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Continuous fungal treatment of non-sterile veterinary hospital effluent: pharmaceuticals removal and microbial community assessment

  • Environmental biotechnology
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Abstract

Source point treatment of effluents with a high load of pharmaceutical active compounds (PhACs), such as hospital wastewater, is a matter of discussion among the scientific community. Fungal treatments have been reported to be successful in degrading this type of pollutants and, therefore, the white-rot fungus Trametes versicolor was applied for the removal of PhACs from veterinary hospital wastewater. Sixty-six percent removal was achieved in a non-sterile batch bioreactor inoculated with T. versicolor pellets. On the other hand, the study of microbial communities by means of DGGE and phylogenetic analyses led us to identify some microbial interactions and helped us moving to a continuous process. PhAC removal efficiency achieved in the fungal treatment operated in non-sterile continuous mode was 44 % after adjusting the C/N ratio with respect to the previously calculated one for sterile treatments. Fungal and bacterial communities in the continuous bioreactors were monitored as well.

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References

  • APHA-AWWA-WEF (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Association/AmericaWaterWorks Association/Water Environment Federation, Washington

    Google Scholar 

  • Asgher M, Bhatti HN, Ashraf M, Legge RL (2008) Recent developments in biodegradation of industrial pollutants by white rot fungi and their enzyme system. Biodegradation 19:771–783. doi:10.1007/s10532-008-9185-3

    Article  CAS  PubMed  Google Scholar 

  • Ayache C, Manes C, Pidou M, CrouĂ© JP, Gernjak W (2013) Microbial community analysis of fouled reverse osmosis membranes used in water recycling. Water Res 47:3291–3299. doi:10.1016/j.watres.2013.03.006

    Article  CAS  PubMed  Google Scholar 

  • Badia-Fabregat M, Lucas D, Gros M, RodrĂ­guez-Mozaz S, BarcelĂł D, Caminal G, Vicent T (2015) Identification of some factors affecting pharmaceutical active compounds (PhACs) removal in real wastewater. Case study of fungal treatment of reverse osmosis concentrate. J Hazard Mater 283:663–671. doi:10.1016/j.jhazmat.2014.10.007

    Article  CAS  PubMed  Google Scholar 

  • Blánquez P, Casas N, Font X, Gabarrell X, SarrĂ  M, Caminal G, Vicent T (2004) Mechanism of textile metal dye biotransformation by Trametes versicolor. Water Res 38:2166–2172. doi:10.1016/j.watres.2004.01.019

    Article  PubMed  Google Scholar 

  • Blánquez P, SarrĂ  M, Vicent MT (2006) Study of the cellular retention time and the partial biomass renovation in a fungal decolourisation continuous process. Water Res 40:1650–1656. doi:10.1016/j.watres.2006.02.010

    Article  PubMed  Google Scholar 

  • Blánquez P, SarrĂ  M, Vicent T (2008) Development of a continuous process to adapt the textile wastewater treatment by fungi to industrial conditions. Process Biochem 43:1–7. doi:10.1016/j.procbio.2007.10.002

    Article  Google Scholar 

  • Bruce A, Highley TL (1991) Control of growth of wood decay Basidiomycetes by Trichoderma spp. and other potentially antagonistic fungi. For Prod J 41:63–67

    CAS  Google Scholar 

  • Casas N, Blánquez P, Vicent T, SarrĂ  M (2013) Laccase production by Trametes versicolor under limited-growth conditions using dyes as inducers. Environ Technol 34:113–119. doi:10.1080/09593330.2012.683820

    Article  CAS  PubMed  Google Scholar 

  • Cruz-MoratĂł C, Ferrando-Climent L, Rodriguez-Mozaz S, BarcelĂł D, Marco-Urrea E, Vicent T, SarrĂ  M (2013a) Degradation of pharmaceuticals in non-sterile urban wastewater by Trametes versicolor in a fluidized bed bioreactor. Water Res 47:5200–5210. doi:10.1016/j.watres.2013.06.007

    Article  PubMed  Google Scholar 

  • Cruz-MoratĂł C, RodrĂ­guez-RodrĂ­guez CE, Marco-Urrea E, SarrĂ  M, Caminal G, Vicent T, Jelic A, GarcĂ­a-Galán MJ, PĂ©rez S, DĂ­az-Cruz MS, Petrovic M, BarcelĂł D (2013b) Biodegradation of Pharmaceuticals by Fungi and Metabolites Identification. In: Vicent T, Caminal G, Eljarrat E, BarcelĂł D (eds) Emerg. Org. Contam. Sludges. Springer, pp 165–213

  • Cruz-MoratĂł C, Lucas D, Llorca M, Rodriguez-Mozaz S, Gorga M, Petrovic M, BarcelĂł D, Vicent T, SarrĂ  M, Marco-Urrea E (2014) Hospital wastewater treatment by fungal bioreactor: removal efficiency for pharmaceuticals and endocrine disruptor compounds. Sci Total Environ 493:365–376. doi:10.1016/j.scitotenv.2014.05.117

    Article  PubMed  Google Scholar 

  • EPA (2000) Assigning values to non-detected/non-quantified pesticide residues in human health food exposure assessments. Washington

  • Font X, Caminal G, Gabarrell X, Romero S, Vicent MT (2003) Black liquor detoxification by laccase of Trametes versicolor pellets. J Chem Technol Biotechnol 78:548–554. doi:10.1002/jctb.834

    Article  CAS  Google Scholar 

  • Fujii K, Kikuchi S (2005) Degradation of benzophenone, a potential xenoestrogen, by a yeast isolated from the activated sludge of a sewage treatment plant in Hokkaido. World J Microbiol Biotechnol 21:1311–1315. doi:10.1007/s11274-005-2704-z

    Article  CAS  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for Basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Generalitat de Catalunya (2003) DECRET 130/2003, de 13 de maig, pel qual s’aprova el Reglament dels serveis pĂşblics de sanejament. DOGC 11143–11158

  • Gros M, RodrĂ­guez-Mozaz S, BarcelĂł D (2012) Fast and comprehensive multi-residue analysis of a broad range of human and veterinary pharmaceuticals and some of their metabolites in surface and treated waters by ultra-high-performance liquid chromatography coupled to quadrupole-linear ion trap tandem. J Chromatogr A 1248:104–121. doi:10.1016/j.chroma.2012.05.084

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harms H, Schlosser D, Wick LY (2011) Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol 9:177–192. doi:10.1038/nrmicro2519

    Article  CAS  PubMed  Google Scholar 

  • Joss A, Zabczynski S, Göbel A, Hoffmann B, Löffler D, Mcardell CS, Ternes TA, Thomsen A, Siegrist H (2006) Biological degradation of pharmaceuticals in municipal wastewater treatment: proposing a classification scheme. Water Res 40:1686–1696. doi:10.1016/j.watres.2006.02.014

    Article  CAS  PubMed  Google Scholar 

  • Jurado A, VĂ zquez-Suñé E, Carrera J, LĂłpez de Alda M, Pujades E, BarcelĂł D (2012) Emerging organic contaminants in groundwater in Spain: a review of sources, recent occurrence and fate in a European context. Sci Total Environ 440:82–94. doi:10.1016/j.scitotenv.2012.08.029

    Article  CAS  PubMed  Google Scholar 

  • Kaal EEJ, de Jong E, Field JA (1993) Stimulation of ligninolytic peroxidase activity by nitrogen nutrients in the white rot fungus Bjerkandera sp. Strain BOS55. Appl Environ Microbiol 59:4031–4036

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kovalova L, Siegrist H, Singer H, Wittmer A, McArdell CS (2012) Hospital wastewater treatment by membrane bioreactor: performance and efficiency for organic micropollutant elimination. Environ Sci Technol 46:1536–1545. doi:10.1021/es203495d

    Article  CAS  PubMed  Google Scholar 

  • Libra JA, Borchert M, Banit S (2003) Competition strategies for the decolorization of a textile-reactive dye with the white-rot fungi Trametes versicolor under non-sterile conditions. Biotechnol Bioeng 82:736–744. doi:10.1002/bit.10623

    Article  CAS  PubMed  Google Scholar 

  • Lu Z, Sun X, Yang Q, Li H, Li C (2009) Persistence and functions of a decolorizing fungal consortium in a non-sterile biofilm reactor. Biochem Eng J 46:73–78. doi:10.1016/j.bej.2009.04.017

    Article  CAS  Google Scholar 

  • Marco-Urrea E, PĂ©rez-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. Bioresour Technol 101:2159–2166. doi:10.1016/j.biortech.2009.11.019

    Article  CAS  PubMed  Google Scholar 

  • Mikesková H, NovotnĂ˝ C, Svobodová K (2012) Interspecific interactions in mixed microbial cultures in a biodegradation perspective. Appl Microbiol Biotechnol 95:861–870. doi:10.1007/s00253-012-4234-6

    Article  PubMed  Google Scholar 

  • Millán B, Lucas R, Robles A, GarcĂ­a T, Alvarez de Cienfuegos G, Gálvez A (2000) A study on the microbiota from olive-mill wastewater (OMW) disposal lagoons, with emphasis on filamentous fungi and their biodegradative potential. Microbiol Res 155:143–147. doi:10.1016/S0944-5013(00)80027-0

    Article  PubMed  Google Scholar 

  • Nguyen LN, Hai FI, Yang S, Kang J, Leusch FDL, Roddick F, Price WE, Nghiem LD (2013) Removal of trace organic contaminants by an MBR comprising a mixed culture of bacteria and white-rot fungi. Bioresour Technol 148:234–241. doi:10.1016/j.biortech.2013.08.142

    Article  CAS  PubMed  Google Scholar 

  • NĂĽbel U, Engelen B, Felske A, Snaidr J, Wieshuber A, Amann RI, Ludwig W, Backhaus H (1996) Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol 178:5636–5643

    PubMed Central  PubMed  Google Scholar 

  • Rajala T, Peltoniemi M, Hantula J, Mäkipää R, Pennanen T (2011) RNA reveals a succession of active fungi during the decay of Norway spruce logs. Fungal Ecol 4:437–448. doi:10.1016/j.funeco.2011.05.005

    Article  Google Scholar 

  • RodrĂ­guez-RodrĂ­guez CE, Jelic A, Pereira MA, Sousa DZ, Petrovic M, Alves MM, Barcelo D, Caminal G, Vicent T (2012) Bioaugmentation of sewage sludge with Trametes versicolor in solid-phase biopiles produces degradation of pharmaceuticals and affects microbial communities. Environ Sci Technol 46:12012–12020

    Article  PubMed  Google Scholar 

  • Ruiz-Dueñas FJ, MartĂ­nez MJ (1996) Enzymatic activities of Trametes versicolor and Pleurotus eryngii implicated in biocontrol of Fusarium oxysporum f. sp. lycopersici. Curr Microbiol 32:151–155. doi:10.1007/s002849900027

    Article  Google Scholar 

  • Santos LHMLM, Gros M, Rodriguez-Mozaz S, Delerue-Matos C, Pena A, BarcelĂł D, Montenegro MCBSM (2013) Contribution of hospital effluents to the load of pharmaceuticals in urban wastewaters: identification of ecologically relevant pharmaceuticals. Sci Total Environ 461–462:302–316. doi:10.1016/j.scitotenv.2013.04.077

    Article  PubMed  Google Scholar 

  • Saratale RG, Saratale GD, Chang JS, Govindwar SP (2009) Decolorization and biodegradation of textile dye navy blue HER by Trichosporon beigelii NCIM-3326. J Hazard Mater 166:1421–1428. doi:10.1016/j.jhazmat.2008.12.068

    Article  CAS  PubMed  Google Scholar 

  • Verdin A, Lounès-Hadj Sahraoui A, Newsam R, Robinson G, Durand R (2005) Polycyclic aromatic hydrocarbons storage by Fusarium solani in intracellular lipid vesicles. Environ Pollut 133:283–291. doi:10.1016/j.envpol.2004.05.040

    Article  CAS  PubMed  Google Scholar 

  • Verlicchi P, Galletti A, Petrovic M, BarcelĂł D (2010) Hospital effluents as a source of emerging pollutants: an overview of micropollutants and sustainable treatment options. J Hydrol 389:416–428. doi:10.1016/j.jhydrol.2010.06.005

    Article  CAS  Google Scholar 

  • Verlicchi P, Al Aukidy M, Zambello E (2012) Occurrence of pharmaceutical compounds in urban wastewater: removal, mass load and environmental risk after a secondary treatment--a review. Sci Total Environ 429:123–155. doi:10.1016/j.scitotenv.2012.04.028

    Article  CAS  PubMed  Google Scholar 

  • Wariishi H, Valli K, Gold MH (1992) Manganese(II) oxidation by manganese peroxidase from the basidiomycete Phanerochaete chrysosporium. Kinetic mechanism and role of chelators. J Biol Chem 267:23688–23695

    CAS  PubMed  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    PubMed Central  CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innins MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protoc. Academic, San Diego, p 315

    Google Scholar 

  • Yang Q, Angly FE, Wang Z, Zhang H (2011) Wastewater treatment systems harbor specific and diverse yeast communities. Biochem Eng J 58–59:168–176. doi:10.1016/j.bej.2011.09.012

    Article  Google Scholar 

  • Yang S, Hai FI, Nghiem LD, Nguyen LN, Roddick F, Price WE (2013) Removal of bisphenol A and diclofenac by a novel fungal membrane bioreactor operated under non-sterile conditions. Int Biodeterior Biodegradation 85:483–490. doi:10.1016/j.ibiod.2013.03.012

    Article  CAS  Google Scholar 

  • Zhang Y, Geissen SU (2012) Elimination of carbamazepine in a non-sterile fungal bioreactor. Bioresour Technol 112:221–227. doi:10.1016/j.biortech.2012.02.073

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Authors want to acknowledge the UAB veterinary hospital staff for their kind permission and help for the samplings. This work has been funded by the Spanish Ministry of Economy and Competitiveness and FEDER (projects CTM2013-48545-C2 and AIB2010PT-00169) and supported by the Generalitat de Catalunya (Consolidated Research Groups 2014-SGR-476 and 2014-SGR-291). The Department of Chemical Engineering of the Universitat Autònoma de Barcelona (UAB) is a member of the Xarxa de Referència en Biotecnologia de la Generalitat de Catalunya. M. Badia-Fabregat and D. Lucas acknowledge the predoctoral grants from UAB and from the Spanish Ministry of Education, Culture and Sports (AP-2010-4926), respectively. The authors also thank the Portuguese Foundation for Science and Technology (FCT) Strategic Project PEst-OE/EQB/LA0023/2013, Project FCOMP-01-0124-FEDER-027462 co-funded by Operational Competitiveness Programme, FEDER, and Project “BioEnv—Biotechnology and Bioengineering for a sustainable world,” REF. NORTE-07-0124-FEDER-000048, co-funded by Programa Operacional Regional do Norte (ON.2 – O Novo Norte), QREN, FEDER.

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Correspondence to Glòria Caminal.

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All authors of the article declare that they have no conflict of interest. This article does not contain any studies with human participants or animals performed by any of the authors.

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Marina Badia-Fabregat and Daniel Lucas contributed equally to this work.

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Badia-Fabregat, M., Lucas, D., Pereira, M.A. et al. Continuous fungal treatment of non-sterile veterinary hospital effluent: pharmaceuticals removal and microbial community assessment. Appl Microbiol Biotechnol 100, 2401–2415 (2016). https://doi.org/10.1007/s00253-015-7105-0

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