Utilization of naproxen by Amycolatopsis sp. Poz 14 and detection of the enzymes involved in the degradation metabolic pathway
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.
KeywordsNaproxen Carbamazepine Amycolatopsis 5-Methoxysalicylic acid Catechol Gentisic acid
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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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