Skip to main content

Advertisement

SpringerLink
Log in

Antibiotika als Umweltkontaminanten — Effekte auf Bodenbakterien

Antibiotics as environmental pollutants: Effects on soil microorganisms

  • Fortschritte in Ökotoxikologie & Umweltchemie
  • Published:
Umweltwissenschaften und Schadstoff-Forschung Submit manuscript

Zusammenfassung

Ziel und Absicht

Die Umweltauswirkungen des Gebrauchs von Arzneimitteln und insbesondere Antibiotika sind nur unvollständig untersucht. In diesem Beitrag wird ausgewählte Literatur zum Thema besprochen. Weiter wird eine Zusammenfassung von Ergebnissen eigener Arbeiten zu Effekten von Antibiotika in Boden-Mikrokosmen gegeben.

Methoden, Ergebnisse und Schlussfolgerungen

Im Mittelpunkt steht die Methode der ‘pollution-induced community tolerance’ (PICT), mit der untersucht wird, ob Antibiotika zu Verschiebungen in der Artenzusammensetzung von bakteriellen Gemeinschaften und damit zu einer erhöhten Toleranz der Gemeinschaft führen. Die hier besprochenen PICT-Experimente beruhen auf der Veratmung von organischen Substraten in Multititerplatten (Biolog Platten). Andere besprochene Methoden sind funktionelle Tests, wie die Bodenrespiration, und molekulare Analysen, wie der Nachweis von Resistenzgenen in der DNA der Bodenorganismen. Die Eignung der PICT-Methode als ökotoxikologisches Effektmaß war Gegenstand mehrerer Experimente. Dabei wurde deutlich, dass die Effekttestung von Antibiotika die Gabe von Nährstoffen erfordert, und dass die PICT-Methode Antibiotikaeffekte spezifisch abbilden kann. Mit der PICT-Methode wurden daraufhin die Effekte von drei verschiedenen Antibiotikaklassen untersucht, und bei Konzentrationen von Tetrazyklinen, wie sie in der Umwelt auftreten können, erste Effekte festgestellt. Mögliche Risiken des Antibiotikaeinsatzes für die Verbreitung von Antibiotika-Resistenzgenen in der Umwelt sind noch nicht abschliessend zu bewerten, was bauptsächlich an der Rolle des natürlichen Hintergrundes an Resistenzgenen liegt.

Empfehlungen und Ausblick

Die PICT-Methode hat sich durch ihre Spezifizität als brauchbare ökotoxikologische Untersuchungsmethode erwiesen. Aufgrund der möglichen Effekte von Tetrazyklin-Antibiotika auf die Struktur der Bakteriengemeinschaft wird zu einem vorsichtigen Umgang mit Antibiotika in der landwirtschaftlichen Praxis geraten. Wir empfehlen, die Risiken eines erhöhten Auftretens von Antibiotika-Resistenz in der Umwelt genauer zu untersuchen.

Abstract

Goal and scope

Among the human and veterinary pharmaceuticals, antibiotics form an important group. Recent research addressed the environmental ‘side effects’ of antibiotics. Evidence for environmental effects of antibiotics has for example been found for the respiratory activity of soil microorganisms. In the present contribution, results of studies on the ecotoxicology of antibiotics that are based on the utilization of carbon substrates in so-called Biolog plates are summarized.

Methods, Results and Conclusions

The method of pollution-induced community tolerance (PICT) takes centre stage. PICT is based on the changes in community composition of environmental communities brought about by a toxicant, which lead to an overall increase in community tolerance to this toxicant. The suitability of such an increase in community tolerance as ecotoxicological endpoint had been the subject of several experiments. It was shown that effect testing of antibiotics requires supplementation of the communities with nutrients, and that the PICT method reveals antibiotic effects with a high specificity. In an application of PICT, effects of three classes of antibacterial compounds were investigated. Dose-response relationships were obtained for all substances, and effect concentrations were partly in the range of expected environmental concentrations. The possible risks of antibiotic use for an increase in the occurrence of antibiotic resistance genes in the environment are also touched upon, including the extent of natural resistance.

Outlook

Due to its specificity, the PICT method has shown to be a suitable ecotoxicological assay. Due to possible effects of tetracyclines on the structure of the soil microbial community, it is advised to use veterinary antibiotics with caution. The risks of an increase in the occurrence of antibiotic resistance in the environment should be investigated in more detail.

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

Literatur

  • Anonymus (2000): Leitlinien für den sorgfältigen Umgang mit antimikrobiell wirksamen Tierarzneimitteln — Mit Erläuterungen, Bundestierärztekammer (BTK), Arbeitsgemeinschaft der Leitenden Veterinärbeamten (ArgeVet)

  • Agersø Y, Sengeløv G, Jensen LB (2004): Development of a rapid method for direct detection of tet(M) genes in soil from Danish farmland. Environ Int 30, 117–122

    Article  Google Scholar 

  • Amann RI, Ludwig W, Schleifer KH (1995): Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59, 143–169

    CAS  Google Scholar 

  • Aminov RI, Chee-Sanford JC, Garrigues N, Teferedegne B, Krapac IJ, White BA, Mackie RI (2002): Development, validation, and application of PCR primers for detection of tetracycline efflux genes of gram-negative bacteria. Appl Environ Microb 68, 1786–1793

    Article  CAS  Google Scholar 

  • Bååth E, Díaz-Raviña M, Frostegård Å, Campbell C (1998): Effect of metalrich sludge amendments on the soil microbial community. Appl Environ Microb 64, 238–245

    Google Scholar 

  • Backhaus T, Froehner K, Altenburger R, Grimme LH (1997): Toxicity testing withVibrio fischeri: A comparison between the long term (24 h) and the short term (30 min) assay. Chemosphere 12, 2925–2938

    Article  Google Scholar 

  • Biolog (2000): Biolog eco plate — Microbial community analysis. Biolog, Hayward

    Google Scholar 

  • Blackwell PA, Lützhoft HC, Ma HP, Halling-Sørensen B, Boxall A, Kay P (2004): Fast and robust simultaneous determination of three veterinary antibiotics in groundwater and surface water using a tandem solid-phase extraction with high-performance liquid chromatography-UV detection. J Chromatogr A 1045, 111–117

    Article  CAS  Google Scholar 

  • Blanck H (2002): A critical review of procedures and approaches used for assessing pollution-induced community tolerance (PICT) in biotic communities. Hum Ecol Risk Assess 8, 1003–1034

    Article  Google Scholar 

  • Blanck H, Admiraal W, Cleven RF, Guasch H, van den Hoop MA, Ivorra N, Nystrom B, Paulsson M, Petterson RP, Sabater S, Tubbing GM (2003): Variability in zinc tolerance, measured as incorporation of radio-labeled carbon dioxide and thymidine, in periphyton communities sampled from 15 European river stretches. Arch Environ Contam Toxicol 44, 17–29

    Article  CAS  Google Scholar 

  • Blanck H, Wängberg S-Å, Molander S (1988): Pollution-induced community tolerance — A new ecotoxicological tool. In: Cairns J, Pratt JR (Hrsg), Functional testing of aquatic biota for estimating hazards of chemicals, Vol STP 988. American Society for Testing and Materials, Philadelphia, PA, USA, 219–230

    Chapter  Google Scholar 

  • Bloem J, Breure AM (2003): Microbial indicators. In: Markert BA, Breure AM, Zechmeister HG (Hrsg), Bioindicators and biomonitors, Vol 6. Elsevier, Amsterdam, 259–282

    Chapter  Google Scholar 

  • Boivin M-E, Breure AM, Posthuma L, Rutgers M (2002): Determination of field effects of contaminants — Significance of pollution-induced community tolerance. Hum Ecol Risk Assess 8, 1035–1055

    Article  Google Scholar 

  • Boivin M-E, Massieux B, Breure AM, van den Enden FP, Greve GD, Rutgers M, Admiraal W (2005): Effect of copper and temperature on aquatic bacterial communities. Aquat Toxicol 71, 345–356

    Article  CAS  Google Scholar 

  • Boleas S, Alonso C, Pro J, Babin MM, Fernandez C, Carbonell G, Tarazona JV (2005): Effects of sulfachlorpyridazine in MS.3-arable land: A multispecies soil system for assessing the environmental fate and effects of veterinary medicines. Environ Toxicol Chem 24, 811–819

    Article  CAS  Google Scholar 

  • Boxall AB, Fogg LA, Blackwell PA, Kay P, Pemberton EJ, Croxford A (2004): Veterinary medicines in the environment. Rev Environ Contam Toxicol 180, 1–91

    Article  CAS  Google Scholar 

  • Boxall ABA, Blackwell P, Cavallo R, Kay P, Tolls J (2002): The sorption and transport of a sulphonamide antibiotic in soil systems. Toxicol Lett 131, 19–28

    Article  CAS  Google Scholar 

  • Brandt KK, Jørgensen NOG, Nielsen TH, Winding A (2004): Microbial community-level toxicity testing of linear alkyl sulfonates in aquatic microcosms. FEMS Microbiol Ecol 49, 229–241

    Article  CAS  Google Scholar 

  • Chee-Sanford JC, Aminov RI, Krapac IJ, Garrigues-Jeanjean N, Mackie RI (2001): Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine production facilities. Appl Environ Microb 67, 1494–1502

    Article  CAS  Google Scholar 

  • Chopra I, Roberts M (2001): Tetracycline Antibiotics: Mode of Action, Applications, Molecular Biology, and Epidemiology of Bacterial Resistance. Microbiol Mol Biol Rev 65, 232–260

    Article  CAS  Google Scholar 

  • D’Costa VM, McGrann KM, Hughes DW, Wright GD (2006): Sampling the antibiotic resistome. Science 311, 374–377

    Article  Google Scholar 

  • Díaz-Raviña M, Bååth E, Frostegård Å (1994): Multiple heavy metal tolerance of soil bacterial communities and its measurement by a thymidine incorporation technique. Appl Environ Microb 60, 2238–2247

    Google Scholar 

  • Engelen B, Meinken K, von Wintzingerode F, Heuer H, Malkomes H-P, Backhaus H (1998): Monitoring impact of a pesticide treatment on bacterial soil communities by metabolic and genetic fingerprinting in addition to conventional testing procedures. Appl Environ Microb 64, 2814–2821

    CAS  Google Scholar 

  • FAO/OIE/WHO (2003): Second Joint FAO/OIE/WHO Expert Workshop on Non-Human Antimicrobial Usage and Antimicrobial Resistance: Management options, FAO/OIE/WHO, Geneva

  • Fernández C, Alonso C, Babin MM, Pro J, Carbonell G, Tarazona JV (2004): Ecotoxicological assessment of doxycycline in aged pig manure using multispecies soil systems. Sci Total Environ 323, 63–69

    Article  Google Scholar 

  • Froehner K, Backhaus T, Grimme LH (2000): Bioassays with Vibrio fischeri for the assessment of delayed toxicity. Chemosphere 40, 821–828

    Article  CAS  Google Scholar 

  • Garland JL (1996): Analytical approaches to the characterization of samples of microbial communities using patterns of potential C source utilization. Soil Biol Biochem 28, 213–221

    Article  CAS  Google Scholar 

  • Garland JL, Mills AL (1991): Classification and characterisation of heterotrophic microbial communities on the basis of pattern of communitylevel sole-carbon-source utilization. Appl Environ Microb 57, 2351–2359

    Google Scholar 

  • Haack SK, Garchow H, Klug MJ, Forney LJ (1995): Analysis of factors affecting the accurancy, reproducibiliby, and interpretation of microbial community carbon source utilization patterns. Applied environmental microbiology 61, 1458–1468

    CAS  Google Scholar 

  • Haller MY, Müller SR, McArdell CS, Alder AC, Suter MJ-F (2002): Quantification of veterinary antibiotics (sulfonamides and trimethoprim) in animal manure by liquid chromatography — Mass spectrometry. J Chrom A 952, 111–120

    Article  CAS  Google Scholar 

  • Halling-Sørensen B, Nors Nielsen S, Lanzky PF, Ingerslev F, Holten Lützhøft HC, Jørgensen SE (1998): Occurrence, fate and effects of pharmaceutical substances in the Environment — A review. Chemosphere 36, 357–393

    Article  Google Scholar 

  • Hamscher G, Pawelzick HT, Höper H, Nau H (2005): Different behaviour of tetracyclines and sulfonamides in sandy soils after repeated fertilization with liquid manure. Environ Toxicol Chem 24, 861–868

    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 

  • Hirsch R, Ternes T, Haberer K, Kratz K-L (1999): Occurrence of antibiotics in the aquatic environment. The Science of the Total Environment 225, 109–118

    Article  CAS  Google Scholar 

  • Hund-Rinke K, Simon M, Lukow T (2004): Effects of tetracycline on the soil microflora: Function, diversity, resistance. JSS-J Soils & Sediments 4, 11–16

    Article  CAS  Google Scholar 

  • Kay P, Blackwell PA, Boxall AB (2004): Fate of veterinary antibiotics in a macroporous tile drained clay soil. Environ Toxicol Chem 23, 1136–1144

    Article  CAS  Google Scholar 

  • Knacker T, Duis K, Ternes T, Fenner K, Escher B, Schmitt H, Römbke J, Garric J, Hutchinson T, Boxall ABA (2005): The EU-project ERAPharm. Incentives for the further development of guidance documents? ESPR-Environ Sci & Pollut Res 12, 62–65

    Article  Google Scholar 

  • Knight BP, McGrath S, Chaudri AM (1997): Biomass carbon measurements and substrate utilization patterns of microbial populations from soils amended with cadmium, copper, or zinc. Appl Environ Microb 63, 39–43

    CAS  Google Scholar 

  • Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD, Barber LB, Buxton HT (2002): Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999–2000: A national reconnaissance. Environ Sci Technol 36, 1202–1211

    Article  CAS  Google Scholar 

  • Kümmerer K (2001) Pharmaceuticals in the environment: Sources, fate, effects and risks, Vol. Springer-Verlag, Berlin

    Google Scholar 

  • Kümmerer K, Alexy R, Hüttig J, Schöll A (2004): Standardized tests fail to assess the effects of antibiotics on environmental bacteria. Water Res 38, 2111–2116

    Article  Google Scholar 

  • Muyzer G (1999): DGGE/TGGE a method for identifying genes from natural ecosystems. Curr Opin Microbiol 2, 317–322

    Article  CAS  Google Scholar 

  • Perreten V, Boerlin P (2003): A new sulfonamide resistance gene (sul3) in Escherichia coli is widespread in the pig population of Switzerland. Antimicrob Agents Chemother 47, 1169–1172

    Article  CAS  Google Scholar 

  • Preston-Mafham J, Boddy L, Randerson PF (2002): Analysis of microbial community functional diversity using sole-carbon-source utilisation profiles — A critique. FEMS Microbiol Ecol 42, 1–14

    CAS  Google Scholar 

  • Rasmussen LD, Sørensen SJ (2001): Effects of mercury contamination on the culturable heterotrophic, functional and genetic diversity of the bacterial community in soil. FEMS Microbiol Ecol 36, 1–9

    Article  CAS  Google Scholar 

  • Roberts MC, Sutcliffe J, Courvalin P, Jensen LB, Rood J, Seppala H (1999): Nomenclature for Macrolide and Macrolide-Lincosamide Streptogramin B Resistance Determinants. Antimicrob Agents Chemother 43, 2823–2830

    CAS  Google Scholar 

  • Röling WFM, van Breukelen BM, Braster M, Goeltom MT, Groen J, van Verseveld HW (2000): Analysis of microbial communities in a landfill leachate polluted aquifer using a new method for anaerobic physiological profiling and 16S rDNA based fingerprinting. Microb Ecol 40, 177–188

    Google Scholar 

  • Rutgers M, Breure AM, Insam H (2006): 8.4. Substrate utilisation in Biolog plates for analysis of CLPP. In: Bloem J, Hopkins DW, Benedetti A (Hrsg), Microbiological Methods for Assessing Soil Quality. CAB International, Wallingford, UK, pp 212–227

    Google Scholar 

  • Rutgers M, van’t Verlaat IM, Wind B, Posthuma L, Breure AM (1998): Rapid method for assessing pollution-induced community tolerance in contaminated soil. Environ Toxicol Chem 17, 2210–2213

    Article  Google Scholar 

  • Sacher F, Stoks PG (2003): Pharmaceutical residues in waters in the Netherlands. Report NO. ISBN: 90-6683-106-5, RIWA — Vereniging van Rivierwaterbedrijven, Nieuwegein

    Google Scholar 

  • Schloss PD, Handelsman J (2004): Status of the Microbial Census. Microbiol Mol Biol Rev 68, 686–691

    Article  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 Biol Biochem 37, 1882–1892

    Article  CAS  Google Scholar 

  • Schmitt H, Martinali B, van Beelen P, Seinen W (2006): On the limits of toxicant-induced tolerance testing: co-tolerance and response variation of antibiotic effects. Environmental Toxicology & Chemistry 25, in press

  • Schmitt H, Stoob K, Hamscher G, Smit E, Seinen W (im Druck): Tetracyclines and tetracycline resistance in agricultural soils — Microcosm and field studies. Microb Ecol

  • Schmitt H, van Beelen P, Tolls J, van Leeuwen CJ (2004): Pollution-induced community tolerance of soil microbial communities caused by the antibiotic sulfachloropyridazine. Environ Sci Technol 38, 1148–1153

    Article  CAS  Google Scholar 

  • Sköld O (2000): Sulfonamide resistance: mechanisms and trends. Drug Resistance Updates 3, 155–160

    Article  Google Scholar 

  • Sköld O (2001): Resistance to trimethoprim and sulfonamides. Veterinary Research 32, 261–273

    Article  Google Scholar 

  • Smalla K, Wachtendorf U, Heuer H, Liu W-T, Forney L (1998): Analysis of BIOLOG GN substrate utilization patterns by microbial communities. Appl Environ Microb 64, 1220–1225

    CAS  Google Scholar 

  • Soldo D, Behra R (2000): Long-term effects of copper on the structure of freshwater periphyton communities and their tolerance to copper, zinc, nickel and silver. Aquat Toxicol 47, 181–189

    Article  CAS  Google Scholar 

  • Thiele S, Beck I-C (2001): Wirkungen pharmazeutischer Antibiotika auf die Bodenmikroflora — Bestimmung mittels ausgewählter bodenbiologischer Testverfahren. Mitteilungen der deutschen Bodenkundlichen Gesellschaft 96, 383–384

    Google Scholar 

  • Thiele-Bruhn S (2003): Pharmaceutical antibiotic compounds in soils — A review. J Plant Nutr Soil Sci 166, 145–167

    Article  CAS  Google Scholar 

  • Thiele-Bruhn S (2005): Microbial inhibition by pharmaceutical antibiotics in different soils — Dose-response relations determined with the iron(III) reduction rest. Environ Toxicol Chem 24, 869–876

    Article  CAS  Google Scholar 

  • Tolls J (2001): Sorption of veterinary pharmaceuticals — A review. Environ Sci Technol 35, 3397–2406

    Article  CAS  Google Scholar 

  • Torsvik V, Goksøyr J, Daae FL (1990): High diversity in DNA of soil bacteria. Appl Environ Microb 56, 782–787

    CAS  Google Scholar 

  • Torsvik V, Ovreas L (2002): Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5, 240–245

    Article  CAS  Google Scholar 

  • Vaclavik E, Halling-Sorensen B, Ingerslev F (2004): Evaluation of manometric respiration tests to assess the effects of veterinary antibiotics in soil. Chemosphere 56, 667–676

    Article  CAS  Google Scholar 

  • VANTURES (2004): MARAN-2004 — Monitoring of antimicrobial resistance and antibiotic usage in animals in The Netherlands in 2004, VANTURES, The Hague

    Google Scholar 

  • Walsh C (2003) Antibiotics: Actions, origins, resistance. ASM Press, Washington DC

    Google Scholar 

  • Westergaard K, Müller AK, Christensen S, Bloem J, Sørensen SJ (2001): Effects of tylosin as a disturbance on the soil microbial community. Soil Biol Biochem 33, 2061–2071

    Article  CAS  Google Scholar 

  • WHO (2001): Global Strategy for Containment of Antimicrobial Resistance, Report No. WHO/CDS/CSR/DRS/2001.2a, World Health Organisation

Download references

Author information

Authors and Affiliations

  1. IRAS, Utrecht University, PO Box 80176, 3508 TD, Utrecht, Niederlande

    Heike Schmitt, Bennie Martinali & Willem Seinen

  2. National Institute for Public Health and the Environment (RIVM), PO Box 1, 3720 BA, Bilthoven, Niederlande

    Heike Schmitt, Bennie Martinali, Patrick van Beelen & Eric Smit

  3. EAWAG, Uberlandstrasse 133, 8600, Dubendorf, Schweiz

    Krispin Stoob

  4. Institut für Lebensmitteltoxikologie, Stiftung Tierärztliche Hochschule Hannover, Bischofsholer Damm 15, 30173, Hannover

    Gerd Hamscher

  5. Institute for Health and Consumer Protection, TP 202, 21020, Ispra (Varese), Italien

    Kees van Leeuwen

Authors
  1. Heike Schmitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bennie Martinali
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Krispin Stoob
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gerd Hamscher
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Patrick van Beelen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eric Smit
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kees van Leeuwen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Willem Seinen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Heike Schmitt.

Additional information

Dr. Heike Schmitt hat 2005 den mit 3000 Euro dotierten Nachwuchspreis der SETAC-German Language Branch gewonnen (vgl. Kammann et al. 2005, UWSF, 17, 254–255) und wurde eingeladen, auf Grundlage Ihrer kumulativen Promotion den vorliegenden Beitrag zu verfassen.

In dem neuen Beitragstyp ‘Fortschritte in Ökotoxikologie & Umweltchemie’ können Befunde aus mehreren eigenen peer reviewed englischsprachigen Originalarbeiten mit einem zusätzlichen internationalen Literaturreview kritisch zusammengefasst und so einem breiteren deutschsprachigen Publikum vorgestellt werden. Dieser Beitragstyp dient insbesondere der Vorstellung kumulativer Doktorarbeiten und der Ergebnisse von größeren Verbundprojekten.

OnlineFirst: 10. April, 2006

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schmitt, H., Martinali, B., Stoob, K. et al. Antibiotika als Umweltkontaminanten — Effekte auf Bodenbakterien. UWSF - Z Umweltchem Ökotox 18, 110–118 (2006). https://doi.org/10.1065/uwsf2006.04.118

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1065/uwsf2006.04.118

Schlagwörter

Keywords

Search

Navigation