Abstract
The global presence of antibiotics in the environment has created concerns about the emergence of antibiotic resistance bacteria and potential hazard to humans and the ecosystem. This work aims to study the removal of levofloxacin, a new generation fluoroquinolone antibiotic from aqueous solutions by enzyme mediated oxidation process and optimization of the conditions thereof by response surface methodology (RSM) using Box-Behnken design (BBD). For this study, experiments were conducted to analyze the effect of independent variables namely, pH, temperature, mediator concentration and antibiotic concentration on the degradation percentage of levofloxacin antibiotic using laccase enzyme derived from Trametes versicolor. The residual levofloxacin concentration was determined using high performance liquid chromatography (HPLC). On applying the quadratic regression analysis, among the main parameters, it was found that the percentage degradation was significantly affected by all the four variables. The predicted values for percentage degradation of levofloxacin were close to the experimental values obtained and the R2 (0.95) indicated that the regression was able to give a good prediction of response for the percentage degradation of levofloxacin in the studied range. The optimal conditions for the maximum degradation (99.9%) as predicted by the BBD were: temperature of 37 °C, pH of 4.5, mediator concentration of 0.1 mM and levofloxacin concentration of 5 μg mL−1. The findings of the study were further extended to study the effect of partially purified enzymes isolated from Pleurotus eryngii, Pleurotus florida and Pleurotus sajor caju on the degradation of levofloxacin at concentrations ranging from as low as 0.1 to as high as 50 µg mL−1 in synthetic wastewater utilizing the optimized conditions generated by BBD. A maximum degradation of 88.8% was achieved with the partially purified enzyme isolated from Pleurotus eryngii at 1 µg mL−1 levofloxacin concentration which was at par with the commercial laccase which showed 89% degradation in synthetic wastewater at the optimized conditions. The biodegradation studies were conducted using only 2 units of laccase. Thus, the expensive commercial laccase can be effectively replaced by crude laccase isolated from indigenous macrofungi such as P. eryngii, P. florida and P. sajor caju as a cost effective alternative to degrade levofloxacin present in contaminated wastewater using as low as 2 units of enzyme for a 72 h treatment period.
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References
Al-Musawi TJ, Kamani H, Bazrafshan E, Panahi AH, Silva MF, Abi G (2019) Optimization the effects of physicochemical parameters on the degradation of cephalexin in sono-Fenton reactor by using box-Behnken response surface methodology. J Catal Lett 149:1186–1196
Arca-Ramos A et al (2016) Assessing the use of nanoimmobilized laccases to remove micropollutants from wastewater. J Environ Sci Pollut Res 23:3217–3228
Asgher M, Noreen S, Bilal MJ (2017) Enhancement of catalytic, reusability, and long-term stability features of Trametes versicolor IBL-04 laccase immobilized on different polymers. J Intern J Biol Macromol 95:54–62
Ashrafi S, Nasseri S, Alimohammadi M, Mahvi A, Faramarzi MA (2016) Optimization of the enzymatic elimination of flumequine by laccase-mediated system using response surface methodology. J Desalin Water Treatment 57:14478–14487
Ayukekbong JA, Ntemgwa M, Atabe AN (2017) The threat of antimicrobial resistance in developing countries: causes and control strategies. J Antimicrob Res Infection Control 6(1):1-8
Balakrishna K, Rath A, Praveenkumarreddy Y, Guruge KS, Subedi B (2017) A review of the occurrence of pharmaceuticals and personal care products in Indian water bodies. J Ecotoxicol Environ Safety 137:113–120.
Becker D et al (2016) Removal of antibiotics in wastewater by enzymatic treatment with fungal laccase–degradation of compounds does not always eliminate toxicity. J Bioresour Technol 219:500–509
Boyd LB et al (2009) Relationships among ciprofloxacin, gatifloxacin, levofloxacin, and norfloxacin MICs for fluoroquinolone-resistant Escherichia coli clinical isolates. J Antimicrobial Agents Chemotherapy 53:229–234
Chaturvedi G, Kaur A, Umar A, Khan MA, Algarni H, Kansal SK (2020) Removal of fluoroquinolone drug, levofloxacin, from aqueous phase over iron based MOFs, MIL-100 (Fe). J Solid State Chem 281:121029
Chen Q, Xin Y, Zhu X (2015) Au-Pd nanoparticles-decorated TiO2 nanobelts for photocatalytic degradation of antibiotic levofloxacin in aqueous solution. J Electrochimica Acta 186:34–42
Dindaş GB, Çalışkan Y, Celebi EE, Tekbaş M, Bektaş N, Yatmaz HC (2020) Treatment of pharmaceutical wastewater by combination of electrocoagulation, electro-fenton and photocatalytic oxidation processes. J Environ Chem Eng 8:103777
Ding H et al (2016) Simultaneous removal and degradation characteristics of sulfonamide, tetracycline, and quinolone antibiotics by laccase-mediated oxidation coupled with soil adsorption. J Hazard Mat 307:350–358
Diwan V, Stalsby Lundborg C, Tamhankar AJ (2013) Seasonal and temporal variation in release of antibiotics in hospital wastewater: estimation using continuous and grab sampling. PLoS ONE 8:e68715. https://doi.org/10.1371/journal.pone.0068715
Diwan V et al (2010) Antibiotics and antibiotic-resistant bacteria in waters associated with a hospital in Ujjain India. BMC Public Health 10:414. https://doi.org/10.1186/1471-2458-10-414
Endimiani A, Brigante G, Bettaccini AA, Luzzaro F, Grossi P (2005) Toniolo AQJBid failure of levofloxacin treatment in community-acquired pneumococcal pneumonia. J BMC Infect Dis 5:1–4
Faramarzi MA, Forootanfar HJC, Biointerfaces SB (2011) Biosynthesis and characterization of gold nanoparticles produced by laccase from paraconiothyrium variabile. J Colloids Surfaces B Biointer 87:23–27
Foroughi M, Rahmani AR, Asgari G, Nematollahi D, Yetilmezsoy K (2018) Optimization of a three-dimensional electrochemical system for tetracycline degradation using box-behnken design. J Fresenius Environ Bull 27:1914–1922
Gholami-Borujeni F, Mahvi AH, Nasseri S, Faramarzi MA, Nabizadeh R, Alimohammadi M (2011) Enzymatic treatment and detoxification of acid orange 7 from textile wastewater. J Appl Biochem Biotechnol 165:1274–1284
Gothwal R, Shashidhar (2017) Occurrence of high levels of fluoroquinolones in aquatic environment due to effluent discharges from bulk drug manufacturers. J Hazard, Toxic, and Radioactive Waste 21 (3) 0501600.
Guerra P, Kim M, Shah A, Alaee M, Smyth SJ (2014) Occurrence and fate of antibiotic, analgesic/anti-inflammatory, and antifungal compounds in five wastewater treatment processes. J Sci Total Environ 473:235–243
Haaland PD (1989) Experimental design in biotechnology, vol 105. CRC Press
Hanna N et al (2018) Presence of antibiotic residues in various environmental compartments of Shandong province in eastern China: its potential for resistance development and ecological and human risk. J Environ Int 114:131–142
e Holanda FH et al (2019) Study of biodegradation of chloramphenicol by endophytic fungi isolated from Bertholletia excelsa (Brazil nuts). J Biocatal Agricul Biotechnol 20:101200
Kays MB, Smith DW, Wack MF (2002) Levofloxacin treatment failure in a patient with fluoroquinolone-resistant streptococcus pneumoniae pneumonia. J Pharmacother J Human Pharmacol Drug Therapy 22:395–399
Kurniawati S, Nicell JA (2008) Characterization of trametes versicolor laccase for the transformation of aqueous phenol. J Bioresour Technol 99:7825–7834
Larsson DJ (2014) Pollution from drug manufacturing: review and perspectives. J Philosz Trans Royal Soc B Biol Sci 369:20130571
Larsson DJ, de Pedro C, Paxeus N (2007) Effluent from drug manufactures contains extremely high levels of pharmaceuticals. J Hazard Mat 148:751–755
Lübbert C, Baars C, Dayakar A, Lippmann N, Rodloff AC, Kinzig M, Sörgel F (2017) Environmental pollution with antimicrobial agents from bulk drug manufacturing industries in Hyderabad, South India, is associated with dissemination of extended-spectrum beta-lactamase and carbapenemase-producing pathogens. J Infection 45:479–491
Lucas D, Badia-Fabregat M, Vicent T, Caminal G, Rodríguez-Mozaz S, Balcázar JL, Barceló D (2016) Fungal treatment for the removal of antibiotics and antibiotic resistance genes in veterinary hospital wastewater. J Chemosphere 152:301–308
Maezawa K, Yajima R, Terajima T, Kizu J, Hori S (2013) Dissolution profile of 24 levofloxacin (100 mg) tablets. J Infection Chem 19:996–998
Maia AS, Tiritan ME, Castro PM (2018) Enantioselective degradation of ofloxacin and levofloxacin by the bacterial strains Labrys portucalensis F11 and Rhodococcus sp FP1. J Ecotoxicol Environ Safety 155:144–151
Mathur P, Sanyal D, Dey P (2021) Optimization of growth conditions for enhancing the production of microbial laccase and its application in treating antibiotic contamination in wastewater. 3 Biotech 11:1–15
McGregor JC, Allen GP, Bearden DT (2008) Levofloxacin in the treatment of complicated urinary tract infections and acute pyelonephritis. Ther Clin Risk Manag 4:843
Mohapatra S, Huang CH, Mukherji S, Padhye LP (2016) Occurrence and fate of pharmaceuticals in WWTPs in India and comparison with a similar study in the United States. J Chemosphere 159:526–535
Morrissey I, Hoshino K, Sato K, Yoshida A, Hayakawa I, Bures MG (1996) Mechanism of differential activities of ofloxacin enantiomers. J Antimicrob Agents Chemotherapy 40:1775–1784
Mutiyar PK, Mittal AK (2014) Occurrences and fate of selected human antibiotics in influents and effluents of sewage treatment plant and effluent-receiving river Yamuna in Delhi (India). J Environ Monitoring Assess 186:541–557
Nasuhoglu D, Rodayan A, Berk D, Yargeau VJ (2012) Removal of the antibiotic levofloxacin (LEVO) in water by ozonation and TiO2 photocatalysis. Chem Eng J 189:41–48
Prieto A, Möder M, Rodil R, Adrian L (2011) Degradation of the antibiotics norfloxacin and ciprofloxacin by a white-rot fungus and identification of degradation products. J Bioresour Technol 102:10987–10995
Saadati N, Abdullah MP, Zakaria Z, Sany SBT, Rezayi M, Hassonizadeh HJ (2013) Limit of detection and limit of quantification development procedures for organochlorine pesticides analysis in water and sediment matrices. Chem Central J 7:63
Sawyer CN, McCarty PL, Parkin GF (2000) Chemistry for environmental engineering, 4th edn. Tata McGraw-Hill Publishing Company Limited, New York
Scoper SV (2008) Review of third-and fourth-generation fluoroquinolones in ophthalmology: in-vitro and in-vivo efficacy. J Advances in Therapy 25:979–994
Seok H, Kang CI, Huh K, Cho SY, Ha YE, Chung DR, Peck KR (2018) Risk factors for community-onset pneumonia caused by levofloxacin-nonsusceptible streptococcus pneumoniae. J Microbial Drug Res 24:1412–1416
Shah A, Shah MJ (2020) Characterisation and bioremediation of wastewater: a review exploring bioremediation as a sustainable technique for pharmaceutical wastewater. J Groundwater Sustain Devel 11:100383
Shao B, Liu Z, Zheng G, Liu Y, Yang X, Zhou C, Chen M, Liu Y, Jiang Y, Yan M (2019) Immobilization of laccase on hollow mesoporous carbon nanospheres: noteworthy immobilization, excellent stability and efficacious for antibiotic contaminants removal. J Hazard Mat 362:318–326
Sun Q, Li M, Ma C, Chen X, Xie X, Yu CP(2016) Seasonal and spatial variations of PPCP occurrence, removal and mass loading in three wastewater treatment plants located in different urbanization areas in Xiamen China. J Environ Poll 208:371–381
Torloni MR, Gomes Freitas C, Kartoglu U, Metin Gülmezoglu A (2016) Quality of oxytocin available in low-and middle-income countries: a systematic review of the literature. J BJOG Intern J Obstetrics Gynaecol 123:2076–2086
Verlicchi P, Al Aukidy M, Jelic A, Petrović M, Barceló DJ (2014) Comparison of measured and predicted concentrations of selected pharmaceuticals in wastewater and surface water: a case study of a catchment area in the Po Valley (Italy). J Sci Total Environ 470:844–854
Wang S-N et al (2018) An extracellular yellow laccase from white rot fungus Trametes sp F1635 and its mediator systems for dye decolorization. J Biochimie 148:46–54
Weng SS, Ku KL, Lai HT (2012) The implication of mediators for enhancement of laccase oxidation of sulfonamide antibiotics. J Bioresour Technology 113:259–264
Weng SS, Liu SM, Lai HT (2013) Application parameters of laccase–mediator systems for treatment of sulfonamide antibiotics. J Bioresour Technol 141:152–159
Widsten P, Kandelbauer A (2008) Laccase applications in the forest products industry: a review. J Enzyme Microbial Technol 42:293–307
Yang W-J, Griffiths PR, Byler DM (1985) Protein conformation by infrared spectroscopy: resolution enhancement by fourier self-deconvolution. J Appl Spectrosc 39:282–287
Zhang S, Wu Z, Chen G, Wang Z (2018) An improved method to encapsulate laccase from trametes versicolor with enhanced stability and catalytic activity. J Catalysts 8:286
Zhao R, Li X, Hu M, Li S, Zhai Q, Jiang Y (2017) Efficient enzymatic degradation used as pre-stage treatment for norfloxacin removal by activated sludge. J Bioprocess Biosys Eng 40:1261–1270
Acknowledgements
We thank The Director, Sustainable Agriculture Division, TERI Deakin Nanobiotechnology Centre, The Energy and Resources Institute, New Delhi for providing necessary facilities to carry out the research work. Special thanks are also extended to the supervisory panel members of TERI Deakin Nanobiotechnology Centre, The Energy and Resources Institute, New Delhi (Dr Pawan Kaur) and School of Life and Environmental Sciences, Burwood Campus, Deakin University Australia (Dr Damien Callahan, Dr Xavier Conlan and Dr Fred Pfeffer).
Funding
This work, which is part of Purvi Mathur’s doctoral thesis work, is jointly supported by the TERI Deakin Nanobiotechnology Centre, The Energy and Resources Institute, New Delhi and School of Life and Environmental Sciences, Deakin University, Australia.
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PM: Experimental work, data curation, writing sections of the original draft, DS: Conceptualization of the study, writing sections of the original draft, review and editing, PD: experimental template, review and editing.
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Mathur, P., Sanyal, D. & Dey, P. The optimization of enzymatic oxidation of levofloxacin, a fluoroquinolone antibiotic for wastetwater treatment. Biodegradation 32, 467–485 (2021). https://doi.org/10.1007/s10532-021-09946-x
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DOI: https://doi.org/10.1007/s10532-021-09946-x