Biotransformation of the Antibiotic Danofloxacin by Xylaria longipes Leads to an Efficient Reduction of Its Antibacterial Activity

Journal of Agricultural and Food Chemistry

Volumn 63, Issue 31, 2015, Pages 6897-6904

  Rusch, Marina ^a   Kauschat, Annika ^a   Spielmeyer, Astrid ^a   Römpp, Andreas ^a   Hausmann, Heike ^a   Zorn, Holger ^a   Hamscher, Gerd ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

fluoroquinolone antibiotics; fungi; high resolution mass spectrometry; N oxidation; NMR

Indexed keywords

BIOCONVERSION; ENZYMES; FUNGI; MANURES; MASS SPECTROMETRY; METABOLITES; NUCLEAR MAGNETIC RESONANCE; SPECTROMETRY; VETERINARY MEDICINE;

ANTI-BACTERIAL ACTIVITY; BIOTRANSFORMATION PROCESS; FLUOROQUINOLONE ANTIBIOTICS; HIGH RESOLUTION MASS SPECTROMETRY; MICROBIAL BIOTRANSFORMATIONS; N-OXIDATION; SPECTROSCOPIC TECHNIQUE; TWO-DIMENSIONAL NUCLEAR MAGNETIC RESONANCE;

ANTIBIOTICS;

FUNGI; XYLARIA LONGIPES;

ANTIINFECTIVE AGENT; DANOFLOXACIN; QUINOLONE DERIVATIVE;

BIOREMEDIATION; BIOTRANSFORMATION; CHEMICAL STRUCTURE; CHEMISTRY; MASS SPECTROMETRY; METABOLISM; XYLARIALES;

ANTI-BACTERIAL AGENTS; BIODEGRADATION, ENVIRONMENTAL; BIOTRANSFORMATION; FLUOROQUINOLONES; MASS SPECTROMETRY; MOLECULAR STRUCTURE; XYLARIALES;

EID: 84938704832     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b02343     Document Type: Article

References (36)

1. Hooper, D. C. Mode of action of fluoroquinolones Drugs 1999, 58, 6-10 10.2165/00003495-199958002-00002
2. McGuirk, P. R.; Jefson, M. R.; Mann, D. D.; Elliott, N. C.; Chang, P.; Cisek, E. P.; Cornell, C. P.; Gootz, T. D.; Haskell, S. L.; Hindahl, M. S.; LaFleur, L. J.; Rosenfeld, M. J.; Shryock, T. R.; Silvia, A. M.; Weber, F. H. Synthesis and structure-activity relationships of 7-diazabicycloalkylquinolones, including danofloxacin, a new quinolone antibacterial agent for veterinary medicine J. Med. Chem. 1992, 35, 611-620 10.1021/jm00082a001
3. Federal Office for Consumer Protection and Food Safety.Dritte Datenerhebung zur Antibiotikaabgabe in der Tiermedizin; http://www.bvl.bund.de/DE/08-PresseInfothek/01-FuerJournalisten/01-Presse-und-Hintergrundinformationen/05-Tierarzneimittel/2014/2014-08-01-pi-Abgabemengen-korrigiert-29-08-2014.html;jsessionid=CA13CE12470E7E50A9FD2FEB86C112C9.2-cid322 (accessed May 2015).
4. World Health Organization. Critically important antimicrobialsfor human medicine; http://www.who.int/foodsafety/publications/antimicrobials-third/en/ (accessed May 2015).
5. Carlucci, G. Analysis of fluoroquinolones in biological fluids by high-performance liquid chromatography J. Chromatogr. A 1998, 812, 343-367 10.1016/S0021-9673(98)00274-X
6. Martinez, M.; McDermott, P.; Walker, R. Pharmacology of the fluoroquinolones: a perspective for the use in domestic animals Vet. J. 2006, 172, 10-28 10.1016/j.tvjl.2005.07.010
7. Boxall, A. B. A.; Johnson, P.; Smith, E. J.; Sinclair, C. J.; Stutt, E.; Levy, L. S. Uptake of veterinary medicines from soils into plants J. Agric. Food Chem. 2006, 54, 2288-2297 10.1021/jf053041t
8. Golet, E. M.; Alder, A. C.; Giger, W. Environmental exposure and risk assessment of fluoroquinolone antibacterial agents in wastewater and river water of the Glatt Valley Watershed, Switzerland Environ. Sci. Technol. 2002, 36, 3645-3651 10.1021/es0256212
9. Hamscher, G.; Mohring, S. A. I. Veterinary drugs in soil and in the aquatic environment Chem. Ing. Technol. 2012, 84, 1052-1061 10.1002/cite.201100255
10. Hamscher, G.; Pawelzick, H. T.; Sczesny, S.; Nau, H.; Hartung, J. Antibiotics in dust originating from a pig-fattening farm: a new source of health hazard for farmers? Environ. Health Perspect. 2003, 111, 1590-1594 10.1289/ehp.6288
11. Janusch, F.; Scherz, G.; Mohring, S. A. I.; Hamscher, G. Determination of fluoroquinolones in chicken feces-A new liquid-liquid extraction method combined with LC-MS/MS Environ. Toxicol. Pharmacol. 2014, 38, 792-799 10.1016/j.etap.2014.09.011
12. Selvam, A.; Zhao, Z.; Wong, J. W. C. Composting of swine manure spiked with sulfadiazine, chlortetracycline and ciprofloxacin Bioresour. Technol. 2012, 126, 412-417 10.1016/j.biortech.2011.12.073
13. Grote, M.; Schwake-Anduschus, C.; Michel, R.; Stevens, H.; Heyser, W.; Langenkämper, G.; Betsche, T.; Freitag, M. Incorporation of veterinary antibiotics into crops from manured soil Landbauforsch. Voelkenrode 2007, 57, 25-32
14. Amorim, C. L.; Moreira, I. S.; Maia, A. S.; Tiritan, M. E.; Castro, P. M. L. Biodegradation of ofloxacin, norfloxacin, and ciprofloxacin as single and mixed substrates by Labrys portucalensis F11 Appl. Microbiol. Biotechnol. 2014, 98, 3181-3190 10.1007/s00253-013-5333-8
15. Chen, Y.; Rosazza, J. P. N.; Reese, C. P.; Chang, H. Y.; Nowakowski, M. A.; Kiplinger, J. P. Microbial models of soil metabolism: biotransformations of danofloxacin J. Ind. Microbiol. Biotechnol. 1997, 19, 378-384 10.1038/sj.jim.2900409
16. Liu, Z.; Sun, P.; Pavlostathis, S. G.; Zhou, X.; Zhang, Y. Adsorption, inhibition, and biotransformation of ciprofloxacin under aerobic conditions Bioresour. Technol. 2013, 144, 644-651 10.1016/j.biortech.2013.07.031
17. Čvančarová, M.; Moeder, M.; Filipová, A.; Reemtsma, T.; Cajthaml, T. Biotransformation of the antibiotic agent flumequine by ligninolytic fungi and residual antibacterial activity of the transformation mixtures Environ. Sci. Technol. 2013, 47, 14128-14136 10.1021/es403470s
18. Parshikov, I. A.; Sutherland, J. B. Microbial transformations of antimicrobial quinolones and related drugs J. Ind. Microbiol. Biotechnol. 2012, 39, 1731-1740 10.1007/s10295-012-1194-x
19. Prieto, A.; Möder, M.; Rodil, R.; Adrian, L.; Marco-Urrea, E. Degradation of the antibiotics norfloxacin and ciprofloxacin by a white-rot fungus and identification of degradation products Bioresour. Technol. 2011, 102, 10987-10995 10.1016/j.biortech.2011.08.055
20. Gröger, D.; Schmauder, H. P. Microbial conversion of thebaine Experientia 1969, 25, 95-96 10.1007/BF01903920
21. Hofrichter, M.; Ullrich, R. Oxidations catalyzed by fungal peroxygenases Curr. Opin. Chem. Biol. 2014, 19, 116-125 10.1016/j.cbpa.2014.01.015
22. Hufford, C. D.; Capiton, G. A.; Clark, A. M.; Baker, J. K. Metabolism of imipramine by microorganisms J. Pharm. Sci. 1981, 70, 151-155 10.1002/jps.2600700209
23. Mitsukura, K.; Hayashi, M.; Yoshida, T.; Nagasawa, T. Oxidation of aromatic N-heterocyclic compounds to N-oxides by Verticillium sp. GF39 cells J. Biosci. Bioeng. 2013, 115, 651-653 10.1016/j.jbiosc.2012.12.002
24. Shibuya, H.; Kitamura, C.; Maehara, S.; Nagahata, M.; Winarno, H.; Simanjuntak, P.; Kim, H. S.; Wataya, Y.; Ohashi, K. Transformation of cinchona alkaloids into 1-N-oxide derivatives by endophytic Xylaria sp. isolated from Cinchona pubescens Chem. Pharm. Bull. 2003, 51, 71-74 10.1248/cpb.51.71
25. Siebers-Wolff, S.; Arfmann, H. A.; Abraham, W. R.; Kieslich, K. Microbiological hydroxylation and N-oxidation of cinchona alkaloids Biocatal. Biotransform. 1993, 8, 47-58 10.3109/10242429309030955
26. Colby, J.; Stirling, D. I.; Dalton, H. The soluble methane mono-oxygenase of Methylococcus capsulatus (Bath) Biochem. J. 1977, 165, 395-402
27. Ullrich, R.; Dolge, C.; Kluge, M.; Hofrichter, M. Pyridine as novel substrate for regioselective oxygenation with aromatic peroxygenase from Agrocybe aegerita FEBS Lett. 2008, 582, 4100-4106 10.1016/j.febslet.2008.11.006
28. Fraatz, M. A.; Naeve, S.; Hausherr, V.; Zorn, H.; Blank, L. M. A minimal growth medium for the basidiomycete Pleurotus sapidus for metabolic flux analysis. Fungal Biol. Biotechnol. 2014, 1, 10.1186/s40694-014-0009-4.
29. European Commission. Commission Regulation(EU) No. 37/2010on pharmacologically active substances and their classification regardingmaximum residue limits in foodstuffs of animal origin; ec.europa.eu/health/files/eudralex/vol-5/reg-2010-37/reg-2010-37-en.pdf (accessed May 2015).
30. Liu, Z. Y.; Zhou, X. N.; Zhang, H. H.; Wan, L.; Sun, Z. L. An integrated method for degradation products detection and characterization using hybrid ion trap/time-of-flight mass spectrometry and data processing techniques: Application to study of the degradation products of danofloxacin under stressed conditions Anal. Bioanal. Chem. 2011, 399, 2475-2486 10.1007/s00216-010-4629-0
31. Chattah, A. K.; Linck, Y. G.; Monti, G. A.; Levstein, P. R.; Breda, S. A.; Manzo, R. H.; Olivera, M. E. NMR and IR characterization of the aluminium complexes of norfloxacin and ciprofloxacin fluoroquinolones Magn. Reson. Chem. 2007, 45, 850-859 10.1002/mrc.2058
32. Jones, I. C.; Sharman, G. J.; Pidgeon, J. 1H and 13C NMR data to aid the identification and quantitation of residual solvents by NMR spectroscopy Magn. Reson. Chem. 2005, 43, 497-509 10.1002/mrc.1578
33. White, L. O.; MacGowan, A. P.; Lovering, A. M.; Reeves, D. S.; Mackay, I. G. A preliminary report on the pharmacokinetics of ofloxacin, desmethyl ofloxacin and ofloxacin N-oxide in patients with chronic renal failure Drugs 1987, 34, 56-61 10.2165/00003495-198700341-00013
34. Venezia, R. A.; Prymas, L. A.; Shayegani, A.; Yocum, D. M. In vitro activities of amifloxacin and two of its metabolites Antimicrob. Agents Chemother. 1989, 33, 762-766 10.1128/AAC.33.5.762
35. Čvančarová, M.; Moeder, M.; Filipová, A.; Cajthaml, T. Biotransformation of fluoroquinolone antibiotics by ligninolytic fungi-metabolites, enzymes and residual antibacterial activity Chemosphere 2015, 136, 311-320 10.1016/j.chemosphere.2014.12.012
36. Palmer, A. C.; Angelino, E.; Kishony, R. Chemical decay of an antibiotic inverts selection for resistance Nat. Chem. Biol. 2010, 6, 105-107 10.1038/nchembio.289