Advertisement

Utilization of naproxen by Amycolatopsis sp. Poz 14 and detection of the enzymes involved in the degradation metabolic pathway

  • B. M. Alanis-Sánchez
  • S. M. Pérez-Tapia
  • S. Vázquez-Leyva
  • I. Mejía-Calvo
  • Z. Macías-Palacios
  • L. Vallejo-Castillo
  • C. M. Flores-Ortiz
  • C. Guerrero-Barajas
  • J. A. Cruz-Maya
  • J. Jan-RobleroEmail author
Original Paper
First Online:

Abstract

The pollution of aquatic environments by drugs is a problem for which scarce research has been conducted in regards of their removal. Amycolatopsis sp. Poz 14 presents the ability to biotransformation naphthalene at high efficiency, therefore, in this work this bacterium was proposed as an assimilator of naproxen and carbamazepine. Growth curves at different concentrations of naproxen and carbamazepine showed that Amycolatopsis sp. Poz 14 is able to utilize these drugs at a concentration of 50 mg L−1 as a source of carbon and energy. At higher concentrations, the bacterial growth was inhibited. The transformation kinetics of naproxen showed the total elimination of the compound in 18 days, but carbamazepine was only eliminated in 19.9%. The supplementation with cometabolites such as yeast extract and naphthalene (structure similar to naproxen) at 50 mg L−1, showed that the yeast extract shortened the naproxen elimination to 6 days and reached a higher global consumption rate compared to the naphthalene cometabolite. The biotransformation of carbamazepine was not improved by the addition of cometabolites. The partial sequencing of the genome of Amycolatopsis sp. Poz 14 detected genes encoding putative enzymes for the degradation of cyclic aromatic compounds and the activities of aromatic monooxygenase, catechol 1,2-dioxygenase and gentisate 1,2-dioxygenase exhibited their involving in the naproxen biodegradation. The HPLC–MS analysis detected the 5-methoxysalicylic acid at the end of the biotransformation kinetics. This work demonstrates that Amycolatopsis sp. Poz 14 utilizes naproxen and transforms it to 5-methoxysalicylic acid which is the initial compound for the catechol and gentisic acid metabolic pathway.

Keywords

Naproxen Carbamazepine Amycolatopsis 5-Methoxysalicylic acid Catechol Gentisic acid 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

Chromatographic analysis performed with the equipment of “Laboratorio Nacional para Servicios Especializados de Investigación, Desarrollo e Innovación (I + D + i) para Farmoquímicos y Biotecnológicos”, LANSEIDI-FarBiotec-CONACyT, which is part of Unidad de Desarrollo e Investigación en Bioprocesos (UDIBI)-IPN” are gratefully acknowledged. BMAS thanks the support of the Consejo Nacional de Ciencia y Tecnología (CONACyT) for the scholarship grant for master’s degree, also the authors wish to acknowledge the financial support provided by the Instituto Politécnico Nacional (IPN) México Grant SIP20195543. Finally, CGB, JACM and JJR appreciate the COFAA and EDI, IPN fellowships, and support from the SNI-CONACyT.

Supplementary material

11274_2019_2764_MOESM1_ESM.tif (97.3 mb)
Supplementary material 1—Growth curve of Amycolatopsis sp. Poz 14 with cometabolites in mineral medium supplemented with naproxen (a) and carbamazepine (b). Both cometabolites were added at 50 mg L-1 (TIF 99,622 kb)
11274_2019_2764_MOESM2_ESM.tif (97.4 mb)
Supplementary material 2—Kinetics of biotransformation of carbamazepine by Amycolatopsis sp. Poz 14 in mineral medium with the addition of naphthalene or yeast extract (YE) at 50 mg L-1. Determination of the kinetics of carbamazepine and growth by the consortium was carried out at an initial concentration of 50 mg L-1 and evaluated every 3 days until 18 days at 30ºC and 100 rpm in cometabolic culture using 50 mg L-1 of naphthalene (a) or YE (b). Data presented in the graph are the mean and standard error of 3 independent assays. (TIF 99,730 kb)
11274_2019_2764_MOESM3_ESM.tif (2.1 mb)
Supplementary material 3—Absence of naproxen at the end of the degradation kinetics by Amycolatopsis sp. Poz 14. Initial kinetic (down) and final kinetic (up) total ion counting (TIC) chromatograms of naproxen, obtained by MS, were compared. It was observed that naproxen amounts were totally degraded. (TIF 2,145 kb)
11274_2019_2764_MOESM4_ESM.tif (1.5 mb)
Supplementary material 4—Retention time of 5-methoxysalicylic acid during the degradation kinetic of naproxen by Amycolatopsis sp. Poz 14. The presence of 5-methoxysalicylic acid was corroborated by extracting its characteristic m/z signal from total m/z acquired data. 214.08, 273.17 and 357.17 m/z signals were extracted from total m/z signal acquired from the MS analysis of initial (down) and final (up) cell culture degradation of naproxen. Analyzed signals were assigned to one main peak at 2.79 min (TIF 1,567 kb)

References

  1. Aracagök YD, Göker H, Cihangir N (2017) Biodegradation of micropollutant naproxen with a selected fungal strain and identification of metabolites. Z Naturforsch C 72(5–6):173–179.  https://doi.org/10.1515/znc-2016-0162 CrossRefPubMedGoogle Scholar
  2. Aus der Beek T, Weber FA, Bergmann A, Hickmann S, Ebert I, Hein A, Küster A (2016) Pharmaceuticals in the environment—global occurrences and perspectives. Environ Toxicol Chem 35(4):823–835.  https://doi.org/10.1002/etc.3339 CrossRefPubMedGoogle Scholar
  3. Bamforth SM, Singleton I (2005) Bioremediation of polycyclic aromatic hydrocarbons: Current knowledge and future directions (Review). J Chem Technol Biotechnol 80(7):723–736.  https://doi.org/10.1002/jctb.1276 CrossRefGoogle Scholar
  4. Bessa VS, Moreira IS, Tiritan ME, Castro PML (2017) Enrichment of bacterial strains for the biodegradation of diclofenac and carbamazepine from activated sludge. Int Biodeter Biodegr 120:135–142.  https://doi.org/10.1016/j.ibiod.2017.02.008 CrossRefGoogle Scholar
  5. Cai Z, Chen Q, Wang H, He Y, Wang W, Zhao X, Ye Q (2012) Degradation of the novel herbicide ZJ0273 by Amycolatopsis sp. M3-1 isolated from soil. Appl Microbiol Biotechnol 96(5):1371–1379.  https://doi.org/10.1007/s00253-011-3867-1 CrossRefPubMedGoogle Scholar
  6. Chaillan F, Le Flèche A, Bury E, Phantavong YH, Grimont P, Saliot A, Oudot J (2004) Identification and biodegradation potential of tropical aerobic hydrocarbon-degrading microorganisms. Res Microbiol 155(7):587–595.  https://doi.org/10.1016/j.resmic.2004.04.006 CrossRefPubMedGoogle Scholar
  7. Corcoran J, Winter MJ, Tyler CR (2010) Pharmaceuticals in the aquatic environment: a critical review of the evidence for health effects in fish. Crit Rev Toxicol 40(4):287–304.  https://doi.org/10.3109/10408440903373590 CrossRefPubMedGoogle Scholar
  8. Cycoń M, Mrozik A, Piotrowska-Seget Z (2019) Antibiotics in the soil environment-degradation and their impact on microbial activity and diversity. Front Microbiol 10:338.  https://doi.org/10.3389/fmicb.2019.00338 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Divari S, Valetti F, Caposio P, Pessione E, Cavaletto M, Griva E, Gribaudo G, Gilardi G, Giunta C (2003) The oxygenase component of phenol hydroxylase from Acinetobacter radioresistens S13. Eur J Biochem 270(10):2244–2253.  https://doi.org/10.1046/j.1432-1033.2003.03592.x CrossRefPubMedGoogle Scholar
  10. Domaradzka D, Guzik U, Hupert-Kocurek K, Wojcieszyńska D (2015a) Cometabolic degradation of naproxen by Planococcus sp. strain S5. Water Air Soil Pollut 226(9):297.  https://doi.org/10.1007/s11270-015-2564-6 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Domaradzka D, Guzik U, Wojcieszyńska D (2015b) Biodegradation and biotransformation of polycyclic non-steroidal anti-inflammatory drugs. Rev Environ Sci Biotechnol 14(2):229–239.  https://doi.org/10.1007/s11157-015-9364-8 CrossRefGoogle Scholar
  12. Feng Y, Khoo HE, Poh CL (1999) Purification and characterization of gentisate 1,2-dioxygenases from Pseudomonas alcaligenes NCIB 9867 and Pseudomonas putida NCIB 9869. Appl Environ Microbiol 65(3):946–950PubMedPubMedCentralGoogle Scholar
  13. Gauthier H, Yargeau V, Cooper DG (2010) Biodegradation of pharmaceuticals by Rhodococcus rhodochrous and Aspergillus niger by co-metabolism. Sci Total Environ 408(7):1701–1706.  https://doi.org/10.1016/j.scitotenv.2009.12.012 CrossRefPubMedGoogle Scholar
  14. Ghafghazi S, Moini Zanjani T, Vosough M, Sabetkasaei M (2017) Interference-free determination of carbamazepine in human serum using high performance liquid chromatography: a comprehensive research with three-way calibration methods. Iran J Pharm Res 16(1):120–131PubMedPubMedCentralGoogle Scholar
  15. Górny D, Guzik U, Hupert-Kocurek K, Wojcieszyńska D (2019a) A new pathway for naproxen utilisation by Bacillus thuringiensis B1(2015b) and its decomposition in the presence of organic and inorganic contaminants. J Environ Manage 239:1–7.  https://doi.org/10.1016/j.jenvman.2019.03.034 CrossRefPubMedGoogle Scholar
  16. Górny D, Guzik U, Hupert-Kocurek K, Wojcieszyńska D (2019b) Naproxen ecotoxicity and biodegradation by Bacillus thuringiensis B1(2015b) strain. Ecotoxicol Environ Saf 167:505–512.  https://doi.org/10.1016/j.ecoenv.2018.10.067 CrossRefPubMedGoogle Scholar
  17. Guerrero-Barajas C, Alanís-Sánchez B, Flores-Ortiz C, Cruz-Maya J, Jan-Roblero J (2019) Enhanced removal of methyl tert-butyl ether by yeast extract supplementation to a bacterial consortium. Rev Mex Ing Quim 18(2):589–604.  https://doi.org/10.24275/uam/izt/dcbi/revmexingquim/2019v18n2/Guerrero CrossRefGoogle Scholar
  18. Hou CT, Lillard MO, Schwartz RD (1976) Protocatechuate 3, 4-dioxygenase from Acinetobacter calcoaceticus. Biochemistry 15(3):582–588CrossRefGoogle Scholar
  19. 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(6):1202–1211.  https://doi.org/10.1021/es011055j CrossRefPubMedGoogle Scholar
  20. Lu Z, Sun W, Li C, Ao X, Yang C, Li S (2019) Bioremoval of non-steroidal anti-inflammatory drugs by Pseudoxanthomonas sp. DIN-3 isolated from biological activated carbon process. Water Res 161:459–472.  https://doi.org/10.1016/j.watres.2019.05.065 CrossRefPubMedGoogle Scholar
  21. Marco-Urrea E, Pérez-Trujillo M, Blánquez P, Vicent T, Caminal G (2010) Biodegradation of the analgesic naproxen by Trametes versicolor and identification of intermediates using HPLC-DAD-MS and NMR. Bioresource Technol 101(7):2159–2166.  https://doi.org/10.1016/j.biortech.2009.11.019 CrossRefGoogle Scholar
  22. Marchlewicz A, Domaradzka D, Guzik U, Wojcieszyńska D (2016) Bacillus thuringiensis B1(2015b) is a Gram-positive bacterium able to degrade naproxen and ibuprofen. Water Air Soil Pollut 227:197.  https://doi.org/10.1007/s11270-016-2893-0 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Ortega-González DK, Martinez-González G, Flores CM, Zaragoza D, Cancino-Diaz JC, Cruz-Maya JA, Jan-Roblero J (2015) Amycolatopsis sp. Poz14 isolated from oil-contaminated soil degrades polycyclic aromatic hydrocarbons. Int Biodeterior Biodegrad.  https://doi.org/10.1016/j.ibiod.2015.01.008 CrossRefGoogle Scholar
  24. Péry AR, Gust M, Vollat B, Mons R, Ramil M, Fink G, Ternes T, Garric J (2008) Fluoxetine effects assessment on the life cycle of aquatic invertebrates. Chemosphere 73(3):300–304.  https://doi.org/10.1016/j.chemosphere.2008.06.029 CrossRefPubMedGoogle Scholar
  25. Pinto PI, Estêvão MD, Power DM (2014) Effects of estrogens and estrogenic disrupting compounds on fish mineralized tissues. Mar Drugs 12(8):4474–4494.  https://doi.org/10.3390/md12084474 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Popa C, Favier L, Dinica R, Semrany S, Djelal H, Amrane A, Bahrim G (2014) Potential of newly isolated wild Streptomyces strains as agents for the biodegradation of a recalcitrant pharmaceutical, carbamazepine. Environ Technol 35(21–24):3082–3091.  https://doi.org/10.1080/09593330.2014.931468 CrossRefPubMedGoogle Scholar
  27. Rodríguez-Rodríguez CE, Marco-Urrea E, Caminal G (2010) Degradation of naproxen and carbamazepine in spiked sludge by slurry and solid-phase Trametes versicolor systems. Bioresour Technol 101(7):2259–2266.  https://doi.org/10.1016/j.biortech.2009.11.089 CrossRefPubMedGoogle Scholar
  28. Serralheiro A, Alves G, Fortuna A, Rocha M, Falcão A (2013) First HPLC-UV method fo rapid and simultaneous quantification of phenobarbital, primidone, phenytoin, carbamazepine, carbamazepine-10,11-epoxide, 10,11-trans-dihydroxy-10,11-dihydrocarbamazepine, lamotrigine, oxcarbazepine and licarbazepine in human plasma. J Chromatogr B 925:1–9.  https://doi.org/10.1016/j.jchromb.2013.02.026 CrossRefGoogle Scholar
  29. Ternes TA (1998) Occurrence of drugs in German sewage treatment plants and rivers. Water Res 32:3245–3260.  https://doi.org/10.1016/S0043-1354(98)00099-2 CrossRefGoogle Scholar
  30. Thelusmond JR, Strathmann TJ, Cupples AM (2016) The identification of carbamazepine biodegrading phylotypes and phylotypes sensitive to carbamazepine exposure in two soil microbial communities. Sci Total Environ 571:1241–1252.  https://doi.org/10.1016/j.scitotenv.2016.07.154 CrossRefPubMedGoogle Scholar
  31. Tokiwa Y, Jarerat A (2004) Biodegradation of poly(l-lactide). Biotechnol Lett 26:771.  https://doi.org/10.1023/B:BILE.0000025927.31028.e3 CrossRefPubMedGoogle Scholar
  32. Vulava VM, Cory WC, Murphey VL, Ulmer CZ (2016) Sorption, photodegradation, and chemical transformation of naproxen and ibuprofen in soils and water. Sci Total Environ 565:1063–1070.  https://doi.org/10.1016/j.scitotenv.2016.05.132 CrossRefPubMedGoogle Scholar
  33. Wang L, Peng Y, Nie X, Pan B, Ku P, Bao S (2016) Gene response of CYP360A, CYP314, and GST and whole-organism changes in Daphnia magna exposed to ibuprofen. Comp Biochem Physiol C 179:49–56.  https://doi.org/10.1016/j.cbpc.2015.08.010 CrossRefGoogle Scholar
  34. Wojcieszyńska D, Guzik U, Greń I, Perkosz M, Hupert-Kocurek K (2011) Induction of aromatic ring: cleavage dioxygenases in Stenotrophomonas maltophilia strain KB2 in cometabolic systems. World J Microbiol Biotechnol 27(4):805–811.  https://doi.org/10.1007/s11274-010-0520-6 CrossRefPubMedGoogle Scholar
  35. Wojcieszyńska D, Domaradzka D, Hupert-Kocurek K, Guzik U (2014) Bacterial degradation of naproxen—undisclosed pollutant in the environment. J Environ Manage 145:157–161.  https://doi.org/10.1016/j.jenvman.2014.06.023 CrossRefPubMedGoogle Scholar
  36. Wojcieszyńska D, Domaradzka D, Hupert-Kocurek K, Guzik U (2016) Enzymes involved in naproxen degradation by Planococcus sp. S5. Pol J Microbiol 65(2):177–182.  https://doi.org/10.5604/17331331.1204477 CrossRefPubMedGoogle Scholar
  37. Zhang Y, Geissen SU (2010) In vitro degradation of carbamazepine and diclofenac by crude lignin peroxidase. J Hazard Mater 176(1–3):1089–1092.  https://doi.org/10.1016/j.jhazmat.2009.10.133 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • B. M. Alanis-Sánchez
    • 1
  • S. M. Pérez-Tapia
    • 2
    • 3
    • 4
  • S. Vázquez-Leyva
    • 2
  • I. Mejía-Calvo
    • 2
  • Z. Macías-Palacios
    • 2
  • L. Vallejo-Castillo
    • 2
  • C. M. Flores-Ortiz
    • 5
  • C. Guerrero-Barajas
    • 6
  • J. A. Cruz-Maya
    • 7
  • J. Jan-Roblero
    • 1
    Email author
  1. 1.Laboratorio de Biotecnología Ambiental, Departamento de Microbiología, Escuela Nacional de Ciencias BiológicasInstituto Politécnico NacionalMexico CityMexico
  2. 2.Unidad de Desarrollo e Investigación en Bioprocesos (UDIBI), Escuela Nacional de Ciencias BiológicasInstituto Politécnico NacionalMexico CityMexico
  3. 3.Departamento de Inmunología, Escuela Nacional de Ciencias BiológicasInstituto Politécnico NacionalMexico CityMexico
  4. 4.Laboratorio Nacional para Servicios Especializados de Investigación, Desarrollo e Innovación (I+D+i) para Farmoquímicos y BiotecnológicosLANSEIDI-FarBiotec-CONACyTMexico CityMexico
  5. 5.Laboratorio de Biogeoquímica, UBIPRO, FES-IztacalaUniversidad Nacional Autónoma de MéxicoTlalnepantlaMexico
  6. 6.Laboratorio de Biotecnología Ambiental, Departamento de Bioprocesos, Unidad Profesional Interdisciplinaria de BiotecnologíaInstituto Politécnico NacionalMexico CityMexico
  7. 7.Unidad Profesional Interdisciplinaria en Ingeniería y Tecnologías AvanzadasInstituto Politécnico NacionalMexico CityMexico

Personalised recommendations

Cite article

Buy options