Sequestration of veterinary medicines in soils

• Applicant: Professor Dr. Wulf Amelung
• Subject Area: Soil Sciences
• Term: from 2005 to 2012
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 5471428

• Final Report Year: 2014

Final Report Abstract

The environmental effects of veterinary antibiotics that currently provoke increasing public concerns largely depend on the fate of these substances following their application with manure to soil. In this context, sorption and sequestration are key processes that govern the antibiotic’s chemical and biological availability in the short and long run. We therefore investigated these processes using two test compounds (sulfadiazine/SDZ and difloxacin/DIF). Our experiments evolved from laboratory incubations to complex mesocosm and field studies, which increasingly permitted integrating the effects of various environmental variables (soil moisture and soil temperature) and particular soil compartments (rhizosphere, aggregates) on the fate of antibiotics. Following these experiments, we sequentially extracted an easily-extractable fraction (EAS, a proxy for bioaccessibility) and a sequestered residual fraction (RES) from soil to account for antibiotic fractions of different binding strength. Under controlled laboratory conditions, the dissipation of easily-extractable SDZ was rapid (DT50 < 21 d), while a second more strongly bound residual fraction concomitantly built up in soil and was then very persistent (DT50 > 290 d). Additional laboratory experiments revealed that the sequestration of SDZ is most likely driven by the diffusion of SDZ into soil organic matter (SOM) and – to a smaller extent – into the pores of iron oxides. The sequestration of SDZ was furthermore paralleled by a pronounced formation of non-extractable residues, amounting to approx. 50% of the applied amount after three months. Out of the two major metabolites of SDZ in manure, only 4-OH-SDZ was preserved in soil yet it lacked evidence of toxicity. The other metabolite, N-Ac-SDZ, however, was rapidly reconverted into the target antibiotic. The field experiments showed a similar behavior under field conditions. The presence of plants even accelerated the dissipation of easily-extractable SDZ in the rhizosphere, presumably as a result of an enhanced biological transformation of SDZ. This implies a reduced exposure of the particularly active microbial communities in the rhizosphere to SDZ. Yet, due to remobilization processes, concentrations never reached zero, i.e., the exposure of microorganisms to SDZ was weak but continuous. The dissipation of both SDZ fractions was largely governed by soil temperature, so that antibiotic concentrations measured in the field could be predicted from a temperature-adjustment of the dissipation rate constants, which was derived from laboratory experiments at different temperatures. The impact of soil moisture, however, was limited to an initially slightly faster dissipation of the EAS- fraction in constantly wet soil relative to a variant with cyclic drying. For SDZ, laboratory results were thus generally transferable to the field situation and this may greatly facilitate the environmental risk assessment of sulfonamides. For DIF, we could show that its bioaccessibility constantly amounted to < 2% of the applied amount. Due to the strong sorption of DIF, its fate in soil was not controlled by climatic variables but likely by equilibrium exchanges with bound residues. As a result, the ASE-extractable DIF was highly persistent (DT50 290 d), though dissipation was again accelerated in the rhizosphere. Non-extractable residues of DIF formed at 60–65% of the applied amount. The fate of DIF was identical under all experimental conditions tested, i.e., we conclude that neither soil moisture nor soil temperature affect the behavior of DIF in soil. Instead, the very pronounced sorption of this compound to soil controlled its environmental fate, and likely also its effects.

Publications

• (2008): Analysis of aged sulfadiazine residues in soils using microwave extraction and liquid chromatography and tandem mass spectrometry. Analytical and Bioanalytical Chemistry 391, 1029–1038
  Förster, M, Laabs, V, Lamshöft, M, Pütz, T, Amelung, W
  
• (2009): Sequestration of Manure-Applied Sulfadiazine Residues in Soils. Environmental Science and Technology 43, 1824–1830
  Förster, M, Laabs, V, Lamshöft, M, Groeneweg, J, Zühlke, S, Spiteller, M, Krauss, M, Kaupenjohann, M, Amelung, W
  
• (2011). Dissipation and Sequestration of the Veterinary Antibiotic Sulfadiazine and Its Metabolites under Field Conditions. Environmental Science and Technology 45, 5216–5222
  Rosendahl, I, Siemens, J, Groeneweg, J, Linzbach, E, Laabs, V, Herrmann, C, Vereecken, H, Amelung, W
  
• (2011): Sequestration of sulfadiazine in soil, PhD thesis, 97 pages, University of Bonn
  Markus Förster
  
• (2012): Persistance of the Fluoroquinolone Antibiotic Difloxacin in Soil and Lacking Effects on Nitrogen Turnover. Journal of Environmental Quality 41, 1275–1283
  Rosendahl, I, Siemens, J, Kindler, R, Groeneweg, J, Zimmermann, J, Czerwinski, S, Lamshöft, M, Laabs, V, Wilke, BM, Vereecken, H, Amelung, W
  
• (2013): Abundance and transferability of antibiotic resistance as related to the fate of sulfadiazine in maize rhizosphere and bulk soil. FEMS Microbiology Ecology 83, 125–134
  Kopmann, C, Jechalke, S, Rosendahl, I, Groeneweg, J, Krögerrecklenfort, E, Zimmerling, U, Weichelt, V, Siemens, J, Amelung, W, Heuer, H, Smalla, K
  
• (2013): Effects of slurry from sulfadiazine (SDZ) and difloxacin (DIF) medicated pigs on the structural diversity of microorganisms in rhizosphere soil. Soil Biology and Biochemistry 62, 92–91
  Reichel, R, Rosendahl, I, Peeters, ETHM, Focks, A, Groeneweg, J, Bierl, R, Leinweber, P, Amelung, W, Thiele-Bruhn, S
  
• (2013): Increased Abundance and Transferability of Resistance Genes after Field Application of Manure from Sulfadiazine-Treated Pigs. Applied and Environmental Microbiology 79, 1704–1711
  Jechalke, S, Kopmann, C, Rosendahl, I, Groeneweg, J, Weichelt, V, Krögerrecklenfort, E, Brandes, N, Nordwig, M, Ding, GC, Siemens, J, Heuer, H, Smalla, K
  
• (2013): Short-term extractability of sulfadiazine after application to soils. Environmental Pollution 172, 180–185
  Müller, T, Rosendahl, I, Focks, A, Siemens, J, Klasmeier, J, Matthies, M
  
• (2014): Fate and effects of veterinary antibiotics in soil. Trends in Microbiology 22, 536-544
  Jechalke, S., Heuer, H., Siemens, J., Amelung, W., Smalla, K.
  
• (2014): Soil microbial community responses to antibiotic-contaminated manure under different soil moisture regimes. Applied Microbiology and Biotechnology 98, 6487-6495
  Reichel, R., Radl, V., Rosendahl, I., Albert, A., Amelung, W., Schloter, M., Theile-Bruhn, S.
  
• (2014): Soil microbial community responses to sulfadiazine-contaminated manure in different soil microhabitats. Applied Soil Ecology 80, 15-25
  Reichel, R., Patzelt, D., Barleben, C., Rosendahl, I., Ellerbrock, R., Thiele-Bruhn, S.
  
• (2014): Structural and functional response of the soil bacterial community to application of manure from difloxacin-treated pigs. FEMS Microbiology Ecology 87, 78-88
  Jechalke, S, Focks, A, Rosendahl, I, Groeneweg, J, Siemens, J, Heuer, H, Smalla, K
  
• (2012): Fate of the veterinary antibiotics sulfadiazine and difloxacin in soil, PhD thesis, 133 pages, University of Bonn
  Ingrid Rosendahl