Fungal and bacterial species in degrading carbamazepine: a metabolite perspective: Mini-review

Valerie Emily; Wong Rui Rui; Yuka Hara; Adura Mohd Adnan; Ong Ghim Hock; Wong Kok Kee

doi:10.18006/2022.10(5).922.931

Authors

Valerie Emily Faculty of Health and Life Sciences, INTI International University, Persiaran Perdana BBN, PutraNilai, 71800 Nilai, Negeri Sembilan, Malaysia. https://orcid.org/0000-0003-0023-5718
Wong Rui Rui Faculty of Health and Life Sciences, INTI International University, Persiaran Perdana BBN, PutraNilai, 71800 Nilai, Negeri Sembilan, Malaysia. https://orcid.org/0000-0002-0028-0159
Yuka Hara Faculty of Health and Life Sciences, INTI International University, Persiaran Perdana BBN, PutraNilai, 71800 Nilai, Negeri Sembilan, Malaysia. https://orcid.org/0000-0002-5044-1942
Adura Mohd Adnan Faculty of Health and Life Sciences, INTI International University, Persiaran Perdana BBN, PutraNilai, 71800 Nilai, Negeri Sembilan, Malaysia. https://orcid.org/0000-0002-9138-0672
Ong Ghim Hock Faculty of Health and Life Sciences, INTI International University, Persiaran Perdana BBN, PutraNilai, 71800 Nilai, Negeri Sembilan, Malaysia. https://orcid.org/0000-0001-9458-9511
Wong Kok Kee Faculty of Health and Life Sciences, INTI International University, Persiaran Perdana BBN, PutraNilai, 71800 Nilai, Negeri Sembilan, Malaysia. https://orcid.org/0000-0001-5402-2561

DOI:

https://doi.org/10.18006/2022.10(5).922.931

Keywords:

Fungi, Bacteria, Degrading carbamazepine, Microbial enzymes

Abstract

Carbamazepine (CBZ) is a ubiquitous pharmaceutical pollutant found in various water environments. This is due to the ineffective CBZ removal, despite employing advanced physiochemical treatment technologies in the current conventional wastewater treatment plants. Thus, bioremediation that utilizes enzymes in microorganisms' systems to bio-mineralize CBZ is suggested as an alternative or complementary technique to remove CBZ more effectively. However, information from published research on the biodegradation of CBZ, the toxicity of metabolites, or toxicity testing was rarely evaluated or assessed cohesively. This aspect is important because if bioremediation of CBZ produces toxic metabolites, it will defeat the main purpose of bioremediation. Thus, the focus of this review is to assess the effectiveness of fungi and bacteria in the biodegradation of CBZ, particularly by looking at the type of enzymes expressed, and the metabolites produced. In this review, information related to the fungal and bacterial species that were reported to degrade CBZ was collated from the published literature and analyzed. Results of the analysis showed that cytochrome P450, laccase, and manganese peroxidase were the common enzymes responsible to degrade CBZ. However, such enzymatic activities can sometimes produce epoxy-CBZ, which is a more toxic compound than the parent compound. Only the fungus Pleurotus ostreatus was able to oxidize epoxy-CBZ via the acridine pathway into acridone, the latter a metabolite that is susceptible to further biodegradation into nontoxic metabolites. However, the identity of the end metabolites is not reported nor characterized. Further, Pseudomonas spp. is the most promising bioremediating agent since it can metabolize CBZ into catechol, the latter can enter the carbon central pathways to generate energy for the bacterial cells.

References

Almeida, Â., Freitas, R., Calisto, V., Esteves, V. I., Schneider, R. J., Soares, A. M., & Figueira, E. (2015). Chronic toxicity of the antiepileptic carbamazepine on the clam Ruditapes philippinarum. Comparative biochemistry and physiology. Toxicology & pharmacology: CBP, 172-173, 26–35. https://doi.org/10.1016/j.cbpc.2015.04.004 DOI: https://doi.org/10.1016/j.cbpc.2015.04.004

Almeida, Â., Soares, A. M. V. M., Esteves, V. I., & Freitas, R. (2021). Occurrence of the antiepileptic carbamazepine in water and bivalves from marine environments: A review. Environmental Toxicology and Pharmacology, 86, 103661. https://doi.org/ 10.1016/j.etap.2021.103661 DOI: https://doi.org/10.1016/j.etap.2021.103661

Alrashood, S. T. (2016). Carbamazepine. Profiles of Drug Substances, Excipients and Related Methodology, 41, 133–321. https://doi.org/10.1016/bs.podrm.2015.11.001 DOI: https://doi.org/10.1016/bs.podrm.2015.11.001

Anku, W. W., Mamo, M. A., & Govender, P. P. (2017). Phenolic compounds in water: sources, reactivity, toxicity and treatment methods. In M. Soto-Hernandez, M. Palma-Tenango, & M.D.R Garcia-Mateos (Eds), Phenolic compounds-natural sources, importance and applications (pp.420-443). IntechOpen. DOI: 10.5772/66927 DOI: https://doi.org/10.5772/66927

Annweiler, E., Richnow, H. H., Antranikian, G., Hebenbrock, S., et al. (2000). Naphthalene degradation and incorporation of naphthalene-derived carbon into biomass by the thermophile Bacillus thermoleovorans. Applied and Environmental Microbiology, 66(2), 518-523. doi: 10.1128/aem.66.2.518-523.2000 DOI: https://doi.org/10.1128/AEM.66.2.518-523.2000

Arye, G., Dror, I., & Berkowitz, B. (2011). Fate and transport of carbamazepine in soil aquifer treatment (SAT) infiltration basin soils. Chemosphere, 82(2), 244–252. https://doi.org/10.1016/ j.chemosphere.2010.09.062 DOI: https://doi.org/10.1016/j.chemosphere.2010.09.062

Asif, M. B., Hai, F. I., Singh, L., Price, W. E., et al. (2017). Degradation of pharmaceuticals and personal care products by white-rot fungi—a critical review. Current Pollution Reports, 3(2), 88–103. https://doi.org/10.1007/s40726-017-0049-5 DOI: https://doi.org/10.1007/s40726-017-0049-5

Aukema, K. G., Escalante, D. E., Maltby, M. M., et al. (2016). In-silico identification of bioremediation potential: Carbamazepine and other recalcitrant personal care products. Environmental Science & Technology, 51(2), 880–888. https://doi.org/10.1021/ acs.est.6b04345 DOI: https://doi.org/10.1021/acs.est.6b04345

Barry, S. M., & Challis, G. L. (2013). Mechanism and catalytic diversity of rieske non-heme iron-dependent oxygenases. ACS Catalysis, 3(10), 2362–2370. https://doi.org/10.1021/cs400087p DOI: https://doi.org/10.1021/cs400087p

Basu, A., & Phale, P. S. (2008). Conjugative transfer of preferential utilization of aromatic compounds from Pseudomonas putida CSV86. Biodegradation, 19(1), 83-92. doi: 10.1007/s10532-007-9117-7 DOI: https://doi.org/10.1007/s10532-007-9117-7

Bessa, V. S., Moreira, I. S., Murgolo, S., Mascolo, G., & Castro, P. M. L. (2019). Carbamazepine is degraded by the bacterial strain Labrys portucalensis F11. Science of the Total Environment, 690, 739–747. https://doi.org/10.1016/j.scitotenv.2019.06.461 DOI: https://doi.org/10.1016/j.scitotenv.2019.06.461

Bleeker, E. A. J., Van Der Geest, H. G., Klamer, H. J. C., De Voogt, P., Wind, E., & Kraak, M. H. S. (1999). Toxic and genotoxic effects of Azaarenes: Isomers and metabolites. Polycyclic Aromatic Compounds, 13(3), 191–203. https://doi.org/10.1080/10406639908020563 DOI: https://doi.org/10.1080/10406639908020563

Brusseau, M., Pepper, I., & Gerba, C. P. (2019). Environmental Toxicology. Environmental and Pollution Science (pp.511-540). Elsevier. https://doi.org/10.1016/b978-0-12-814719-1.00028-8 DOI: https://doi.org/10.1016/B978-0-12-814719-1.00028-8

Buchicchio, A., Bianco, G., Sofo, A., Masi, S., & Caniani, D. (2016). Biodegradation of carbamazepine and clarithromycin by Trichoderma harzianum and Pleurotus ostreatus investigated by liquid chromatography–high-resolution tandem mass spectrometry (FTICR MS-IRMPD). Science of the Total Environment, 557-558, 733–739. https://doi.org/10.1016/j.scitotenv.2016.03.119 DOI: https://doi.org/10.1016/j.scitotenv.2016.03.119

Cajthaml, T., Möder, M., Kačer, P., Šašek, V., & Popp, P. (2002). Study of fungal degradation products of polycyclic aromatic hydrocarbons using gas chromatography with ion trap mass spectrometry detection. Journal of Chromatography A, 974(1-2), 213–222. https://doi.org/10.1016/s0021-9673(02)00904-4 DOI: https://doi.org/10.1016/S0021-9673(02)00904-4

Chen, H., Gu, X., Zeng, Q., & Mao, Z. (2019). Acute and chronic toxicity of carbamazepine on the release of chitobiase, molting, and reproduction in Daphnia similis. International Journal of Environmental Research and Public Health, 16(2), 209. https://doi.org/10.3390/ijerph16020209 DOI: https://doi.org/10.3390/ijerph16020209

Clara, M., Strenn, B., & Kreuzinger, N. (2004). Carbamazepine as a possible anthropogenic marker in the aquatic environment: investigations on the behaviour of carbamazepine in wastewater treatment and during groundwater infiltration. Water Research, 38(4), 947–954. https://doi.org/10.1016/j.watres.2003.10.058 DOI: https://doi.org/10.1016/j.watres.2003.10.058

Cleuvers, M. (2003). Aquatic ecotoxicity of pharmaceuticals including the assessment of combination effects. Toxicology Letters, 142(3), 185–194. https://doi.org/10.1016/s0378-4274(03)00068-7 DOI: https://doi.org/10.1016/S0378-4274(03)00068-7

Črešnar, B., & Petrič, Š. (2011). Cytochrome P450 enzymes in the fungal kingdom. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, 1814(1), 29–35. https://doi.org/10.1016/ j.bbapap.2010.06.020 DOI: https://doi.org/10.1016/j.bbapap.2010.06.020

Crini, G., & Lichtfouse, E. (2018). Advantages and disadvantages of techniques used for wastewater treatment. Environmental Chemistry Letters, 17(145–155). https://doi.org/10.1007/s10311-018-0785-9 DOI: https://doi.org/10.1007/s10311-018-0785-9

Dai, C., Zhou, X., Zhang, Y., Duan, Y., Qiang, Z., & Zhang, T. C. (2012). Comparative study of the degradation of carbamazepine in water by advanced oxidation processes. Environmental Technology, 33(10), 1101–1109. https://doi.org/10.1080/ 09593330.2011.610359 DOI: https://doi.org/10.1080/09593330.2011.610359

Dennis, J. J., & Zylstra, G. J. (2004). Complete sequence and genetic organization of pDTG1, the 83 kilobase naphthalene degradation plasmid from Pseudomonas putida strain NCIB 9816-4. Journal of molecular biology, 341(3), 753-768. doi: 10.1016/j.jmb.2004.06.034 DOI: https://doi.org/10.1016/j.jmb.2004.06.034

Di, L., & Kerns, E. H. (2016). Solution Stability. Drug-like Properties (pp. 207-217), Elsevier publication. https://doi.org/ 10.1016/b978-0-12-801076-1.00013-7 DOI: https://doi.org/10.1016/B978-0-12-801076-1.00013-7

Freitas, R., Almeida, Â., Pires, A., Velez, C., et al. (2015). The effects of carbamazepine on macroinvertebrate species: Comparing bivalves and polychaetes biochemical responses. Water Research, 85, 137–147. https://doi.org/10.1016/j.watres.2015.08.003 DOI: https://doi.org/10.1016/j.watres.2015.08.003

Golan-Rozen, N., Chefetz, B., Ben-Ari, J., Geva, J., & Hadar, Y. (2011). Transformation of the recalcitrant pharmaceutical compound carbamazepine by Pleurotus ostreatus: Role of cytochrome p450 monooxygenase and manganese peroxidase. Environmental Science & Technology, 45(16), 6800–6805. https://doi.org/10.1021/es200298t DOI: https://doi.org/10.1021/es200298t

Golan-Rozen, N., Seiwert, B., Riemenschneider, C., Reemtsma, T., et al. (2015). Transformation pathways of the recalcitrant pharmaceutical compound carbamazepine by the white-rot fungus pleurotus ostreatus: effects of growth conditions. Environmental Science & Technology, 49(20), 12351–12362. https://doi.org/ 10.1021/acs.est.5b02222 DOI: https://doi.org/10.1021/acs.est.5b02222

Gold, M. H., & Alic, M. (1993). Molecular biology of the lignin-degrading basidiomycete Phanerochaete chrysosporium. Microbiological Reviews, 57(3), 605–622. https://doi.org/10.1128/ mr.57.3.605-622.1993 DOI: https://doi.org/10.1128/mr.57.3.605-622.1993

Hai, F., Yang, S., Asif, M., Sencadas, V., et al. (2018). Carbamazepine as a possible anthropogenic marker in water: occurrences, toxicological effects, regulations, and removal by wastewater treatment technologies. Water, 10(2), 107. https://doi.org/10.3390/w10020107 DOI: https://doi.org/10.3390/w10020107

Heberer, T., & Feldmann, D. (2005). Contribution of effluents from hospitals and private households to the total loads of diclofenac and carbamazepine in municipal sewage effluents—modeling versus measurements. Journal of Hazardous Materials, 122(3), 211–218. https://doi.org/10.1016/j.jhazmat.2005.03.007 DOI: https://doi.org/10.1016/j.jhazmat.2005.03.007

Heye, K., Becker, D., Lütke Eversloh, C., Durmaz, V., et al. (2016). Effects of carbamazepine and two of its metabolites on the non-biting midge Chironomus riparius in a sediment full life cycle toxicity test. Water Research, 98, 19–27. https://doi.org/10.1016/ j.watres.2016.03.071 DOI: https://doi.org/10.1016/j.watres.2016.03.071

Hildén, K., & Mäkelä, M. R. (2018). Role of fungi in wood decay. In B. D. Roitberg (Ed.), Reference module in life sciences (Vol. 2018). Elsevier. https://doi.org/10.1016/B978-0-12-809633-8.12424-0 DOI: https://doi.org/10.1016/B978-0-12-809633-8.12424-0

Huerta-Fontela, M., Galceran, M.T., & Ventura, F. (2011). Occurrence and removal of pharmaceuticals and hormones through drinking water treatment. Water Research, 45 (3), 1432-1442. https://doi.org/10.1016/j.watres.2010.10.036 DOI: https://doi.org/10.1016/j.watres.2010.10.036

Izmalkova, T. Y., Sazonova, O. I., Nagornih, M. O., Sokolov, S. L., Kosheleva, I. A., & Boronin, A. M. (2013). The organization of naphthalene degradation genes in Pseudomonas putidastrain AK5. Research in Microbiology, 164(3), 244-253. doi: 10.1016/j.resmic.2012.12.007 DOI: https://doi.org/10.1016/j.resmic.2012.12.007

Jarque, S., Masner, P., Klánová, J., Prokeš, R., & Bláha, L. (2016). Bioluminescent Vibrio fischeri assays in the assessment of seasonal and spatial patterns in toxicity of contaminated river sediments. Frontiers in Microbiology, 7, 1738. https://doi.org/ 10.3389/fmicb.2016.01738 DOI: https://doi.org/10.3389/fmicb.2016.01738

Jelic, A., Cruz-Morató, C., Marco-Urrea, E., Sarrà, M., et al. (2012). Degradation of carbamazepine by Trametes versicolor in an air pulsed fluidized bed bioreactor and identification of intermediates. Water Research, 46(4), 955–964. https://doi.org/ 10.1016/j.watres.2011.11.063 DOI: https://doi.org/10.1016/j.watres.2011.11.063

Johnson, B.T. (2005). Microtox® Acute Toxicity Test. In: C. Blaise, and J.F. Férard, (eds) Small-scale freshwater toxicity investigations. (pp. 69-105). Springer. https://doi.org/10.1007/1-4020-3120-3_2 DOI: https://doi.org/10.1007/1-4020-3120-3_2

Jos, A., Repetto, G., Rios, J. C., Hazen, M. J., et al. (2003). Ecotoxicological evaluation of carbamazepine using six different model systems with eighteen endpoints. Toxicology in Vitro, 17(5-6), 525–532. https://doi.org/10.1016/s0887-2333 (03)00119-x DOI: https://doi.org/10.1016/S0887-2333(03)00119-X

Kallemeijn, W. W., Witte, M. D., Wennekes, T., & Aerts, J. M. F. G. (2014). Mechanism-based inhibitors of glycosidases. Advances in Carbohydrate Chemistry and Biochemistry, 71, 297–338. https://doi.org/10.1016/b978-0-12-800128-8.00004-2 DOI: https://doi.org/10.1016/B978-0-12-800128-8.00004-2

Kosjek, T., Andersen, H. R., Kompare, B., et al. (2009). Fate of carbamazepine during water treatment. Environmental Science & Technology, 43(16), 6256–6261. https://doi.org/10.1021/ es900070h DOI: https://doi.org/10.1021/es900070h

Li, A., Cai, R., Cui, D., Qiu, T., et al. (2013). Characterization and biodegradation kinetics of a new cold-adapted carbamazepine-degrading bacterium, Pseudomonas sp. CBZ-4. Journal of Environmental Sciences, 25(11), 2281–2290. https://doi.org/ 10.1016/s1001-0742(12)60293-9 DOI: https://doi.org/10.1016/S1001-0742(12)60293-9

Li, X., de Toledo, R. A., Wang, S., & Shim, H. (2015). Removal of carbamazepine and naproxen by immobilized Phanerochaete chrysosporium under non-sterile condition. New Biotechnology, 32(2), 282–289. https://doi.org/10.1016/j.nbt.2015.01.003 DOI: https://doi.org/10.1016/j.nbt.2015.01.003

Mahajan, M. C., Phale, P. S., & Vaidyanathan, C. S. (1994). Evidence for the involvement of multiple pathways in the biodegradation of 1-and 2-methylnaphthalene by Pseudomonas putida CSV86. Archives of Microbiology, 161(5), 425-433. doi: 10.1007/BF00288954 DOI: https://doi.org/10.1007/BF00288954

Miao, X.S., Yang, J.J., & Metcalfe, C. D. (2005). Carbamazepine and its metabolites in wastewater and in biosolids in a municipal wastewater treatment plant. Environmental Science & Technology, 39(19), 7469–7475. https://doi.org/10.1021/es050261e DOI: https://doi.org/10.1021/es050261e

Mir-Tutusaus, J. A., Parladé, E., Villagrasa, M., Barceló, D., et al. (2019). Long-term continuous treatment of non-sterile real hospital wastewater by Trametes versicolor. Journal of Biological Engineering, 2019(47), 1-13. https://doi.org/10.1186/s13036-019-0179-y DOI: https://doi.org/10.1186/s13036-019-0179-y

Montefiori, M., Jørgensen, F. S., & Olsen, L. (2017). Aldehyde oxidase: Reaction mechanism and prediction of site of metabolism. ACS Omega, 2(8), 4237–4244. https://doi.org/10.1021/ acsomega.7b00658 DOI: https://doi.org/10.1021/acsomega.7b00658

Naghdi, M., Taheran, M., Brar, S. K., Kermanshahi-pour, A., et al. (2018). Biotransformation of carbamazepine by laccase-mediator system: Kinetics, by-products and toxicity assessment. Process Biochemistry, 67, 147–154. https://doi.org/10.1016/ j.procbio.2018.02.009 DOI: https://doi.org/10.1016/j.procbio.2018.02.009

Nozaki, M., Ono, K., Nakazawa, T., Kotani, S., & Hayaishi, O. S. A. M. U. (1968). Metapyrocatechase: II. The role of iron and sulfhydryl groups. Journal of Biological Chemistry, 243(10), 2682-2690. doi: 10.1016/S0021-9258(18)93426-5 DOI: https://doi.org/10.1016/S0021-9258(18)93426-5

Oesch-Bartlomowicz, B., & Oesch, F. (2007). mechanisms of toxification and detoxification which challenge drug candidates and drugs. Comprehensive Medicinal Chemistry II, 5, 193–214. https://doi.org/10.1016/b0-08-045044-x/00124-3 DOI: https://doi.org/10.1016/B0-08-045044-X/00124-3

Olicón-Hernández, D. R., González-López, J., & Aranda, E. (2017). overview on the biochemical potential of filamentous fungi to degrade pharmaceutical compounds. Frontiers in Microbiology, 8. https://doi.org/10.3389/fmicb.2017.01792 DOI: https://doi.org/10.3389/fmicb.2017.01792

Park, H.G., Kim, T.W., Chae, M.Y., & Yoo, I.K. (2007) Activated carbon-containing alginate adsorbent for the simultaneous removal of heavy metals and toxic organics. Process Biochemistry, 42 (10), 1371-1377 DOI: https://doi.org/10.1016/j.procbio.2007.06.016

Popa, C., Favier, L., Dinica, R., Semrany, S., et al. (2014). Potential of newly isolated wild Streptomyces strains as agents for the biodegradation of a recalcitrant pharmaceutical, carbamazepine. Environmental Technology, 35(24), 3082–3091. https://doi.org/10.1080/09593330.2014.931468 DOI: https://doi.org/10.1080/09593330.2014.931468

PubChem. (2021b). Carbamazepine. PubChem. Retrieved from https://pubchem.ncbi.nlm.nih.gov/compound/2554#section=2D-Structure

Radjenović, J., Petrović, M., Ventura, F., & Barceló, D. (2008). Rejection of pharmaceuticals in nanofiltration and reverse osmosis membrane drinking water treatment. Water Research, 42(14), 3601–3610. https://doi.org/10.1016/j.watres.2008.05.020 DOI: https://doi.org/10.1016/j.watres.2008.05.020

Resnick, S. M., Lee, K., & Gibson, D. T. (1996). Diverse reactions catalyzed by naphthalene dioxygenase from Pseudomonas sp. strain NCIB 9816. Journal of Industrial Microbiology, 17(5), 438-457. doi: 10.1007/BF01574775 DOI: https://doi.org/10.1007/BF01574775

Rodríguez-Rodríguez, C. E., Marco-Urrea, E., & Caminal, G. (2010). Degradation of naproxen and carbamazepine in spiked sludge by slurry and solid-phase Trametes versicolor systems. Bioresource Technology, 101(7), 2259–2266. https://doi.org/ 10.1016/j.biortech.2009.11.089 DOI: https://doi.org/10.1016/j.biortech.2009.11.089

Rosario-Ortiz, F. L., Wert, E. C., & Snyder, S. A. (2010). Evaluation of UV/H2O2 treatment for the oxidation of pharmaceuticals in wastewater. Water Research, 44(5), 1440–1448. https://doi.org/10.1016/j.watres.2009.10.031 DOI: https://doi.org/10.1016/j.watres.2009.10.031

Schweigert, N., Zehnder, A. J. B., & Eggen, R. I. L. (2001). Chemical properties of catechols and their molecular modes of toxic action in cells, from microorganisms to mammals. Minireview. Environmental Microbiology, 3(2), 81–91. https://doi.org/10.1046/j.1462-2920.2001.00176.x DOI: https://doi.org/10.1046/j.1462-2920.2001.00176.x

Sichel, C., Garcia, C., & Andre, K. (2011). Feasibility studies: UV/chlorine advanced oxidation treatment for the removal of emerging contaminants. Water Research, 45(19), 6371–6380. https://doi.org/10.1016/j.watres.2011.09.025 DOI: https://doi.org/10.1016/j.watres.2011.09.025

Singh, N., Kumar, A., & Sharma, B. (2019). Role of fungal enzymes for bioremediation of hazardous chemicals. In: A. Yadav, S. Singh, S. Mishra, and A. Gupta, (eds) Recent Advancement in White Biotechnology Through Fungi. (pp 237-256). Springer. https://doi.org/10.1007/978-3-030-25506-0_9 DOI: https://doi.org/10.1007/978-3-030-25506-0_9

Snyder, S. A., Adham, S., Redding, A. M., Cannon, F. S., DeCarolis, J., Oppenheimer, J., Wert, E. C., & Yoon, Y. (2007). Role of membranes and activated carbon in the removal of endocrine disruptors and pharmaceuticals. Desalination, 202(1-3), 156–181. https://doi.org/10.1016/j.desal.2005.12.052 DOI: https://doi.org/10.1016/j.desal.2005.12.052

Ternes, T. A., Herrmann, N., Bonerz, M., Knacker, T., et al. (2004). A rapid method to measure the solid–water distribution coefficient (Kd) for pharmaceuticals and musk fragrances in sewage sludge. Water Research, 38(19), 4075–4084. https://doi.org/10.1016/j.watres.2004.07.015 DOI: https://doi.org/10.1016/j.watres.2004.07.015

Yen, K. M., Serdar, C. M., & Gunsalus, I. C. (1988). Genetics of naphthalene catabolism in pseudomonads. CRC Critical reviews in microbiology, 15(3), 247-268. doi: 10.3109/10408418809104459 DOI: https://doi.org/10.3109/10408418809104459

Zouboulis, A. I., Moussas, P. A., & Psaltou, S. G. (2019). Groundwater and Soil Pollution: Bioremediation. Encyclopedia of Environmental Health, 369–381. https://doi.org/10.1016/b978-0-12-409548-9.11246-1 DOI: https://doi.org/10.1016/B978-0-12-409548-9.11246-1