Skip to main content
SpringerLink
Log in

Sulfadiazine Uptake and Effects on Salix fragilis L. and Zea mays L. Plants

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

Frequently, sulfonamide antibiotic agents reach arable soils via excreta of medicated livestock. In this study, accumulation and phytotoxicity indicators were analyzed to evaluate the effects of sulfonamides on plants. In a greenhouse experiment, willow (Salix fragilis L.) and maize (Zea mays L.) plants were grown for 40 days in soil spiked with 10 and 200 mg kg−1 sulfadiazine (SDZ). Distribution of SDZ and major metabolites among bulk and rhizosphere soil, roots, leaves, and stems was determined using accelerated solvent extraction and LC − MS/MS analysis. Accumulation of SDZ was stronger in willow. The antibiotic was mainly stored inside roots and 4-hydroxy-sulfadiazine presence increased with the administered SDZ concentration. SDZ altered root geotropism, increased the lateral root number, and affected plant water uptake. The high concentration caused serious stress in willow (e.g., reduced C/N ratio and total chlorophyll content) and the death of maize plants. Even at environmentally relevant soil concentrations (10 mg kg−1), SDZ exhibited adverse effects on root growth, while at artificially high concentrations (200 mg kg−1), it showed a strong potential to impair plant performance and biomass. Willow, a fast growing tree species, showed potential for possible phytoremediation purposes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

SDZ:

Sulfadiazine

dm:

Dry mass

fm:

Fresh mass

4-OH-SDZ:

4-hydroxy-sulfadiazine

5-OH-SDZ:

5-hydroxy-sulfadiazine

N-Ac-SDZ:

N-acetyl-sulfadiazine

References

  • Antignac, J., Le Bizec, B., Monteau, F., & Andre, F. (2003). Validation of analytical methods based on mass spectrometric detection according to the “2002/657/EC” European decision: guideline and application. Analytica Chimica Acta, 483, 325–334.

    Article  CAS  Google Scholar 

  • Aust, M., Godlinski, F., Travis, G. R., Hao, X., McAllister, T. A., Leinweber, P., et al. (2008). Distribution of sulfamethazine, chlortetracycline and tylosin in manure and soil of Canadian feedlots after subtherapeutic use in cattle. Environmental Pollution, 156, 1243–1251.

    Article  CAS  Google Scholar 

  • Barret, M. (1995). Metabolism of herbicides by cytochrome P450 in corn. Drug Metabolism and Drug Interactions, 12, 299–316.

    Article  Google Scholar 

  • Bialk, H. M., Simpson, A. J., & Pedersen, J. A. (2005). Cross-coupling of sulfonamide antimicrobial agents with model humic constituents. Environmental Science and Technology, 39, 4463–4473.

    Article  CAS  Google Scholar 

  • Boonsaner, M., & Hawker, D. W. (2010). Accumulation of oxytetracycline and norfloxacin from saline soil by soybeans. Sciences of the Total Environment, 408, 1731–1737.

    Article  CAS  Google Scholar 

  • Boonsirichai, K., Guan, C., Chen, R., & Masson, P. H. (2002). Root gravitropism: an experimental tool to investigate basic cellular and molecular processes underlying mechanosensing and signal transmission in plants. Annual Review of Plant Biology, 53, 421–447.

    Article  CAS  Google Scholar 

  • Boxall, A. B. A., Fogg, L. A., Blackwell, P. A., Blackwell, P., Kay, P., Pemberton, E. J., et al. (2004). Veterinary medicines in the environment. Reviews of Environmental Contamination and Toxicology, 180, 1–9.

    Article  CAS  Google Scholar 

  • Boxall, A. B. A., Johnson, P., Smith, E. J., Sinclair, C. J., Stutt, E., & Levy, L. S. (2006). Uptake of veterinary medicines from soils into plants. Journal of Agricultural and Food Chemistry, 54, 2288–2297.

    Article  CAS  Google Scholar 

  • Burken, J. G. (2003). Uptake and metabolism of organic compounds: green-liver model. In S. C. McCutcheon & J. L. Schnoor (Eds.), Phytoremediation: transformation and control of contaminants (pp. 59–84). Hoboken: Wiley.

    Google Scholar 

  • Chiou, C. T., Kile, D. E., Rutherford, D. W., Sheng, G., & Boyd, S. A. (2000). Sorption of selected organic compounds from water to a peat soil and its humic-acid and humin fractions: potential sources of the sorption nonlinearity. Environmental Science and Technology, 34, 1254–1258.

    Article  CAS  Google Scholar 

  • Christian, T., Schneider, R. J., Färber, H. A., Skutlarek, D., Meyer, M. T., & Goldbach, H. E. (2003). Determination of antibiotic residues in manure, soil, and surface waters. Acta Hydrochimica et Hydrobiologica, 31, 36–44.

    Article  CAS  Google Scholar 

  • De Liguoro, M., Poltronieri, C., Capolongo, F., & Montesissa, C. (2007). Use of sulfadimethoxine in intensive calf farming: evaluation of transfer to stable manure and soil. Chemosphere, 68, 671–676.

    Article  Google Scholar 

  • R Development Core Team (2008). R: a language and environment for statistical computing. RFoundation for Statistical Computing, Vienna. http://www.R-project.org.

  • Ding, C., & He, J. (2010). Effect of antibiotics in the environment on microbial populations. Applied Microbiology and Biotechnology, 87, 925–941.

    Article  CAS  Google Scholar 

  • Dolliver, H., Kumar, K., & Gupta, G. (2007). Sulfamethazine uptake by plants from manure-amended soil. Journal of Environmental Quality, 36, 1224–1230.

    Article  CAS  Google Scholar 

  • Ferro, S., Trentin, A. R., Caffieri, S., & Ghisi, R. (2010). Antibacterial sulfonamides: accumulation and effects in barley plants. Fresenius Environmental Bulletin, 19, 2094–2099.

    CAS  Google Scholar 

  • Förster, M., Laabs, V., Lamshöft, M., Pütz, T., & Amelung, W. (2008). Analysis of aged sulfadiazine residues in soils using microwave extraction and liquid chromatography tandem mass spectrometry. Analytical and Bioanalytical Chemistry, 391, 1029–1038.

    Article  Google Scholar 

  • Förster, M., Laabs, V., Lamshöft, M., Groeneweg, J., Zühlke, S., Spiteller, M., et al. (2009). Sequestration of manure-applied sulfadiazine residues in soils. Environmental Science and Technology, 43, 1824–1830.

    Article  Google Scholar 

  • Gerhardt, K. E., Huang, X., Glick, B. R., & Greenberg, B. M. (2009). Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Science, 176, 20–30.

    Article  CAS  Google Scholar 

  • Grote, M., Vockel, A., Schwarze, D., Mehlich, A., & Freitag, M. (2004). Fate of antibiotics in food chain and environment originating from pigfattening (part 1). Fresenius Environmental Bulletin, 13, 1216–1224.

    CAS  Google Scholar 

  • Grote, M., Schwake-Anduschus, C., Michel, R., Langenkämper, G., Betsche, T., Hayen, H., et al. (2007). Aufnahme und Transport von Tierarzneistoffen in Nutzpflanzen. In R. Röder, K. Weiß, & M. Sengl (Eds.), Tierarzneimittel in der Umwelt (pp. 161–173). Munich: Oldenbourg Industrieverlag.

    Google Scholar 

  • Halling-Sørensen, B., Nors Nielsen, S., Lanzky, P. F., Ingerslev, F., Holten Lützhøft, H. C., & Jørgensen, S. E. (1998). Occurrence, fate and effects of pharmaceutical substances in the environment—a review. Chemosphere, 36, 357–393.

    Article  Google Scholar 

  • Hammesfahr, U., Heuer, H., Manzke, B., Smalla, K., & 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.

    Article  CAS  Google Scholar 

  • Hamscher, G., Sczesny, S., Hoper, 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. Analytical Chemistry, 74, 1509–1518.

    Article  CAS  Google Scholar 

  • Hamscher, G., Pawelzick, H. T., Sczesny, S., Nau, H., & Hartung, J. (2003). Antibiotics in dust originating from a pig-fattening farm: a new source of health hazard for farmers? Environmental Health Perspectives, 111, 1590–1594.

    Article  CAS  Google Scholar 

  • Hölzel, C. S., Harms, K. S., Küchenhoff, H., Kunz, A., Müller, C., Meyer, K., et al. (2010). Phenotypic and genotypic bacterial antimicrobial resistance in liquid pig manure is variously associated with contents of tetracyclines and sulfonamides. Journal of Applied Microbiology, 108, 1642–1656.

    Article  Google Scholar 

  • Höper, H., Kues, H., Nau, H., & Hamscher, G. (2002). Eintrag und Verbleib von Tierarzneimittelwirkstoffen in Böden. Bodenschutz, 4, 141–148.

    Google Scholar 

  • Jjemba, P. K. (2002). The potential impact of veterinary and human therapeutic agents in manure and biosolids on plants grown on arable land: a review. Agriculture, Ecosystems and Environment, 93, 267–278.

    Article  Google Scholar 

  • Jørgensen, S. E., & Halling-Sørensen, B. (2000). Drugs in the environment. Chemosphere, 40, 691–699.

    Article  Google Scholar 

  • Kreuzig, R., & Höltge, S. (2005). Investigations on the fate of sulfadiazine in manured soil: laboratory experiments and test plot studies. Environmental Toxicology and Chemistry, 24, 771–776.

    Article  CAS  Google Scholar 

  • Kumar, K. (2005). Antibiotic use in agriculture and its impact on the terrestrial environment. Advances in Agronomy, 87, 1–54.

    Article  CAS  Google Scholar 

  • Kuzovkina, Y. A., & Quigley, M. F. (2005). Willows beyond wetlands: uses of Salix L. species for environmental projects. Water, Air and Soil Pollution, 162, 183–204.

    Article  CAS  Google Scholar 

  • Langhammer, J.-P., Führ, F., & Büning-Pfaue, H. (1990). Verbleib von Sulfonamid-Rückständen aus der Gülle in Boden und Nutzpflanze. Lebensmittelchemie, 44, 93.

    Google Scholar 

  • Li, Z., Alfenito, M., Rea, P. A., Walbot, V., & Dixon, R. A. (1997). Vacuolar uptake of the phytoalexin medicarpin by the glutathione conjugate pump. Phytochemistry, 45, 689–693.

    Article  CAS  Google Scholar 

  • Lichtenthaler, H. K. (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology, 148, 350–382.

    Article  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, 1636–1642.

    Article  CAS  Google Scholar 

  • Lynch, J. (1995). Root architecture and plant productivity. Plant Physiology, 109, 7–13.

    CAS  Google Scholar 

  • Marschner, P. (2012). Mineral nutrition of higher plants (thirdth ed., p. 651). San Diego: Academic.

    Google Scholar 

  • Michelini, L., Meggio, F., La Rocca, N., Ferro, S., & Ghisi, R. (2012). Accumulation and effects of sulfadimethoxine in Salix fragilis L. plants: a preliminary study to phytoremediation purposes. International Journal of Phytoremediation, 14, 388–402.

    Article  Google Scholar 

  • Migliore, L., Brambilla, G., Cozzolino, S., & Gaudio, L. (1995). Effect on plants of sulphadimethoxine used in intensive farming (Panicum miliaceum, Pisum sativum and Zea mays). Agriculture, Ecosystems and Environment, 52, 103–110.

    Article  CAS  Google Scholar 

  • Migliore, L., Brambilla, G., Casoria, P., Civitareale, C., Cozzolino, S., & Gaudio, L. (1996). Effect of sulphadimethoxine contamination on barley (Hordeum distichum L., Poaceae, Liliposida). Agriculture, Ecosystems and Environment, 60, 121–128.

    Article  CAS  Google Scholar 

  • Migliore, L., Civitareale, C., Cozzolino, S., Casoria, P., Brambilla, G., & Gaudio, L. (1998). Laboratory models to evaluate phytotoxicity of sulphadimethoxine on terrestrial plants. Chemosphere, 37, 2957–2961.

    Article  CAS  Google Scholar 

  • Migliore, L., Rotini, A., Cerioli, N. L., Cozzolino, S., & Fiori, M. (2010). Phytotoxic antibiotic sulfadimethoxine elicits a complex hormetic response in the weed Lythrum salicaria L. Dose–response, 8, 414–427.

    CAS  Google Scholar 

  • Mikes, O., & Trapp, S. (2010). Acute toxicity of the dissociating veterinary antibiotics trimethoprim to willow trees at varying pH. Bulletin of Environmental Contamination and Toxicology, 85, 556–561.

    Article  CAS  Google Scholar 

  • Pilon-Smits, E. (2005). Phytoremediation. Annual Review of Plant Biology, 56, 15–39.

    Article  CAS  Google Scholar 

  • Pressman, B. C., Harris, E. J., Jagger, W. S., & Johnson, J. H. (1967). Antibiotic-mediated transport of alkali ions across lipid barriers. Proceedings of the National Academy of Sciences of the United States of America, 58, 1949–1956.

    Article  CAS  Google Scholar 

  • Sarmah, A. K., Meyer, M. T., & Boxall, A. B. A. (2006). A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere, 65, 725–759.

    Article  CAS  Google Scholar 

  • Sartorius, M., Riccio, A., Cermola, M., Casoria, P., Patriarca, E. J., & Taté, R. (2009). Sulphadimethoxine inhibits Phaseolus vulgaris root growth and development of N-fixing nodules. Chemosphere, 76, 306–312.

    Article  CAS  Google Scholar 

  • Schachtman, D. P., & Schroeder, J. I. (1994). Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature, 370, 655–658.

    Article  CAS  Google Scholar 

  • Schmitt, H., Haapakangas, H., & 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.

    Article  CAS  Google Scholar 

  • Schwarz, J., Aust, M.-O., & Thiele-Bruhn, S. (2010). Metabolites from fungal laccase-catalysed transformation of sulfonamides. Chemosphere, 81, 1469–1476.

    Article  CAS  Google Scholar 

  • Stokstad, E. L. R., & Jukes, T. H. (1987). Sulfonamides and folic acid antagonists: a historical review. Journal of Nutrition, 117, 1335–1341.

    CAS  Google Scholar 

  • Sukul, P., & Spiteller, M. (2006). Sulfonamides in the environment as veterinary drugs. Reviews of Environmental Contamination and Toxicology, 187, 67–101.

    Article  CAS  Google Scholar 

  • Taiz, L., & Zeiger, E. (2009). Fisiologia vegetale (thirdth ed., p. 446). Padova: Piccin.

    Google Scholar 

  • Thiele-Bruhn, S. (2003). Pharmaceutical antibiotic compounds in soils—a review. Journal of Plant Nutrition and Soil Science, 166, 145–167.

    Article  CAS  Google Scholar 

  • Thiele-Bruhn, S., Seibicke, T., Schulten, H. R., & Leinweber, P. (2004). Sorption of sulfonamide pharmaceutical antibiotics on whole soils and particle-size fractions. Journal of Environmental Quality, 33, 1331–1342.

    Article  CAS  Google Scholar 

  • Trapp, S., & Karlson, U. (2001). Aspects of phytoremediation of organic pollutants. Journal of Soils and Sediments, 1, 37–43.

    Article  CAS  Google Scholar 

  • Trapp, S., Matthies, M., Scheunert, I., & Topp, E. M. (1990). Modeling the bioconcentration of organic chemicals in plants. Environmental Science and Technology, 28, 1246–1252.

    Article  Google Scholar 

  • Wehrhan, A., Streck, T., Groeneweg, J., Vereecken, H., & Kasteel, R. (2010). Long-term sorption and desorption of sulfadiazine in soil: experiments and modeling. Journal of Environmental Quality, 39, 654–666.

    Article  CAS  Google Scholar 

  • Zacchini, M., Pietrini, F., Scarascia Mugnozza, G., Iori, V., Pietrosanti, L., & Massacci, A. (2009). Metal tolerance, accumulation and translocation in poplar and willow clones treated with cadmium in hydroponics. Water, Air, and Soil Pollution, 197, 23–34.

    Article  CAS  Google Scholar 

  • Zayed, A., Gowthaman, S., & Terry, N. (1998). Phytoaccumulation of trace elements by wetlands plants: I. Duckweed. Journal of Environmental Quality, 27, 715–721.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was partly funded by a grant of “Ing. Aldo Gini” Foundation and through the financial support of Veneto Agricoltura Agency and of the German Research Foundation DFG. The support and assistance of M.-O. Aust, E. Sieberger, and P. Ziegler is highly appreciated. We thank B.-M. Wilke and two anonymous reviewers for valuable comments on the manuscript.

Author information

Authors and Affiliations

  1. D.A.F.N.A.E. Department, University of Padova, Agripolis, viale dell’Università 16, 35020, Legnaro, Padua, Italy

    L. Michelini & R. Ghisi

  2. Soil Science, Faculty of Geography/Geosciences, University of Trier, Behringstrasse 21, 54286, Trier, Germany

    R. Reichel & S. Thiele-Bruhn

  3. Geobotany, Faculty of Geography/Geosciences, University of Trier, Behringstrasse 21, 54286, Trier, Germany

    W. Werner

Authors
  1. L. Michelini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Reichel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. W. Werner
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. Ghisi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. Thiele-Bruhn
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. Michelini.

Electronic supplementary materials

Below is the link to the electronic supplementary material.

ESM 1

(DOC 10591 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Michelini, L., Reichel, R., Werner, W. et al. Sulfadiazine Uptake and Effects on Salix fragilis L. and Zea mays L. Plants. Water Air Soil Pollut 223, 5243–5257 (2012). https://doi.org/10.1007/s11270-012-1275-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11270-012-1275-5

Keywords

Search

Navigation