paddy soils. Science of the Total Environment, 407, 428–437. https://doi.org/10.1016/j.scitotenv.2008.08.007
Tang, J. Y., Zhang, J. C., Ren, L. H., Zhou, Y. Y., Gao, J., Luo, L., Yang, Y., Peng, Q. H., Huang, H. L., & Chen, A. W. (2019). Diagnosis of soil contamination using microbiological indices: A review on heavy metal pollution. Journal of Environmental Management, 242, 121–130. https://doi.org/10.1016/j.jenvman.2019.04.061
Tribedi, P., Gupta, A. D., & Sil, A. K. (2015). Adaptation of Pseudomonas sp. AKS2 in biofilm on low-density polyethylene surface: An effective strategy for efficient survival and polymer degradation. Bioresources and Bioprocessing, 2, 14. https://doi.org/10.1186/s40643-015-0044-x
Turner, S., Mikutta, R., Meyer-Stüve, S., Guggenberger, G., Schaarschmidt, F., Lazar, C. S., Dohrmann, R., & Schippers, A. (2017). Microbial community dynamics in soil depth profiles over 120,000 years of ecosystem development. Frontiers in Microbiology, 8, 874. https://doi.org/10.3389/fmicb.2017.00874
Uwizeyimana, H., Wang, M., Chen, W., & Khan, K. (2017). The eco-toxic effects of pesticide and heavy metal mixtures towards earthworms in soil. Environmental Toxicology and Pharmacology, 55, 20–29. https://doi.org/10.1016/j.etap.2017.08.001
Wang, J. H., Zhu, L. S., Meng, Y., Wang, J., Xie, H., & Zhang, Q. M. (2012). The combined stress effects of atrazine and cadmium on the earthworm Eisenia fetida. Environmental Toxicology and Chemistry, 31, 2035–2040. https://doi.org/10.1002/etc.1907
Wang, L. J., Wang, J. H., Zhu, L. S., & Wang, J. (2018). Toxic effects of oxytetracycline and copper, separately or combined, on soil microbial biomasses. Environmental Geochemistry and Health, 40(2), 763–776. https://doi.org/10.1007/s10653-017-0022-7
Wang, L. J., Xia, X. M., Zhang, W. J., Wang, J. H., Zhu, L. S., Wang, J., Wei, Z. Y., & Ahmad, Z. (2019a). Separate and joint eco-toxicological effects of sulfadimidine and copper on soil microbial biomasses and ammoxidation microorganisms abundances. Chemosphere, 228, 556–564. https://doi.org/10.1016/j.chemosphere.2019.04.165
Wang, L. J., Wang, J. H., Wang, J., Zhu, L. S., 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. https://doi.org/10.1016/j.jhazmat.2020.122334
Wang, S. Q., Li, T. X., Zheng, Z. C., & Chen, H. Y. H. (2019b). Soil aggregate-associated bacterial metabolic activity and community structure in different aged tea plantations. Science of the Total Environment, 654, 1023–1032. https://doi.org/10.1016/j.scitotenv.2018.11.032
Wang, T., Zhang, J., Tao, M. T., Xu, C. M., & Chen, M. (2021). Quantitative characterization of toxicity interaction within antibiotic-heavy metal mixtures on Chlorella pyrenoidosa by a novel area-concentration ratio method. Science of The Total Environment, 762, 144180. https://doi.org/10.1016/j.scitotenv.2020.144180
Wang, X. M., Lan, B. R., Fei, H. X., Wang, S. Y., & Zhu, G. B. (2021). Heavy metal could drive co-selection of antibiotic resistance in terrestrial subsurface soils. Journal of Hazardous Materials, 411, 124848. https://doi.org/10.1016/j.jhazmat.2020.124848
Wei, Z. Y., Wang, J. H., Zhu, L. S., Wang, J., & Zhu, G. D. (2018). Toxicity of enrofloxacin, copper and their interactions on soil microbial populations and ammonia-oxidizing archaea and bacteria. Scientific Reports, 8(1), 5828. https://doi.org/10.1038/s41598-018-24016-8
Wu, M. H., Que, C. J., Tang, L., Xu, H., Xiang, J. J., Wang, J. J., Shi, W. Y., & Xu, G. (2016a). Distribution, fate, and risk assessment of antibiotics in five wastewater treatment plants in Shanghai. China. Environmental Science and Pollution Research, 23(18), 18055–18063. https://doi.org/10.1007/s11356-016-6946-0
Wu, X. Q., Xue, Q., Xiang, Y., Ding, X. L., Xu, X., & Ye, J. (2016b). Community and functional diversity of bacteria associated with propagative and dispersal forms of Bursaphelenchus xylophilus. Nematology, 18(10), 1185–1198. https://doi.org/10.1163/15685411-00003024
Yang, R., Xia, X. M., Wang, J. H., Zhu, L. S., Wang, J., Ahmad, Z., Yang, L. L., Mao, S. S., & Chen, Y. Y. (2020). Dose and time-dependent response of single and combined artificial contamination of sulfamethazine and copper on soil enzymatic activities. Chemosphere, 250, 126161. https://doi.org/10.1016/j.chemosphere.2020.126161
Yang, Y. J., Li, C. X., Li, J., Schneider, R., & Lamberts, W. (2013). Growth dynamics of Chinese wingnut (Pterocarya stenoptera) seedlings and its effects on soil chemical properties under simulated water change in the three gorges reservoir region of Yangtze River. Environmental Science and Pollution Research, 20, 7112–7123. https://doi.org/10.1007/s11356-013-1878-4
Yang, Y. Y., Song, W. J., Lin, H., Wang, W. B., Du, L. N., & Xing, W. (2018). Antibiotics and antibiotic resistance genes in global lakes: A review and meta-analysis. Environment International, 116, 60–73. https://doi.org/10.1016/j.envint.2018.04.011
Yin, Y. C., & Yan, Z. Z. (2020). Variations of soil bacterial diversity and metabolic function with tidal flat elevation gradient in an artificial mangrove wetland. Science of The Total Environment, 718, 137385. https://doi.org/10.1016/j.scitotenv.2020.137385
Yu, Z. Y., Gunn, L., Wall, P., & Fanning, S. (2017). Antimicrobial resistance and its association with tolerance to heavy metals in agriculture production. Food Microbiology, 64, 23–32. https://doi.org/10.1016/j.fm.2016.12.009
Zbrun, M. V., Rossler, E., Olivero, C. R., Soto, L. P., Zimmermann, J. A., Frizzo, L. S., & Signorini, M. L. (2021). Possible reservoirs of thermotolerant Campylobacter at the farm between rearing periods and after the use of enrofloxacin as a therapeutic treatment. International Journal of Food Microbiology, 340, 109046. https://doi.org/10.1016/j.ijfoodmicro.2021.109046
Zeng, Q. T., Sun, J. T., & Zhu, L. Z. (2019). Occurrence and distribution of antibiotics and resistance genes in greenhouse and open-field agricultural soils in China. Chemosphere, 224, 900–909. https://doi.org/10.1016/j.chemosphere.2019.02.167
Zhang, B. C., Kong, W. D., Wu, N., & Zhang, Y. M. (2016). Bacterial diversity and community along the succession of biological soil crusts in the Gurbantunggut Desert, northern China. Journal of Basic Microbiology, 56, 670–679. https://doi.org/10.1002/jobm.201500751
Zhang, C., Zhou, T. T., Zhu, L. S., Du, Z. K., Li, B., Wang, J., Wang, J. H., & Sun, Y. A. (2019). Using enzyme activities and soil microbial diversity to understand the effects of fluoxastrobin on microorganisms in fluvo-aquic soil. Science of the Total Environment, 666, 89–93. https://doi.org/10.1016/j.scitotenv.2019.02.240
Zhang, J. N., Mazni, A. Z., Chee, K. L., & Joo, S. T. (2020). Application of bacteriocins in food preservation and infectious disease treatment for humans and livestock: A review. Royal Society of Chemistry Advances, 10, 38937–38964.
Zhang, Q., Wu, J., Yu, Y. Y., He, Y. J., Huang, Y., Fan, N. S., Huang, B. C., & Jin, R. C. (2020). Microbial and genetic responses of anammox process to the successive exposure of different antibiotics. Chemical Engineering Journal, 420, 127576.
Zhang, Q. Q., Ying, G. G., Pan, C. G., Liu, Y. S., & Zhao, J. L. (2015). Comprehensive evaluation of antibiotics emission and fate in the river basins of China: Source analysis, multimedia modeling, and linkage to bacterial resistance. Environmental Science and Technology, 49(11), 6772–6782. https://doi.org/10.1021/acs.est.5b00729
Zhang, S. X., Zhang, Q. Q., Liu, Y. S., Yan, X. T., Zhang, B., Xing, C., Zhao, J. L., & Ying, G. G. (2020). Emission and fate of antibiotics in the Dongjiang River Basin, China: implications for antibiotic resistance risk. Science of The Total Environment, 712, 136518. https://doi.org/10.1016/j.scitotenv.2020c.136518
Zhang, W., Huang, M. H., Qi, F. F., Sun, P. Z., & Van Ginkel, S. W. (2013). Effect of trace tetracycline concentrations on the structure of a microbial community and the development of tetracycline resistance genes in sequencing batch reactors. Bioresource Technology, 150, 9–14. https://doi.org/10.1016/j.biortech.2013.09.081
Zhang, W. J., Xia, X. M., Wang, J. H., Zhu, L. S., Wang, J., Wang, G. C., Chen, Y. Y., & Kim, Y. M. (2021). Oxidative stress and genotoxicity of nitenpyram to earthworms (Eisenia foetida). Chemosphere, 264, 128493. https://doi.org/10.1016/j.chemosphere.2020.128493
Zhang, X. R., Zhang, J. C., Han, Q. F., Wang, X. L., Wang, S. G., Yuan, X. Z., Zhang, B. Y., & Zhao, S. (2021). Antibiotics in mariculture organisms of different growth stages: Tissue-specific bioaccumulation and influencing factors. Environmental Pollution, 288, 117715. https://doi.org/10.1016/j.envpol.2021b.117715
Zhang, Y., Cheng, D. M., Zhang, Y. T., Xie, J., Xiong, H. Y., Wan, Y., Zhang, Y. Q., Chen, X. P., & Shi, X. J. (2021). Soil type shapes the antibiotic resistome profiles of long-term manured soil. Science of The Total Environment, 786, 147361. https://doi.org/10.1016/J.SCITOTENV.2021c.147361
Zhao, F. K., Yang, L., Li, G., Fang, L., Yu, X. W., Tang, Y. T., Li, M., & Chen, L. D. (2022). Veterinary antibiotics can reduce crop yields by modifying soil bacterial community and earthworm population in agro-ecosystems. Science of The Total Environment, 808, 152056. https://doi.org/10.1016/j.scitotenv.2021.152056
Zhao, H. X., Quan, W. N., Bekele, T. G., Chen, M., Zhang, X., & Qu, B. C. (2018). Effect of copper on the accumulation and elimination kinetics of fluoroquinolones in the zebrafish (Danio rerio). Ecotoxicology and Environmental Safety, 156, 135–140. https://doi.org/10.1016/j.ecoenv.2018.03.025
Zhao, Y., Cocerva, T., Cox, S., Tardif, S., Su, J. Q., Zhu, Y. G., & Brandt, K. K. (2019). Evidence for co-selection of antibiotic resistance genes and mobile genetic elements in metal polluted urban soils. Science of the Total Environment, 656, 512–520. https://doi.org/10.1016/j.scitotenv.2018.11.372
Zhi, S. L., Shen, S. Z., Zhou, J., Ding, G. Y., & Zhang, K. Q. (2020). Systematic analysis of occurrence, density and ecological risks of 45 veterinary antibiotics: Focused on family livestock farms in Erhai Lake basin, Yunnan, China. Environmental Pollution, 267, 115539. https://doi.org/10.1016/j.envpol.2020.115539
Zhou, C. R., Ma, Q., Li, S. L., Zhu, M. M., Xia, Z. Q., & Yu, W. T. (2021). Toxicological effects of single and joint sulfamethazine and cadmium stress in soil on pakchoi (Brassica chinensis L.). Chemosphere, 263, 128296. https://doi.org/10.1016/j.chemosphere.2020.128296
Acknowledgements
This work was supported by the National Natural Science Foundation of China [Grant number 41671320], the Natural Science Foundation of Shandong Province, China [ZR2016JL029], and the Special Funds of Taishan Scholar of Shandong Province, China [Grant number JQ201711].
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Zhang, W., Wang, J., Zhu, L. et al. New insights into the effects of antibiotics and copper on microbial community diversity and carbon source utilization. Environ Geochem Health 45, 4779–4793 (2023). https://doi.org/10.1007/s10653-023-01491-1
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DOI: https://doi.org/10.1007/s10653-023-01491-1