Abstract
Fluoroquinolone (FQ) antibiotics are extensively used both in human and veterinary medicine, and their accumulation in the environment is causing an increasing concern. In this study, the biodegradation of the three most worldwide used FQs, namely ofloxacin, norfloxacin, and ciprofloxacin, by the fluoroorganic-degrading strain Labrys portucalensis F11 was assessed. Degradation occurred when the FQs were supplied individually or as mixture in the culture medium, in the presence of an easily degradable carbon source. Consumption of individual FQs was achieved at different extents depending on its initial concentration, ranging from 0.8 to 30 μM. For the lowest concentration, total uptake of each FQ was observed but stoichiometric fluoride release was not achieved. Intermediate compounds were detected and identified by LC-MS/MS with a quadrupole time of flight detector analyzer. Biotransformation of FQs by L. portucalensis mainly occurred through a cleavage of the piperazine ring and displacement of the fluorine substituent allowing the formation of intermediates with less antibacterial potency. FQ-degrading microorganisms could be useful for application in bioaugmentation processes towards more efficient removal of contaminants in wastewater treatment plants.
Similar content being viewed by others
References
Adjei MD, Deck J, Heinze TM, Freeman JP, Williams AJ, Sutherland JB (2007) Identification of metabolites produced from N-phenylpiperazine by Mycobacterium spp. J Ind Microbiol Biotechnol 34:219–224. doi:10.1007/s10295-006-0189-x
Adjei MD, Heinze TM, Deck J, Freeman JP, Williams AJ, Sutherland JB (2006) Transformation of the antibacterial agent norfloxacin by environmental mycobacteria. Appl Environ Microbiol 72:5790–5793. doi:10.1128/AEM.03032-05
Amorim CL, Carvalho MF, Afonso CMM, Castro PML (2013a) Biodegradation of fluoroanilines by the wild strain Labrys portucalensis. Int Biodeterior Biodegrad 80:10–15. doi:10.1016/j.ibiod.2013.02.001
Amorim CL, Ferreira ACS, Carvalho MF, Afonso CMM, Castro PML (2013b) Mineralization of 4-fluorocinnamic acid by a Rhodococcus strain. Appl Microbiol Biotechnol. doi:10.1007/s00253-013-5149-6
An T, Yang H, Song W, Li G, Luo H, Cooper WJ (2010) Mechanistic considerations for the advanced oxidation treatment of fluoroquinolone pharmaceutical compounds using TiO2 heterogeneous catalysis. J Phys Chem A 114:2569–2575. doi:10.1021/jp911349y
Babić S, Periša M, Skorić I (2013) Photolytic degradation of norfloxacin, enrofloxacin and ciprofloxacin in various aqueous media. Chemosphere 91:1635–1642. doi:10.1016/j.chemosphere.2012.12.072
Backhaus T, Scholze M, Grimme L (2000) The single substance and mixture toxicity of quinolones to the bioluminescent bacterium Vibrio fischeri. Aquat Toxicol 49:49–61. doi:10.1016/S0166-445X(99)00069-7
Brown KD, Kulis J, Thomson B, Chapman TH, Mawhinney DB (2006) Occurrence of antibiotics in hospital, residential, and dairy effluent, municipal wastewater, and the Rio Grande in New Mexico. Sci Total Environ 366:772–783. doi:10.1016/j.scitotenv.2005.10.007
Calza P, Medana C, Carbone F, Giancotti V, Baiocchi C (2008) Characterization of intermediate compounds formed upon photoinduced degradation of quinolones by high-performance liquid chromatography/high-resolution multiple-stage mass spectrometry. Rapid Commun Mass Spectrom 22:1533–1552. doi:10.1002/rcm
Carlesi Jara C, Fino D, Specchia V, Saracco G, Spinelli P (2007) Electrochemical removal of antibiotics from wastewaters. Appl Catal B 70:479–487. doi:10.1016/j.apcatb.2005.11.035
Carvalho MF, Ferreira Jorge R, Pacheco CC, De Marco P, Castro PML (2005) Isolation and properties of a pure bacterial strain capable of fluorobenzene degradation as sole carbon and energy source. Environ Microbiol 7:294–298. doi:10.1111/j.1462-2920.2004.00714.x
De Kreuk MK, Heijnen JJ, van Loosdrecht MCM (2005) Simultaneous COD, nitrogen and phosphate removal by aerobic granular sludge. Biotech Bioeng 90:761–769. doi:10.1002/bit.20470
Duque AF, Bessa VS, Carvalho MF, de Kreuk MK, van Loosdrecht MCM, Castro PML (2011) 2-Fluorophenol degradation by aerobic granular sludge in a sequencing batch reactor. Water Res 45:6745–6752. doi:10.1016/j.watres.2011.10.033
Egli T (2010) How to live at very low substrate concentration. Water Res 44:4826–4837. doi:10.1016/j.watres.2010.07.023
Fent K, Weston AA, Caminada D (2006) Ecotoxicology of human pharmaceuticals. Aquat Toxicol 76:122–159. doi:10.1016/j.aquatox.2005.09.009
Golet EM, Alder AC, Giger W (2002) Environmental exposure and risk assessment of fluoroquinolone antibacterial agents in wastewater and river water of the Glatt Valley Watershed, Switzerland. Environ Sci Technol 36:3645–3651. doi:10.1021/es0256212
Halling-Sørensen B, Sengeløv G, Ingerslev F, Jensen LB (2003) Reduced antimicrobial potencies of oxytetracycline, tylosin, sulfadiazin, streptomycin, ciprofloxacin, and olaquindox due to environmental processes. Arch Environ Contam Toxicol 44:7–16. doi:10.1007/s00244-002-1234-z
Hapeshi E, Fotiou I, Fatta-Kassinos D (2012) Sonophotocatalytic treatment of ofloxacin in secondary treated effluent and elucidation of its transformation products. Chem Eng J 224:96–105. doi:10.1016/j.cej.2012.11.048
Isidori M, Lavorgna M, Nardelli A, Pascarella L, Parrella A (2005) Toxic and genotoxic evaluation of six antibiotics on non-target organisms. Sci Total Environ 346:87–98. doi:10.1016/j.scitotenv.2004.11.017
Janssen DB, Dinkla IJT, Poelarends GJ, Terpstra P (2005) Bacterial degradation of xenobiotic compounds: evolution and distribution of novel enzyme activities. Environ Microbiol 7:1868–1882. doi:10.1111/j.1462-2920.2005.00966.x
Kim D-W, Heinze TM, Kim B-S, Schnackenberg LK, Woodling KA, Sutherland JB (2011) Modification of norfloxacin by a Microbacterium sp. strain isolated from a wastewater treatment plant. Appl Environ Microbiol 77:6100–6108. doi:10.1128/AEM.00545-11
Kovar K, Chaloupka V, Egli T (2002) A threshold substrate concentration is required to initiate the degradation of 3-phenylpropionic acid in Escherichia coli. Acta Biotechnol 22:285–298. doi:10.1002/1521-3846
Kümmerer K (2009) The presence of pharmaceuticals in the environment due to human use—present knowledge and future challenges. J Environ Manag 90:2354–2366. doi:10.1016/j.jenvman.2009.01.023
Kümmerer K, Al-Ahmad A, Mersch-Sundermann V (2000) Biodegradability of some antibiotics, elimination of the genotoxicity and affection of wastewater bacteria in a simple test. Chemosphere 40:701–710. doi:10.1016/S0045-6535(99)00439-7
Larsson DGJ, de Pedro C, Paxeus N (2007) Effluent from drug manufactures contains extremely high levels of pharmaceuticals. J Hazard Mater 148:751–755. doi:10.1016/j.jhazmat.2007.07.008
Li B, Zhang T (2010) Biodegradation and adsorption of antibiotics in the activated sludge process. Environ Sci Technol 44:3468–3473. doi:10.1021/es903490h
Lindberg RH, Olofsson U, Rendahl P, Johansson MI, Tysklind M, Andersson BA (2006) Behavior of fluoroquinolones and trimethoprim during mechanical, chemical, and active sludge treatment of sewage water and digestion of sludge. Environ Sci Technol 40:1042–1048. doi:10.1021/es0516211
Loh K-C, Yu Y-G (2000) Kinetics of carbazole degradation by Pseudomonas putida in presence of sodium salicylate. Water Res 34:4131–4138. doi:10.1016/S0043-1354(00)00174-3
Moreira IS, Amorim CL, Carvalho MF, Castro PML (2012a) Co-metabolic degradation of chlorobenzene by the fluorobenzene degrading wild strain Labrys portucalensis. Int Biodeterior Biodegrad 72:76–81. doi:10.1016/j.ibiod.2012.05.013
Moreira IS, Amorim CL, Carvalho MF, Castro PML (2012b) Degradation of difluorobenzenes by the wild strain Labrys portucalensis. Biodegrad 23:653–662. doi:10.1007/s10532-012-9541-1
Natarajan R, Azerad R, Badet B, Copin E (2005) Microbial cleavage of C-F bond. J Fluorine Chem 126:424–435. doi:10.1016/j.jfluchem.2004.12.001
Paul T, Dodd MC, Strathmann TJ (2010) Photolytic and photocatalytic decomposition of aqueous ciprofloxacin: transformation products and residual antibacterial activity. Water Res 44:3121–3132. doi:10.1016/j.watres.2010.03.002
Picó Y, Andreu V (2007) Fluoroquinolones in soil-risks and challenges. Anal Bioanal Chem 387:1287–1299. doi:10.1007/s00216-006-0843-1
Prieto A, Möder M, Rodil R, Adrian L, Marco-Urrea E (2011) Degradation of the antibiotics norfloxacin and ciprofloxacin by a white-rot fungus and identification of degradation products. Bioresour Technol 102:10987–10995. doi:10.1016/j.biortech.2011.08.055
Sukul P, Spiteller M (2007) Fluoroquinolone antibiotics in the environment. Rev Environ Contam Toxicol 191:131–162. doi:10.1007/978-0-387-69163-3_5
Vasconcelos TG, Henriques DM, König A, Martins AF, Kümmerer K (2009) Photo-degradation of the antimicrobial ciprofloxacin at high pH: identification and biodegradability assessment of the primary by-products. Chemosphere 76:487–493. doi:10.1016/j.chemosphere.2009.03.022
Wetzstein H, 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 65:1556–1563
Zhou NA, Lutovsky AC, Andaker GL, Gough HL, Ferguson JF (2013) Cultivation and characterization of bacterial isolates capable of degrading pharmaceutical and personal care products for improved removal in activated sludge wastewater treatment. Biodegrad. doi:10.1007/s10532-013-9630-9
Acknowledgments
C.L. Amorim, I.S. Moreira, and A.S. Maia wish to acknowledge a research grant from Fundação para a Ciência e Tecnologia (FCT), Portugal (ref. SFRH/BD/47109/2008, SFRH/BPD/87251/2012, and SFRH/BD/86939/2012, respectively) and Fundo Social Europeu (Programa Operacional Potencial Humano, Quadro de Referência Estratégico Nacional). This work was supported by FCT through the projects PTDC/EBB-EBI/111699/2009, CEQUIMED-Pest-OE/SAU/UI4040/2011, and PEst-OE/EQB/LA0016/2011.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 92 kb)
Rights and permissions
About this article
Cite this article
Amorim, C.L., Moreira, I.S., Maia, A.S. et al. Biodegradation of ofloxacin, norfloxacin, and ciprofloxacin as single and mixed substrates by Labrys portucalensis F11. Appl Microbiol Biotechnol 98, 3181–3190 (2014). https://doi.org/10.1007/s00253-013-5333-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-013-5333-8