Biodegradation

, Volume 23, Issue 1, pp 145–156 | Cite as

Biotransformation of three pharmaceutical active compounds by the fungus Phanerochaete chrysosporium in a fed batch stirred reactor under air and oxygen supply

  • A. I. Rodarte-Morales
  • G. Feijoo
  • M. T. Moreira
  • J. M. Lema
Original Paper

Abstract

White-rot fungi are a group of microorganisms capable of degrading xenobiotic compounds, such as polycyclic aromatic hydrocarbons or synthetic dyes, by means of the action of extracellular oxidative enzymes secreted during secondary metabolism. In this study, the transformation of three anti-inflammatory drugs: diclofenac, ibuprofen and naproxen were carried out by pellets of Phanerochaete chrysosporium in fed-batch bioreactors operating under continuous air supply or periodic pulsation of oxygen. The performance of the fungal reactors was steady over a 30-day treatment and the effect of oxygen pulses on the pellet morphology was evidenced. Complete elimination of diclofenac was achieved in the aerated and the oxygenated reactors, even with a fast oxidation rate in the presence of oxygen (77% after 2 h), reaching a total removal after 23 h. In the case of ibuprofen, this compound was completely oxidized under air and oxygen supply. Finally, naproxen was oxidized in the range of 77 up to 99% under both aeration conditions. These findings demonstrate that the oxidative capability of this microorganism for the anti-inflammatory drugs is not restricted to an oxygen environment, as generally accepted, since the fungal reactor was able to remove these compounds under aerated and oxygenated conditions. This result is very interesting in terms of developing viable reactors for the oxidation of target compounds as the cost of aeration can be significantly reduced.

Keywords

Pharmaceutical White-rot fungi (WRF) Degradation Diclofenac Ibuprofen Naproxen 

References

  1. Bao W, Fukushima Y, Jensen KA, Moen MA, Hammel KE (1994) Oxidative degradation of non-phenolic lignin during lipid peroxidation by fungal manganese peroxidase. FEBS Lett 354:297–300PubMedCrossRefGoogle Scholar
  2. Cabana H, Jones JP, Agathos SN (2007) Elimination of endocrine disrupting chemicals using white rot fungi and their lignin modifying enzymes: a review. Eng Life Sci 5:429–456CrossRefGoogle Scholar
  3. Call HP, Mücke I (1997) Minireview: history, overview and applications of mediated ligninolytic systems, especially laccase-mediator-systems (Lignozym-Process). J Biotechnol 53:163–202CrossRefGoogle Scholar
  4. Cañas AI, Camarero S (2010) Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol Adv 28:694–705PubMedCrossRefGoogle Scholar
  5. Carballa M, Omil F, Lema JM, Llompart M, García-Jares C, Rodríguez I, Gómez M, Ternes T (2004) Behavior of pharmaceuticals, cosmetics and hormones in a sewage treatment plant. Water Res 38:2918–2926PubMedCrossRefGoogle Scholar
  6. Carballa M, Omil F, Lema JM (2005) Removal of cosmetic ingredients and pharmaceuticals in sewage primary treatment. Water Res 39:4790–4796PubMedCrossRefGoogle Scholar
  7. Clara M, Strenn B, Gans O, Martínez E, Kreuzinger N, Kroiss H (2005) Removal of selected pharmaceuticals, fragrances and endocrine disrupting compounds in a membrane bioreactor and conventional wastewater treatment plants. Water Res 39:4797–4807PubMedCrossRefGoogle Scholar
  8. Eibes G, Debernardi G, Feijoo G, Moreira MT, Lema JM (2011) Oxidation of pharmaceutically active compounds by a ligninolytic fungal peroxidase. Biodegradation 22:539–550PubMedCrossRefGoogle Scholar
  9. Esplugas S, Bila DM, Krause GT, Dezotti M (2007) Review article: ozonation and advanced oxidation technologies to remove endocrine disrupting chemicals (EDCs) and pharmaceuticals and personal care products (PPCPs) in water effluents. J Hazard Mater 149:631–642PubMedCrossRefGoogle Scholar
  10. Field JA, De Jong E, Feijoo CG, De Bont JAM (1992) Biodegradation of polycyclic aromatic hydrocarbons by new isolates of white rot fungi. Appl Environ Microbiol 58(7):2219–2226PubMedGoogle Scholar
  11. Gagnon C, Lajeunesse A, Cejka P, Gagné F, Hausler R (2008) Degradation of selected acidic and neutral pharmaceutical products in a primary-treated wastewater by disinfection processes. Ozone Sci Eng 30:387–392CrossRefGoogle Scholar
  12. Hata T, Shintate H, Kawai S, Okamura H, Nishida T (2010) Elimination of carbamazepine by repeated treatment with laccase in the presence of 1-hydroxybenzotriazole. J Hazard Mater 181:1175–1178PubMedCrossRefGoogle Scholar
  13. Ikehata K, Naghashkar N, El-Din MG (2006) Degradation of aqueous pharmaceuticals by ozonation and advanced oxidation processes: a review. Ozone Sci Eng 28(6):353–414CrossRefGoogle Scholar
  14. Jiménez-Tobón GA, Penninckx MJ, Lejeune R (1997) The relationship between pellet size and production of Mn(II) peroxidase by Phanerochaete chrysosporium in submerged culture. Enzyme Microb Technol 21:537–542CrossRefGoogle Scholar
  15. Kosjek T, Heath E, Kompare B (2007) Removal of pharmaceutical residues in a pilot wastewater treatment plant. Anal Bioanal Chem 387:1379–1387PubMedCrossRefGoogle Scholar
  16. Lindqvist N, Tuhkanen T, Kronberg L (2005) Occurrence of acidic pharmaceuticals in raw and treated sewages and in receiving waters. Water Res 39:2219–2228PubMedCrossRefGoogle Scholar
  17. Lloret L, Eibes G, Lú-Chau T, Moreira MT, Feijoo G, Lema JM (2010) Laccase-catalyzed degradation of anti-inflammatories and estrogens. Biochem Eng J 51:124–131CrossRefGoogle Scholar
  18. Marco-Urrea E, Pérez-Trujillo M, Vicent T, Caminal G (2009) Ability of white-rot fungi to remove selected pharmaceuticals and identification of degradation products of ibuprofen by Trametes versicolor. Chemosphere 74:765–772PubMedCrossRefGoogle Scholar
  19. Marco-Urrea E, Pérez-Trujillo M, Cruz-Morató C, Caminal G, Vicent T (2010a) Degradation of the drug sodium diclofenac by Trametes versicolor pellets and identification of some intermediates by NMR. J Hazard Mater 176:836–842PubMedCrossRefGoogle Scholar
  20. Marco-Urrea E, Pérez-Trujillo M, Blánquez P, Vicent T, Caminal G (2010b) Biodegradation of the analgesic naproxen by Trametes versicolor and identification of intermediates using HPLC-DAD-MS and NMR. Bioresour Technol 101:2159–2166PubMedCrossRefGoogle Scholar
  21. Méndez-Arriaga F, Esplugas S, Giménez J (2010) Degradation of the emerging contaminant ibuprofen in water by photo-Fenton. Water Res 44:589–595PubMedCrossRefGoogle Scholar
  22. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31(3):426–428CrossRefGoogle Scholar
  23. Miura D, Tanaka H, Wariishi H (2004) Metabolomic differential display analysis of the white-rot basidiomycete Phanerochaete chrysosporium grown under air and 100% oxygen. FEMS Microbiol Lett 234:111–116PubMedCrossRefGoogle Scholar
  24. Moreira MT, Sanromán A, Feijoo G, Lema JM (1996) Control of pellet morphology of filamentous fungi in fluidized bed bioreactors by means of a pulsing flow. Application to Aspergillus niger and Phanerochaete chrysosporium. Enzyme Microb Technol 19:261–266PubMedCrossRefGoogle Scholar
  25. Reddersen K, Heberer T (2003) Multi-compound methods for the detection of pharmaceutical residues in various waters applying solid phase extraction (SPE) and gas chromatography with mass spectrometric (GC-MS) detection. J Sep Sci 26:1443–1450CrossRefGoogle Scholar
  26. Reif R, Suárez S, Omil F, Lema JM (2008) Fate of pharmaceuticals and cosmetic ingredients during the operation of a MBR treating sewage. Desalination 221:511–517CrossRefGoogle Scholar
  27. Rodarte-Morales AI, Feijoo C, Moreira MT, Lema JM (2011) Degradation of selected pharmaceutical and personal care products (PPCPs) by white-rot fungi. World J Microbiol Biotechnol. doi 10.1007/s11274-010-0642-x
  28. Rodríguez I, Quintana JB, Carpinteiro J, Carro AM, Lorenzo RA, Cela R (2003) Determination of acidic drugs in sewage by gas chromatography-mass spectrometry as tert-butylmethylsilyl derivatives. J Chromatogr 985:265–274CrossRefGoogle Scholar
  29. Rodríguez-Rodríguez CE, Marco-Urrea E, Caminal G (2010) Naproxen degradation test to monitor Trametes versicolor activity in solid-state bioremediation processes. J Hazard Mater 179:1152–1155PubMedCrossRefGoogle Scholar
  30. Rothschild N, Levkowitz A, Hadar Y, Dosoretz CG (1999) Manganese deficiency can replace high oxygen levels needed for lignin peroxidase formation by Phanerochaete chrysosporium. Appl Environ Microbiol 65(2):483–488PubMedGoogle Scholar
  31. Suárez S, Ramil M, Omil F, Lema JM (2005) Removal of pharmaceutically active compounds in nitrifying-denitrifying plants. Water Sci Technol 52(8):9–14PubMedGoogle Scholar
  32. Suárez S, Carballa M, Omil F, Lema JM (2008) How are pharmaceutical and personal care products (PPCPs) removed from urban wastewaters? Rev Environ Sci Biotechnol 7:125–138CrossRefGoogle Scholar
  33. Tien M, Kirk TK (1984) Lignin-degrading enzyme from Phanerochaete chrysosporium: purification, characterization, and catalytic properties of a unique H2O2-requiring oxygenase. Proc Natl Acad Sci USA 81:2280–2284PubMedCrossRefGoogle Scholar
  34. Tien M, Kirk TK (1988) Lignin peroxidase of Phanerochaete chrysosporium. In: Wood WA, Klogg ST (eds) Methods in enzymology-biomass, part b, lignin, pectin, and chitin, vol 161. Academic Press, San Diego, pp 238–249CrossRefGoogle Scholar
  35. Tsung-Hsien Y, Yu-Chen L, Lateef SK, Cheng-Fang L, Ping-Yi Y (2009) Removal of antibiotics and non-steroidal anti-inflammatory drugs by extended sludge age biological process. Chemosphere 77:175–181CrossRefGoogle Scholar
  36. Vogna D, Marotta R, Andreozzi R, Napolitano A, d′Ischia M (2004) Kinetic and chemical assessment of the UV//H2O2 treatment of antiepileptic drug carbamazepine. Chemosphere 54:497–505PubMedCrossRefGoogle Scholar
  37. Wesenberg D, Kyriakides I, Agathos SN (2003) White rot fungi and their enzymes for the treatment of industrial dye effluents. Biotechnol Adv 22:161–187PubMedCrossRefGoogle Scholar
  38. Zeddel A, Majcherczyk A, Huttermann A (1993) Degradation of polychlorinated-biphenyls by white-rot fungi Pleurotus-ostreatus and Trametes-versicolor in a solid-state system. Toxicol Environ Chem 40(1–4):255–266CrossRefGoogle Scholar
  39. Zhang Y, Geißen SU (2010) In vitro degradation of carbamazepine and diclofenac by crude lignin peroxidase. J Hazard Mater 176:1089–1192PubMedCrossRefGoogle Scholar
  40. Zhang Y, Geißen SU, Gal C (2008) Carbamazepine and diclofenac: removal in wastewater treatment plants and occurrence in water bodies. Chemosphere 73:1151–1161PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • A. I. Rodarte-Morales
    • 1
  • G. Feijoo
    • 1
  • M. T. Moreira
    • 1
  • J. M. Lema
    • 1
  1. 1.Department of Chemical Engineering, School of EngineeringUniversity of Santiago de CompostelaSantiago de CompostelaSpain

Personalised recommendations