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Effects of compost containing oxytetracycline on enzyme activities and microbial communities in maize rhizosphere soil

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Abstract

Veterinary antibiotics can enter agricultural fields via the application of livestock manure containing antibiotics. However, the response of soil microorganisms to compost containing antibiotics is not well understood. A 120-day pot experiment was conducted to investigate the impact of compost containing oxytetracycline (OTC) on the enzyme activities and microbial communities in maize rhizosphere soil. Swine manure was artificially spiked with OTC at four concentrations, 35, 70, 105, and 140 mg kg−1, and combined with straw to produce compost. The compost products were applied to soil planted with maize. Rhizosphere soil samples were collected on days 1, 15, 30, 60, and 120. The results indicated that the urease activities first increased and then declined, while in contrast, the alkaline phosphatase activities first decreased and then increased slightly. Catalase exhibited dose-related activation during the maize growth period. At the end of the experiment, the soil enzyme activities were similar to their initial values, indicating that the soil enzymes showed a level of recovery. The carbon metabolic activity levels were higher in the soils with high OTC concentrations than in the control, whereas the Shannon diversity index was higher in the control soil. The results of principal component analysis (PCA) indicated that the application of compost containing OTC shifted the structure of the soil microbial community and negatively affected its stability. These results suggest that the compost containing OTC exerted selective pressure on enzyme activities and microbial communities in maize rhizosphere soil and decreased their resilience to antibiotic pollution.

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References

  • Anderson TH (2003) Microbial eco-physiological indicators to asses soil quality. Agric Ecosyst Environ 98:285–293

    Article  Google Scholar 

  • Baguer AJ, Jensen J, Krogh PH (2000) Effects of the antibiotics oxytetracycline and tylosin on soil fauna. Chemosphere 40:751–757

    Article  CAS  Google Scholar 

  • Bending GD, Turner MK, Jones JE (2002) Interactions between crop residue and soil organic matter quality and the functional diversity of soil microbial communities. Soil Biol Biochem 34:1073–1082

    Article  CAS  Google Scholar 

  • Boleas S, Alonso C, Pro J, Fernández C, Carbonell G, Tarazona JV (2005) Toxicity of the antimicrobial oxytetracycline to soil organisms in a multi-species-soil system (MS-3) and influence of manure co-addition. J Hazard Mater 122:233–241

    Article  CAS  Google Scholar 

  • Brandt KK, Sjøholm OR, Krogh KA, Halling-Sørensen B, Nybroe O (2009) Increased pollution-induced bacterial community tolerance to sulfadiazine in soil hotspots amended with artificial root exudates. Environ Sci Technol 43:2963–2968

    Article  CAS  Google Scholar 

  • Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234

    Article  CAS  Google Scholar 

  • Chi ZX, Liu RT, Zhang H (2010) Potential enzyme toxicity of oxytetracycline to catalase. Sci Total Environ 408:5399–5404

    Article  CAS  Google Scholar 

  • Demoling LA, Bååth E, Greve G, Wouterse M, Schmitt H (2009) Effects of sulfamethoxazole on soil microbial communities after adding substrate. Soil Biol Biochem 41:840–848

    Article  CAS  Google Scholar 

  • Dijck PV, van de Voorde H (1976) Sensitivity of environmental microorganism to antimicrobial agents. Appl Environ Microbiol 31:332–336

    Google Scholar 

  • Elena MC, Carmen GB, Scharf S, Gans O (2007) Environmental monitoring study of selected veterinary antibiotics in animal manure and soils in Austria. Environ Pollut 148:1–10

    Article  Google Scholar 

  • Fang H, Yu YL, Chu XQ, Wang XG, Yang XE, Yu JQ (2009) Degradation of chlorpyrifos in laboratory soil and its impact on soil microbial functional diversity. J Environ Sci 21:380–386

    Article  CAS  Google Scholar 

  • Fernandes JP, Almeida CMR, Pereira AC, Ribeiro IL, Reis I, Carvalho P, Basto MCP, Mucha AP (2015) Microbial community dynamics associated with veterinary antibiotics removal in constructed wetlands microcosms. Bioresour Technol 182:26–33

    Article  CAS  Google Scholar 

  • Frankenberger WT, Dick WA (1983) Relationship between enzyme activities and microbial growth and activity indices in soil. Soil Sci Soc Am J 47:945–951

    Article  CAS  Google Scholar 

  • Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57:2351–2359

    CAS  Google Scholar 

  • Gu C, Karthikeyan KG, Sibley SD, Pedersen JA (2007) Complexation of the antibiotic tetracycline with humic acid. Chemosphere 66:1494–1501

    Article  CAS  Google Scholar 

  • Guan SY, Zhang D, Zhang Z (1986) Soil enzymes and research methods. Agricultural Press, Beijing, pp 260–339

    Google Scholar 

  • Guo B, Yao LX, Liu ZZ, He ZH, Zhou CM, Li GL, Yang BM, Huang LX (2011) Effects of sulfa drug on soil enzyme activities. Ecol Environ Sci 20:970–974 (in Chinese)

    Google Scholar 

  • Guo XL, Gu J, Gao H, Qin QJ, Chen ZX, Shao L, Chen L, Li HL, Zhang WJ, Chen SN, Liu J (2012) Effects of Cu on metabolisms and enzyme activities of microbial communities in the process of composting. Bioresour Technol 108:140–148

    Article  CAS  Google Scholar 

  • Hamscher G, Sczesny S, Höper H, Nau H (2002) Determination of persistent tetracycline residues in soil fertilized with liquid manure by high-performance liquid chromatography with electrospray ionization tandem mass spectrometry. Anal Chem 74:1509–1518

    Article  CAS  Google Scholar 

  • Ho YB, Zakaria MP, Latif PA, Saari N (2013) Degradation of veterinary antibiotics and hormone during broiler manure composting. Bioresour Technol 131:476–484

    Article  CAS  Google Scholar 

  • Jechalke S, Heuer H, Siemens J, Amelung W, Smalla K (2014) Fate and effects of veterinary antibiotics in soil. Trends Microbiol 22:536–545

    Article  CAS  Google Scholar 

  • Kemper N (2008) Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indic 8:1–13

    Article  CAS  Google Scholar 

  • Kim KR, Owens G, Ok YS, Park WK, Lee DB, Kwon SI (2012) Decline in extractable antibiotics in manure-based composts during composting. Waste Manag 32:110–116

    Article  CAS  Google Scholar 

  • Li YW, Mo CH, Zhao N, Tai YP, Bao YO, Wang JY, Li MY, Liang WM (2009) Investigation of sulfonamides and tetracyclines antibiotics in soils from various vegetable fields. Environ Sci 30:1762–1766 (in Chinese)

    CAS  Google Scholar 

  • Liu F, Ying GG, Zhou QX, Tao R, Su HC, Li X (2009a) Effects of antimicrobial drugs on soil microbial respiration. Environ Sci 30:1280–1285 (in Chinese)

    CAS  Google Scholar 

  • Liu F, Ying GG, Tao R, Zhao JL, Yang JF, Zhao LF (2009b) Effects of six selected antibiotics on plant growth and soil microbial and enzymatic activities. Environ Pollut 157:1636–1642

    Article  CAS  Google Scholar 

  • Liu B, Li YX, Zhang XL, Feng CH, Gao M, Shen Q (2015a) Effects of composting process on the dissipation of extractable sulfonamides in swine manure. Bioresour Technol 175:284–290

    Article  CAS  Google Scholar 

  • Liu B, Li YX, Zhang XL, Wang J, Gao M (2015b) Effect of chlortetracycline on soil microbial communities: comparisons of enzyme activities to the functional diversity via Biolog EcoPlate™. Eur J Soil Biol 68:69–76

    Article  CAS  Google Scholar 

  • Melaku S, Dams R, Moens L (2005) Determination of trace elements in agricultural soil samples by inductively coupled plasma-mass spectrometry: microwave acid digestion versus aqua regia extraction. Anal Chim Acta 543:117–123

    Article  CAS  Google Scholar 

  • Mojica ERE, Aga DS (2011) Antibiotics pollution in soil and water: potential ecological and human health issues. Encyclopedia of Environmental Health 97–110. https://doi.org/10.1016/B978-0-444-52272-6.00338-X

  • Paola G, Valeria A, Anna BC (2018) Ecological effects of antibiotics on natural ecosystems. Microchem J 136:25–29

    Article  Google Scholar 

  • Pinna MV, Castaldi P, Deiana P, Pusino A, Garau G (2012) Sorption behavior of sulfamethazine on unamended and manure-amended soils and short-term impact on soil microbial community. Ecotoxicol Environ Saf 84:234–242

    Article  Google Scholar 

  • Qian X, Gu J, Sun W, Li YD, Fu QX, Wang XJ, Gao H (2014) Changes in the soil nutrient levels, enzyme activities, microbial community function, and structure during apple orchard maturation. Appl Soil Ecol 77:18–25

    Article  Google Scholar 

  • Qian X, Gu J, Pan HJ, Zhang KY, Sun W, Wang XJ, Gao H (2015) Effects of living mulches on the soil nutrient contents, enzyme activities, and bacterial community diversities of apple orchard soils. Eur J Soil Biol 70:23–30

    Article  CAS  Google Scholar 

  • Schloter M, Dilly O, Munch JC (2003) Indicators for evaluating soil quality. Agric Ecosyst Environ 98:255–262

    Article  Google Scholar 

  • Thiele-Bruhn S, Beck IC (2005) Effect of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere 59:457–465

    Article  CAS  Google Scholar 

  • Warman PR (1980) The effect of amprolium and aureomycin antibiotic on the nitrification of poultry manure-amended soil. J Soil Sci Soc USA 44:1333–l334

    Article  CAS  Google Scholar 

  • Yang JF, Ying GG, Zhou LJ, Liu S, Zhao JL (2009) Dissipation of oxytetracycline in soils under different redox conditions. Environ Pollut 157:2704–2709

    Article  CAS  Google Scholar 

  • Yao ZP, Li ZJ, Lang YC, Zhang YQ, Yao JH, Xie XY (2009) Dynamic responses of soil enzymatic activities to oxytetracycline in soil. Plant Nutr Fertilizer Sci 15:696–700 (in Chinese)

    CAS  Google Scholar 

  • Zarfl C, Klasmeier J, Matthies M (2009) A conceptual model describing the fate of sulfadiazine and its metabolites observed in manure-amended soils. Chemosphere 77:720–726

    Article  CAS  Google Scholar 

  • Zhang SQ, Zhang FD, Liu XM (2005) Determination and analysis on main harmful composition in excrement of scale livestock and poultry feedlots. Plant Nutr Fertilizer Sci 11:822–829 (in Chinese)

    Google Scholar 

  • Zhen LS, Gu J, Hu T, Liu C, Jia FA, Lü R (2015) Kinetics of petroleum hydrocarbon degradation in soil and diversity of microbial community during composting. Transactions of the Chinese Society of Agricultural Engineering 31:231–238 (in Chinese)

    CAS  Google Scholar 

Download references

Acknowledgements

We thank American Journal Experts (AJE) for their professional English language editing services.

Funding

This work was supported by the National Natural Science Foundation (40771109, 40871119), the Fund of the Ministry of Agriculture of China (grant number 2010-Z20), and the Shaanxi Province Academy of Sciences (2014K-13, 2016K-21).

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Authors and Affiliations

  1. Shaanxi Province Institute of Microbiology, Xi’an, 710043, Shaanxi, China

    Lisha Zhen & Ting Hu

  2. College of Natural Resources and Environment, Northwest A & Forestry University, Yangling, 712100, Shaanxi, China

    Lisha Zhen, Jie Gu, Ting Hu & Zhixue Chen

Authors
  1. Lisha Zhen
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  2. Jie Gu
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  3. Ting Hu
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  4. Zhixue Chen
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Correspondence to Jie Gu.

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Responsible editor: Diane Purchase

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Zhen, L., Gu, J., Hu, T. et al. Effects of compost containing oxytetracycline on enzyme activities and microbial communities in maize rhizosphere soil. Environ Sci Pollut Res 25, 29459–29467 (2018). https://doi.org/10.1007/s11356-018-2964-4

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