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Toxicity of enrofloxacin and cadmium alone and in combination to enzymatic activities and microbial community structure in soil

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Abstract

Antibiotics and heavy metals have long-term potential toxicity to the environment, and their residuals in agricultural soils are receiving more and more attention. To evaluate the ecotoxicological effects of enrofloxacin and cadmium on soil enzymatic activities and microbial community structure, soil samples were exposed to individual and combined contaminants over 28 days. The results indicated that the toxic effects of enrofloxacin alone on soil enzymatic activities were relatively small and showed no concentration dependence. In contrast, significant inhibition of soil enzymatic activities was observed upon cadmium contamination by itself. Overall, the combination of two contaminants also has toxic effect on enzymatic activities; an antagonism between enrofloxacin and cadmium was observed. On 14 and 21 days, individual enrofloxacin and cadmium reduced average well color development (AWCD), Shannon, McIntosh, Simpson indices, and substrate utilization, except for Shannon, McIntosh, Simpson indices of the cadmium 0.4 mmol/kg treatment were higher than the control on 21 days. In general, combined treatments led to higher value of these microbial diversity indicators than those found under separate contamination, although there were some exceptions. With the increase in enrofloxacin concentration, the utilization of any carbon source by the microorganisms gradually decreased. In addition, the AWCD value and substrate utilization decreased as time increased. In the separate and combined contaminant treatments, the order of substrate utilization by soil microorganisms was aliphatics > amino acids > saccharides > metabolites. Thus, enrofloxacin and cadmium had a variable but generally negative influence on soil enzymatic activities and microbial community structure.

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References

  • Anderson, T. H. (2003). Microbial eco-physiological indicators to asses soil quality. Agriculture, Ecosystems & Environment,98(1), 285–293.

    Google Scholar 

  • Arthur, E., Moldrup, P., Holmstrup, M., Schjønning, P., Winding, A., Mayer, P., et al. (2012). Soil microbial and physical properties and their relations along a steep copper gradient. Agriculture, Ecosystems & Environment,159(18), 9–18.

    CAS  Google Scholar 

  • Babić, S., Periša, M., & Škorić, I. (2013). Photolytic degradation of norfloxacin, enrofloxacin and ciprofloxacin in various aqueous media. Chemosphere,91(11), 1635–1642.

    Google Scholar 

  • Bermudez, G. M. A., Jasan, R., Plá, Rita, & Pignata, María L. (2012). Heavy metals and trace elements in atmospheric fall-out: their relationship with topsoil and wheat element composition. Journal of Hazardous Materials,213–214, 447–456.

    Google Scholar 

  • Chigbo, C., & Batty, L. (2013). Effect of combined pollution of chromium and benzo(a)pyrene on seed growth of lolium perenne. Chemosphere,90(2), 164–169.

    CAS  Google Scholar 

  • Fernández-Calviño, D., Soler-Rovira, P., Polo, A., Díaz-Raviña, M., Arias-Estévez, M., & Plaza, C. (2010). Enzyme activities in vineyard soils long-term treated with copper-based fungicides. Soil Biology & Biochemistry,42(12), 2119–2127.

    Google Scholar 

  • Gao, M., Song, W., Zhou, Q., Ma, X., & Chen, X. (2013). Interactive effect of oxytetracycline and lead on soil enzymatic activity and microbial biomass. Environmental Toxicology and Pharmacology,36(2), 667–674.

    CAS  Google Scholar 

  • Ge, T., Nie, S., Wu, J., Xiao, H., Tong, C., Huang, D., et al. (2011). Chemical properties, microbial biomass, and activity differ between soils of organic and conventional horticultural systems under greenhouse and open field management: a case study. Journal of Soils and Sediments,11(1), 25–36.

    CAS  Google Scholar 

  • Gothwal, R., & Shashidhar, T. (2015). Antibiotic pollution in the environment: a review. CLEAN - Soil, Air, Water,43(4), 479–489.

    CAS  Google Scholar 

  • 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(4), 1434–1443.

    CAS  Google Scholar 

  • Hassan, W., Akmal, M., Muhammad, I., Younas, M., Zahaid, K. R., & Ali, F. (2013). Response of soil microbial biomass and enzymes activity to cadmium (cd) toxicity under different soil textures and incubation times. Australian Journal of Crop Science,7(5), 674–680.

    CAS  Google Scholar 

  • Hu, X. F., Jiang, Y., Shu, Y., Hu, X., Liu, L., & Luo, F. (2014). Effects of mining wastewater discharges on heavy metal pollution and soil enzyme activity of the paddy fields. Journal of Geochemical Exploration,147, 139–150.

    CAS  Google Scholar 

  • Huang, R. X., Bei, W., Pei, Z. G., Shan, X. Q., Zhang, S. Z., & Williams, P. N. (2009). Accumulation, subcellular distribution and toxicity of copper in earthworm (eisenia fetida) in the presence of ciprofloxacin. Environmental Science and Technology,43(10), 3688–3693.

    CAS  Google Scholar 

  • Ibrahim, H. K., Abdelmoety, M. M., Abdelgawad, S. A., Alghobashy, M. A., & Kawy, M. A. (2017). Validated electrochemical and chromatographic quantifications of some antibiotic residues in pharmaceutical industrial waste water. Environmental Science and Pollution Research,24(8), 1–12.

    Google Scholar 

  • Kelepertzis, E. (2014). Accumulation of heavy metals in agricultural soils of mediterranean: insights from argolida basin, peloponnese, greece. Geoderma,221–222(27), 82–90.

    Google Scholar 

  • Khan, S., Aell, H., Qiao, M., Rehman, S., & He, J. Z. (2010). Effects of cd and pb on soil microbial community structure and activities. Environmental Science and Pollution Research,17(2), 288–296.

    CAS  Google Scholar 

  • Kong, W. D., Zhu, Y. G., Fu, B. J., Marschner, P., & He, J. Z. (2006). The veterinary antibiotic oxytetracycline and cu influence functional diversity of the soil microbial community. Environmental Pollution,143(1), 129–137.

    CAS  Google Scholar 

  • Larson, C. (2014). China gets serious about its pollutant-laden soil. Science,343(6178), 1415–1416.

    Google Scholar 

  • Leston, S., Nunes, M., Viegas, I., Nebot, C., Cepeda, A., Pardal, M. Â., et al. (2014). The influence of sulfathiazole on the macroalgae ulva lactuca. Chemosphere,100, 105–110.

    CAS  Google Scholar 

  • Li, Y. S., Tang, H., Hu, Y. X., Wang, X. H., Ai, X. J., Tang, L., et al. (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(5), 312–320.

    CAS  Google Scholar 

  • Li, Z., Ma, Z., van der Kuijp, T. J., Yuan, Z., & Huang, L. (2014). A review of soil heavy metal pollution from mines in china: pollution and health risk assessment. Science of the Total Environment,468–469, 843–853.

    Google Scholar 

  • Liu, A., Liu, M., Menghong, L. I., Xiaoxuan, M. A., Sun, X., & Wang, H. (2013). Collaborative effects of cu and antibiotic on soil microbial activities. Ecology & Environmental Sciences,22(11), 1825–1829. (in Chinese).

    Google Scholar 

  • Liu, B., Li, Y., Zhang, X., Wang, J., & Gao, M. (2015). Effects of chlortetracycline on soil microbial communities: comparisons of enzyme activities to the functional diversity via biolog ecoplates™. European Journal of Soil Biology,68, 69–76.

    CAS  Google Scholar 

  • Liu, F., Wu, J., Ying, G. G., Luo, Z., & Feng, H. (2012). Changes in functional diversity of soil microbial community with addition of antibiotics sulfamethoxazole and chlortetracycline. Applied Microbiology and Biotechnology,95(6), 1615–1623.

    CAS  Google Scholar 

  • Liu, F., Ying, G. G., Tao, R., Zhao, J. L., Yang, J. F., & Zhao, L. F. (2009). Effects of six selected antibiotics on plant growth and soil microbial and enzymatic activities. Environmental Pollution,157(5), 1636–1642.

    CAS  Google Scholar 

  • Liu, X., Tian, G., Jiang, D., Zhang, C., & Kong, L. (2016). Cadmium (cd) distribution and contamination in chinese paddy soils on national scale. Environmental Science and Pollution Research,23(18), 1–12.

    Google Scholar 

  • Lópezgresa, M. P., Ortiz, R., Perelló, L., Latorre, J., Liugonzález, M., Garcíagranda, S., et al. (2002). Interactions of metal ions with two quinolone antimicrobial agents (cinoxacin and ciprofloxacin). Spectroscopic and X-ray structural characterization. Antibacterial studies. Journal of Inorganic Biochemistry,92(1), 65–74.

    Google Scholar 

  • Ma, S. C., Zhang, H. B., Ma, S. T., Wang, R., Wang, G. X., Shao, Y., et al. (2015). Effects of mine wastewater irrigation on activities of soil enzymes and physiological properties, heavy metal uptake and grain yield in winter wheat. Ecotoxicology and Environmental Safety,113(113C), 483–490.

    CAS  Google Scholar 

  • Martins, V. V., Zanetti, M. O., Pitondosilva, A., & Stehling, E. G. (2014). Aquatic environments polluted with antibiotics and heavy metals: a human health hazard. Environmental Science and Pollution Research,21(9), 5873–5878.

    CAS  Google Scholar 

  • Nayak, A. K., Raja, R., Rao, K. S., Shukla, A. K., Mohanty, S., Shahid, M., et al. (2015). Effect of fly ash application on soil microbial response and heavy metal accumulation in soil and rice plant. Ecotoxicology and Environmental Safety,114, 257–262.

    CAS  Google Scholar 

  • Nizova, A. A. (1969). study of sucrase activity in turf-podzol heavy-loamy soil. Mikrobiologiia,38(2), 336–339.

    CAS  Google Scholar 

  • Ostermann, A., Gao, J., Welp, G., Siemens, J., Roelcke, M., Heimann, L., et al. (2014). Identification of soil contamination hotspots with veterinary antibiotics using heavy metal concentrations and leaching data–a field study in china. Environmental Monitoring and Assessment,186(11), 7693–7707.

    CAS  Google Scholar 

  • Pan, J., & Yu, L. (2011). Effects of Cd or/and Pb on soil enzyme activities and microbial community structure. Ecological Engineering,37(11), 1889–1894.

    Google Scholar 

  • Qiang, Z., & Adams, C. (2004). Potentiometric determination of acid dissociation constants (pka) for human and veterinary antibiotics. Water Research,38(12), 2874–2890.

    CAS  Google Scholar 

  • Rehman, Z. U., Khan, S., Brusseau, M. L., & Shah, M. T. (2017). Lead and cadmium contamination and exposure risk assessment via consumption of vegetables grown in agricultural soils of five-selected regions of Pakistan. Chemosphere,168, 1589–1596.

    CAS  Google Scholar 

  • Renella, G., Mench, M., Lelie, D. V. D., Pietramellara, G., Ascher, J., Ceccherini, M. T., et al. (2004). Hydrolase activity, microbial biomass and community structure in long-term cd-contaminated soils. Soil Biology & Biochemistry,36(3), 443–451.

    CAS  Google Scholar 

  • Riaz, L., Mahmood, T., Coyne, M. S., Khalid, A., Rashid, A., Hayat, M. T., et al. (2017). Physiological and antioxidant response of wheat (Triticum aestivum) seedlings to fluoroquinolone antibiotics. Chemosphere,177, 250.

    CAS  Google Scholar 

  • Robson, T. C., Braungardt, C. B., Rieuwerts, J., & Worsfold, P. (2014). Cadmium contamination of agricultural soils and crops resulting from sphalerite weathering. Environmental Pollution,184, 283–289.

    CAS  Google Scholar 

  • Sharma, S. K., Ramesh, A., Sharma, M. P., Joshi, O. P., Govaerts, B., Steenwerth, K. L., et al. (2010). Microbial community structure and diversity as indicators for evaluating soil quality. Biodiversity, Biofuels, Agroforestry and Conservation Agriculture,5, 317–358.

    Google Scholar 

  • Simmons, R. W., Pongsakul, P., Saiyasitpanich, D., & Klinphoklap, S. (2005). Elevated levels of cadmium and zinc in paddy soils and elevated levels of cadmium in rice grain downstream of a zinc mineralized area in Thailand: implications for public health. Environmental Geochemistry and Health,27(5–6), 501–511.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Tai, Y. P., Mo, C. H., Li, Y. W., Wu, X. L., Zou, X., Gao, P., et al. (2010). Concentration and distribution of quinolone antibiotics in long-term manure-amended soils. China Environmental Science,30(6), 816–821. (in Chinese).

    CAS  Google Scholar 

  • Trasar-Cepeda, C., Leirós, M. C., & Gil-Sotres, F. (2008). Hydrolytic enzyme activities in agricultural and forest soils. Some implications for their use as indicators of soil quality. Soil Biology & Biochemistry,40(9), 2146–2155.

    CAS  Google Scholar 

  • Turel, I. (2002). The interactions of metal ions with quinolone antibacterial agents. Coordination Chemistry Reviews,232(1), 27–47.

    CAS  Google Scholar 

  • Viti, C., & Giovannetti, L. (2005). Characterization of cultivable heterotrophic bacterial communities in Cr-polluted and unpolluted soils using biolog and ardra approaches. Applied Soil Ecology,28(2), 101–112.

    Google Scholar 

  • Wen, B., Huang, R., Wang, P., Zhou, Y., Shan, X. Q., & Zhang, S. (2011). Effect of complexation on the accumulation and elimination kinetics of cadmium and ciprofloxacin in the Earthworm eisenia fetida. Environmental Science and Technology,45(10), 4339–4345.

    CAS  Google Scholar 

  • Xian, Y., Wang, M., & Chen, W. (2015). Quantitative assessment on soil enzyme activities of heavy metal contaminated soils with various soil properties. Chemosphere,139, 604–608.

    CAS  Google Scholar 

  • Xu, Y. P., Liu, S. Y., Guo, F., & Zhang, B. (2016). Evaluation of the oxidation of enrofloxacin by permanganate and the antimicrobial activity of the products. Chemosphere,144, 113–121.

    CAS  Google Scholar 

  • Yang, X., Song, Y., Kai, J., & Cao, X. (2012). Enzymatic biomarkers of Earthworms eisenia fetida, in response to individual and combined cadmium and pyrene. Ecotoxicology and Environmental Safety,86(4), 162–167.

    CAS  Google Scholar 

  • Yuan, Z. M., Liu, H. J., Han, J., Sun, J. J., Wu, X. Y., & Yao, J. (2017). Monitoring soil microbial activities in different cropping systems using combined methods. Pedosphere,27(1), 138–146.

    Google Scholar 

  • Zhai, L. M., Liao, X. Y., Chen, T. B., Yan, X. L., Xie, H., Wu, B., et al. (2008). Regional assessment of cadmium pollution in agricultural lands and the potential health risk related to intensive mining activities: A case study in Chenzhou City, China. Journal of Environmental Sciences,20(6), 696–703.

    CAS  Google Scholar 

  • Zhang, H., Zhang, L., Wang, J., Zhu, K., Wang, H., & Yang, Q. (2012). Influence of oxytetracycline exposure on antibiotic resistant bacteria and enzyme activities in wheat rhizosphere soil. Acta Ecologica Sinica,32(2), 508–516. (in Chinese).

    Google Scholar 

  • Zhang, H. J., Zhang, X. Z., Li, T. X., & Huang, F. (2014a). Variation of cadmium uptake, translocation among rice lines and detecting for potential cadmium-safe cultivars. Environmental Earth Sciences,71(1), 277–286.

    CAS  Google Scholar 

  • Zhang, W. L., Du, Y., Zhai, M. M., & Shang, Q. (2014b). Cadmium exposure and its health effects: a 19-year follow-up study of a polluted area in china. Science of the Total Environment,470–471(2), 224–228.

    Google Scholar 

  • Zhang, X., Wang, H., He, L., Lu, K., Sarmah, A., Li, J., et al. (2013). Using biochar for remediation of soils contaminated with heavy metals and organic pollutants. Environmental Science and Pollution Research,20(12), 8472–8483.

    CAS  Google Scholar 

  • Zhang, X., Xia, Y. S., Shang, Y. J., Zhao, Q. Q., & Shi, J. (2017). Effects of biochar (BC) on microbial diversity of cadmium(Cd) contaminated soil. China Environmental Science,37(1), 252–262. (in Chinese).

    Google Scholar 

  • Zhou, X., Chen, C., Yue, L., Sun, Y., Ding, H., & Liu, Y. (2008). Excretion of enrofloxacin in pigs and its effect on ecological environment. Environmental Toxicology and Pharmacology,26(3), 272–277.

    CAS  Google Scholar 

  • Zhou, Z., Wang, S., Guo, L., Dong, J., & Zhang, N. (2014). Influences of duck feces and ciprofloxacin on soil microbial community functional diversity in ustic cambosols. Asian Journal of Ecotoxicology,9, 1118–1125. (in Chinese).

    Google Scholar 

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Acknowledgements

The present study was supported by grants from the National Science and Technology Major Project of the Ministry of Science and Technology of China (Nos. 2017YFD0800703 and 2016YFD0201203); the National Natural Science Foundation of China (No. 21377075); the Natural Science Foundation of Shandong Province, China (Nos. JQ201711 and ZR2016JL029); and the Special Funds of Taishan Scholar of Shandong Province, China. We also very thank Michael L. Thompson from Iowa State University for review of this manuscript.

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  1. Lanjun Wang and Wenjie Zhang have contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Agricultural Environment in Universities of Shandong, College of Resources and Environment, Shandong Agricultural University, 61 Daizong Road, Taian, 271018, People’s Republic of China

    Lanjun Wang, Wenjie Zhang, Jinhua Wang, Lusheng Zhu, Jun Wang & Saihong Yan

  2. State Key Laboratory of Water Resources and Water Hydropower Engineering Science, Wuhan University, Hubei, 430072, People’s Republic of China

    Zulfiqar Ahmad

  3. Department of Environmental Sciences, PMAS Arid Agriculture University, Rawalpindi, 46300, Pakistan

    Zulfiqar Ahmad

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  1. Lanjun Wang
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  3. Jinhua Wang
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Wang, L., Zhang, W., Wang, J. et al. Toxicity of enrofloxacin and cadmium alone and in combination to enzymatic activities and microbial community structure in soil. Environ Geochem Health 41, 2593–2606 (2019). https://doi.org/10.1007/s10653-019-00307-5

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