Applied Microbiology and Biotechnology

, Volume 71, Issue 1, pp 90–100 | Cite as

Patterns of metabolites produced from the fluoroquinolone enrofloxacin by basidiomycetes indigenous to agricultural sites

Applied Microbial and Cell Physiology

Abstract

Supernatants of mycelial cultures of seven basidiomycetous fungi indigenous to agricultural sites were evaluated for metabolites generated from the veterinary fluoroquinolone enrofloxacin (EFL) by employing high–performance liquid chromatography/high–resolution electrospray ionization mass spectrometry. From exact masses, molecular formulae were derived, and the most probable chemical structures were deduced. Patterns of major metabolites were surprisingly similar but differed greatly from that provided by Gloeophyllum striatum due to the absence of monohydroxylated EFL congeners and a greater variety of metabolites with a modified piperazine moiety. The structures of three metabolites were elucidated by 1H–nuclear magnetic resonance spectroscopy. Of 61 compounds detected, 48 were new, while 13 were known from a pattern of 87 EFL metabolites identified for G. striatum. Ethylpiperazine moieties carrying oxido, hydroxy, oxo, and acetoxy groups, or showing partial degradation, were linked to the unmodified, oxidatively decarboxylated, or multiply hydroxylated core of EFL and to isatin– and anthranilic acid–type EFL congeners. Cleavage of the fluoro–aromatic bond was observed for two, 14CO2 formation for six species. Metabolites with a hydroxylated aromatic part implied subsequent ring cleavage to be brought about by the formation of potentially four oxidizable ortho–aminophenol– and one catechol–type intermediates. EFL degradation appears to be a common activity among basidiomycetes.

References

  1. Boxall ABA, Kolpin DW, Halling-Sørensen B, Tolls J (2003) Are veterinary medicines causing environmental risks? Environ Sci Technol 37:286A–294APubMedCrossRefGoogle Scholar
  2. Chen Y, Rosazza JPN, Reese CP, Chang H-Y, Nowakowski MA, Kiplinger JP (1997) Microbial models of soil metabolism: biotransformations of danofloxacin. J Ind Microbiol Biotechnol 19:378–384CrossRefPubMedGoogle Scholar
  3. Dalhoff A, Bergan T (1998) Pharmacokinetics of fluoroquinolones in experimental animals. In: Kuhlmann J, Dalhoff A, Zeiler H-J (eds) Quinolone antibacterials. Springer, Berlin Heidelberg New York, pp 179–206Google Scholar
  4. Field JA (2003) Biodegradation of chlorinated compounds by white rot fungi. In: Häggblom MM, Bossert ID (eds) Dehalogenation. Microbial processes and environmental applications. Kluwer, Boston, pp 159–204Google Scholar
  5. Greene CE, Budsberg SC (1993) Veterinary use of quinolones. In: Hooper DC, Wolfson JS (eds) Quinolone antimicrobial agents, 2nd edn. American Society for Microbiology, Washington, DC, pp 473–488Google Scholar
  6. Gollet EM, Xifra I, Siegrist H, Alder AC, Giger W (2003) Environmental exposure assessment of fluoroquinolone antibacterial agents from sewage to soil. Environ Sci Technol 37:3243–3249CrossRefPubMedGoogle Scholar
  7. Hawksworth DL, Kirk PM, Sutton BC, Pegler DN (1995) Ainsworth & Bisby’s dictionary of the fungi, 8th edn. International Mycological Institute. CAB, WallingfordGoogle Scholar
  8. Kramer C, Kreisel G, Fahr K, Käβbohrer J, Schlosser D (2004) Degradation of 2-fluorophenol by the brown-rot fungus Gloeophyllum striatum: evidence for the involvement of extracellular Fenton chemistry. Appl Microbiol Biotechnol 64:387–395CrossRefGoogle Scholar
  9. Kümmerer K (2004) Resistance in the environment. J Antimicrob Chemother 54:311–320CrossRefPubMedGoogle Scholar
  10. Levi S (1992) The antibiotic paradox: how miracle drugs are destroying the miracle. Plenum, New YorkGoogle Scholar
  11. Midtvedt T (1990) Resistance situation of oral antibiotics in the Scandinavian countries with special reference to the fluoro-quinolones. Scand J Infect Dis 68(Suppl):S7–S13Google Scholar
  12. Murphy CD (2003) New frontiers in biological halogenation. J Appl Microbiol 94:539–548CrossRefPubMedGoogle Scholar
  13. Parshikov IA, Freeman JP, Lay JO Jr, Beger RD, Williams AJ, Sutherland JB (2000) Microbial transformation of enrofloxacin by the fungus Mucor ramannianus. Appl Environ Microbiol 66:2664–2667CrossRefPubMedGoogle Scholar
  14. Parshikov IA, Heinze TM, Moody JD, Freeman JP, Williams AJ, Sutherland JB (2001) The fungus Pestalotiopsis guepini as a model for biotransformation of ciprofloxacin and norfloxacin. Appl Microbiol Biotechnol 56:474–477CrossRefPubMedGoogle Scholar
  15. Ralph JP, Catcheside DEA (2002) Biodegradation by white-rot fungi. In: Osiewacz HD (ed) The mycota, vol X. Springer, Berlin Heidelberg New York, pp 303–326Google Scholar
  16. Scheer M, de Jong A, Froyman R, Heinen E (1997) Antimicrobial activity in the digestive tract of broiler chickens treated orally with enrofloxacin. J Vet Pharmacol Ther 20(Suppl 1):201–202Google Scholar
  17. Schlosser D, Höfer C (2002) Laccase-catalyzed oxidation of Mn2+ in the presence of natural Mn3+ chelators as a novel source of extracellular H2O2 production and its impact on manganese peroxidase. Appl Environ Microbiol 68:3514–3521CrossRefPubMedGoogle Scholar
  18. Sommer C, Bibby BM (2002) The influence of veterinary medicines on the decomposition of dung organic matter in soil. Eur J Soil Biol 38:155–159CrossRefGoogle Scholar
  19. Stadler M, Wollweber H, Mühlbauer A, Henkel T, Asakawa Y, Hashimoto T, Ju Y-M, Rogers JD, Wetzstein H-G, Tichy H-V (2001) Secondary metabolite profiles, genetic fingerprints and taxonomy of Daldinia and allies. Mycotaxon 77:379–429Google Scholar
  20. Stalpers JA (1978) Identification of wood-inhabiting Aphyllophorales in pure culture. Studies in mycology, no 16. Centraalbureau voor Schimmelcultures, Baarn, The NetherlandsGoogle Scholar
  21. Wetzstein H-G, Schmeer N, Karl W (1997) Degradation of the fluoroquinolone enrofloxacin by the brown rot fungus Gloeophyllum striatum: identification of metabolites. Appl Environ Microbiol 63:4272–4281PubMedGoogle Scholar
  22. Wetzstein H-G, Stadler M, Tichy H-V, Dalhoff A, Karl W (1999) Degradation of ciprofloxacin by basidiomycetes and identification of metabolites generated by the brown rot fungus Gloeophyllum striatum. Appl Environ Microbiol 65:1556–1563PubMedGoogle Scholar
  23. Wetzstein H-G, Anderson JPE (2000) Degradation potential for the veterinary fluoroquinolone enrofloxacin is present in 33 agricultural soils sampled on 5 continents. In: Anderson JPE, Arthur MF, Leake CR, et al (Advisory Group to SETAC Europe, eds) Pesticides, soil microbiology and sustainable agriculture. Scientific program and abstracts of the 3rd international symposium on environmental aspects of pesticide microbiology. Theissen, Monheim am Rhein, pp 74–75Google Scholar
  24. Wicklow DT (1992) The coprophilous fungal community: an experimental system. In: Carrol GC, Wicklow DT (eds) The fungal community. Its organization and role in the ecosystem, 2nd edn. Dekker, New York, pp 715–728Google Scholar
  25. Wiuff C, Lykkesfeldt J, Aarestrup FM, Svendsen O (2002) Distribution of enrofloxacin in intestinal tissue and contents of healthy pigs after oral and intramuscular administration. J Vet Pharmacol Ther 25:335–342CrossRefPubMedGoogle Scholar
  26. Wood TM, Garcia-Campayo V (1994) Enzymes and mechanisms involved in microbial cellulolysis. In: Ratledge C (ed) Biochemistry of microbial degradation. Kluwer, Dordrecht, pp 197–231Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Animal Health DivisionBayer HealthCare AGLeverkusenGermany
  2. 2.Bayer CropScience AGMonheim am RheinGermany
  3. 3.Bayer Industry Services GmbH & Co. OHGLeverkusenGermany

Personalised recommendations