The effects of oxytetracycline (OTC) and sulfamethoxazole (SMX) antibiotics on potential nitrification and alkaline phosphatase and urease activities in a calcareous soil

Document Type : Original Article

Authors

Abstract

Pharmaceutical antibiotics such as oxytetracycline (OTC) and sulfamethoxazole (SMX) are highly consumed for the treatment of infectious diseases and to growth improvement in livestock and poultry industry every year. More than 90 percent of consumed antibiotics may be excreted from the animal's body as main compounds and bioactive metabolites, and introduced into the soil environment which may impose adverse effects on non-target microorganisms. The effects of antibiotics on soil microbial functions have not been well determined yet. In this study, in order to assess the impact of oxytetracycline and sulfamethoxazole on soil microbial functions, a factorial experiment was conducted based on completely randomized design with factors of concentrations (0, 1, 10, 25, 50 and 100 mg.kg-1 soil), time (1, 4 and 21 days) and kind of antibiotics in the laboratory conditions. Soil microbial community functions were evaluated by measuring the activities of alkaline phosphatase and urease and potential nitrification. The results showed that oxytetracycline severely affected alkaline phosphatase and urease activities in the first day of incubation. But, the activities of these enzymes were recovered with increasing the incubation time. While, sulfamethoxazole significantly inhibited activities of alkaline phosphatase and urease enzymes compared to control treatment during the incubation. The effect of oxytetracycline and sulfamethoxazole on potential nitrification followed the same pattern so that nitrification rate increased with increasing concentrations of antibiotics in the early days of incubation, but these antibiotics had adverse effects on potential nitrification over time. Overall, OTC antibiotic exerted adverse effects on soil microbial functions in the early days of incubation, while SMX antibiotic exerted long term effects on soil microbial parameters.

Keywords

References

References
Aga D.S., Goldfish R., and Kulshrestha P. 2003. Application of ELISA in determining the fate of tetracyclines in land-applied livestock wastes. Analyst, 128: 658-662.
Al-Ahmad A., Daschner F.D., and Kümmerer K. 1999. Biodegradability of cefotiam, ciprofloxacin, meropenem, penicillin G and sulfamethoxazole and inhibition of wastewater bacteria. Archives of Environmental Contamination and Toxicology, 37: 158-163.
Bailey V.L., Smith J.L., and Bolton H. 2003. Novel antibiotics as inhibitors for the selective respiratory inhibition method of measuring fungal: bacterial ratios in soil. Biology and Fertility of Soils, 38: 154-160.
Baran W., Adamek E., Sobczak A., and Sochacka J. 2009. The comparison of photocatalytic activity of Fe-salts, TiO2 and TiO2/FeCl3 during the sulfanilamide degradation process. Catalysis Communications, 10: 811-814.
Berg P., and Rosswall T. 1985. Ammonium oxidizer numbers, potential and actual oxidation rates in two Swedish arable soils. Biology and Fertility of Soils, 1: 131-140.
Black C.A., Evans D., and Dinauer R. 1965. Methods of Soil Analysis, No 9, American Society of Agronomy Madison, WI. Pp. 961-1011.
Boleas S., Alonso C., Pro J., Fernandez C., Carbonell G., and Tarazona J.V. 2005. Toxicity of the antimicrobial oxytetracycline to soil organisms in a multi-species-soil system (MS·3) and influence of manure co-addition. Journal of Hazardous Materials, 122: 233-241.
Bouyoucos G.J. 1962. Hydrometer method improved for making particle size analyses of soils. Agronomy Journal, 54: 464-465.
Ding C., and He J. 2010. Effect of antibiotics in the environment on microbial populations. Applied Microbiology and Biotechnology, 87: 925-941.
Drillia P., Dokianakis S.N., Fountoulakis M.S., Kornaros M., Stamatelatou K., and Lyberatos G. 2005. On the occasional biodegradation of pharmaceuticals in the activated sludge process: the example of the antibiotic sulfamethoxazole. Journal of Hazardous Materials, 122: 259-265.
Fang H., Han Y., Yin Y., Pan X., and Yu Y. 2014. Variations in dissipation rate, microbial function and antibiotic resistance due to repeated introductions of manure containing sulfadiazine and chlortetracycline to soil. Chemosphere, 96: 51-56.
Gutierrez I.R., Watanabe N., Harter T., Glaser B., and Radke M. 2010. Effect of sulfonamide antibiotics on microbial diversity and activity in a Californian Mollic Haploxeral. Journal of Soils and Sediments, 10: 537-544.
Hackbarth C.J., and Chambers H.F. 1989. Methicillin-resistant staphylococci: genetics and mechanisms of resistance. Antimicrobial Agents and Chemotherapy, 33: 99-104.
Haluschak P. 2006. Laboratory Methods of Soil Analysis. Canada-Manitoba Soil Survey, pp. 3-133.
Hammesfahr U., Heuer H., Manzke B., Smalla K., and Thiele-Bruhn S. 2008. Impact of the antibiotic sulfadiazine and pig manure on the microbial community structure in agricultural soils. Soil Biology and Biochemistry, 40: 1583-1591.
Hammesfahr U., Kotzerke A., Lamshöft M., Wilke B.M., Kandeler E., and Thiele-Bruhn S. 2011. Effects of sulfadiazine-contaminated fresh and stored manure on a soil microbial community. European Journal of Soil Biology, 47: 61-68.
 Hamscher G., Sczesny S., Hoper H., Pawelzick H., and 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. Analytical Chemistry, 74: 1509-1518.
Heise J., Hiiltge S., Schrader S., and Kreuzig R. 2006. Chemical and biological characterization of non-extractable sulfonamide residues in soil. Chemosphere, 65:2352-2357.
Heuer H., Schmitt H., and Smalla K. 2011. Antibiotic resistance gene spread due to manure application on agricultural fields. Current Opinion in Microbiology, 14: 236-243.
Ji L., Chen W., Duan L., and Zhu D. 2009. Mechanisms for strong adsorption of tetracycline to carbon nanotubes: a comparative study using activated carbon and graphite as adsorbents. Environmental Science and Technology, 43: 2322-2327.
Kahle M., and Stamm C. 2007. Time and pH-dependent sorption of the veterinary antimicrobial sulfathiazole to clay minerals and ferrihydrite. Chemosphere, 68: 1224-1231.
Katipoglu-Yazan T., Merlin C., Pons M.N., Ubay-Cokgor E., and Orhon D. 2016. Chronic impact of sulfamethoxazole on the metabolic activity and composition of enriched nitrifying microbial culture. Water Research, 100: 546-555.
Kong W.D., Zhu Y.G., Fu B.J., Marschner P., and He J.Z. 2006. The veterinary antibiotic oxytetracycline and Cu influence functional diversity of the soil microbial community. Environmental Pollution, 143: 129-137.
 Kong W.D., Zhu Y.G., Liang Y.C., Zhang J., Smith F.A., and Yang A. 2007. Uptake of oxytetracycline and its phytotoxicity to alfalfa (Medicago sativa L.). Environmental Pollution, 147: 187-193.
Kumar K., Thompson A., Singh A.K., Chander Y., Gupta S.C. 2004. Enzyme linked immunosorbent assay for ultratrace determination of antibiotics in aqueous samples. Journal of Environmental Quality, 33: 250-256.
Liu B., Li X., Zhang X., Wang J., and 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.
Liu W., Pan N., Chen W., Jiao W., and Wang M. 2012. Effect of veterinary oxytetracycline on functional diversity of soil microbial community. Plant Soil and Environment, 58: 295-301.
Martinez J.L. 2009. Environmental pollution by antibiotics and by antibiotic resistance determinants. Environmental Pollution, 157: 2893-2902.
Mijangos I., Becerril J.E.M., Albizu I., Epelde L., and Garbisu C. 2009. Effects of glyphosate on rhizosphere soil microbial communities under two different plant compositions by cultivation-dependent and-independent methodologies. Soil Biology and Biochemistry, 41: 505-513.
Nelson K.L., Brözel V.S., Gibson S.A., Thaler R., and Sharon A. 2011. Influence of manure from pigs fed chlortetracycline as growth promotant on soil microbial community structure. World Journal of Microbiology and Biotechnology, 27: 659-668. 
Park J.Y., and Huwe B. 2016. Effect of pH and soil structure on transport of sulfonamide antibiotics in agricultural soils. Environmental Pollution, 213: 561-570.
Qasemian L., Guiral D., Ziarelli F., Van Dang T.K., and Farnet A. 2012. Effects of anthracene on microbial activities and organic matter decomposition in a Pinus halepensis litter from a Mediterranean coastal area. Soil Biology and Biochemistry, 46: 148-154.
Reichel R., Rosendahl I., Peeters E.T.H.M., Focks A., Groeneweg J., Bierl R., Schlichting A., Amelung W., and Thiele-Bruhn S. 2013. Effects of slurry from sulfadiazine- (SDZ) and difloxacin- (DIF) medicated pigs on the structural diversity of microorganisms in bulk and rhizosphere soil. Soil Biology and Biochemistry, 62: 82-91.
Rodríguez-Loinaz G., Onaindia M., Amezaga I., Mijangos I., and Garbisu C. 2008. Relationship between vegetation diversity and soil functional diversity in native mixed-oak forests. Soil Biology and Biochemistry, 40: 49-60.
Rosendahl I., Siemens J., Groeneweg J., Linzbach E., Laabs V., Herrmann C., Vereecken H., and Amelung W. 2011. Dissipation and sequestration of the veterinary antibiotic sulfadiazine and its metabolites under field conditions. Environmental Science and Technology, 45: 5216-5222.
Schloter M., Dilly O., and Munch J.C. 2003. Indicators for evaluating soil quality. Agriculture Ecosystems and Environment, 98: 255-262.
Schmitt H., Haapakangas H., and van Beelen P. 2005. Effects of antibiotics on soil microorganisms: time and nutrients influence pollution-induced community tolerance. Soil Biology and Biochemistry, 37: 1882-1892.
Tabatabai M.A. 1994. Soil enzymes. In: Weaver R.W., Angle J.S., and Bottomley P.S (Eds). Methods of soil analysis- Part 2, Microbiological and biochemical properties, Soil Science Society of America,Madison, WI, pp. 801-834.
Thiele-Bruhn S., and Beck I.C. 2005. Effects of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere, 59: 457-465.
Walkley A., and Black I.A. 1934. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science, 37: 29-38.
Wang Q., Guo M., and Yate S.R. 2006. Degradation kinetics of manure-derived sulfadimethoxine in amended soil. Journal of Agricultural and Food Chemistry, 54: 157-163.
Wu N., Qiao M., Zhang, B., Cheng W.D., Zhu Y.G. 2010. Abundance and diversity of tetracycline resistance genes in soils adjacent to representative swine feedlots in China. Environmental Science and Technology, 44: 6933-6939.
Yang J., Ying G., Yang L., Zhao J., Liu F., Tao R., Yu Z., and Peng P. 2009a. Degradation behavior of sulfadiazine in soils under different conditions. Journal of Environmental Science and Health, 44: 241-248.
Yang Q., Zhang J., Zhu K., and Zhang H. 2009b. Influence of oxytetracycline on the structure and activity of microbial community in wheat rhizosphere soil. Journal of Environmental Sciences, 21: 954-959.
Yao X.H., Min H., Lü Z.H., and Yuan H.P. 2006. Influence of acetamiprid on soil enzymatic activities and respiration. European Journal of Soil Biology, 42: 1200-126.
Zhang Y., Xu J., Zhong Z., Guo C., Li L., He Y., Fan W., and Chen Y. 2013. Degradation of sulfonamides antibiotics in lake water and sediment. Environmental Science and Pollution Research, 20: 2372-2380.
Zielezny Y., Groeneweg J., Vereecken H., and Tappe W. 2006. Impact of sulfadiazine and chlortetracycline on soil bacterial community structure and respiratory activity. Soil Biology and Biochemistry, 38: 2372-2380.
Applied Soil Research
Volume 6, Issue 2
August 2018
Pages 1-14

Files

History

  • Receive Date: 05 December 2016
  • Revise Date: 06 August 2018
  • Accept Date: 30 December 2017

Share

How to cite

Statistics