Skip to main content
SpringerLink
Log in

Decolorization and detoxication of reactive industrial dyes by immobilized fungi Trametes pubescens and Pleurotus ostreatus

  • Published:
Folia Microbiologica Aims and scope Submit manuscript

Abstract

Trametes pubescens and Pleurotus ostreatus, immobilized on polyurethane foam cubes in bioreactors, were used to decolorize three industrial and model dyes at concentrations of 200, 1000 and 2000 ppm. Five sequential cycles were run for each dye and fungus. The activity of laccase, Mn-dependent and independent peroxidases, lignin peroxidase, and aryl-alcohol oxidase were daily monitored during the cycles and the toxicity of media containing 1000 and 2000 ppm of each dye was assessed by the Lemna minor (duckweed) ecotoxicity test. Both fungi were able to efficiently decolorize all dyes even at the highest concentration, and the duckweed test showed a significant reduction (p ≤ 0.05) of the toxicity after the decolorization treatment. T. pubescens enzyme activities varied greatly and no clear correlation between decolorization and enzyme activity was observed, while P. ostreatus showed constantly a high laccase activity during decolorization cycles. T. pubescens showed better decolorization and detoxication capability (compared to the better known P. ostreatus). As wide differences in enzyme activity of the individual strains were observed, the strong decolorization obtained with the two fungi suggested that different dye decolorization mechanisms might be involved.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AAO:

aryl alcohol oxidase

ABTS:

2,2′-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid)

B49:

Reactive Blue 49 (anthraquinone dye)

BOD:

biological oxygen demand

COD:

chemical oxygen demand

DE:

decolorization efficiency

DMAB:

3-dimethylaminobenzoic acid

LiP:

lignin peroxidase

LNMM:

low-nitrogen mineral medium

MBTH:

3-methyl-2-benzothiazolinone hydrazone hydrochloride

MiP:

Mn-independent peroxidase

MnP:

Mn-dependent peroxidase

MUT:

Mycotheca Universitatis Taurinensis

PUF:

polyurethane foam

R243:

Reactive Red 243 (azo dye)

RBBR:

Remazol Brilliat Blue R (anthraquinone dye)

References

  • Abadulla E., Robra K.H., Gubitz G.M., Silva L.M., Cavaco-Paulo A.: Enzymatic decolorization of textile dyeing effluents. Textile Res.J. 70, 409–414 (2000).

    Article  CAS  Google Scholar 

  • Aksu Z.: Application of biosorption for the removal of organic pollutants; review. Proc.Biochem. 40, 997–1026 (2005).

    Article  CAS  Google Scholar 

  • Anastasi A., Varese G.C., Casieri, L., Filipello Marchisio V.: Basidiomycetes from compost and their dye degradation and enzyme activities. Compost Sci. Util. 14, 284–289 (2006).

    CAS  Google Scholar 

  • Bailey J.E., Ollis D.F.: Biochemical Engineering Fundamentals, 2nd ed., p. 984. McGraw-Hill, Singapore 1986.

    Google Scholar 

  • Banat I.M., Nigam P., Singh D., Marchant R.: Microbial decolorization of textile-dye-containing effluents; review. Biores.Technol. 58, 217–227 (1996).

    Article  CAS  Google Scholar 

  • Ben Hamman O., XXXde la Rubia T., Martinez J.: Effect of carbon and nitrogen limitation on lignin peroxidase and manganese peroxidase production by Phanerochaete flavido-alba. J.Appl.Microbiol. 83, 751–757 (1997).

    Article  CAS  Google Scholar 

  • Botella C., XXXde Ory I., Webb C., Cantero D., Blandino A.: Hydrolytic enzyme production by Aspergillus awamori on grape pomade. Biochem.Eng.J. 26, 100–106 (2005).

    Article  CAS  Google Scholar 

  • Bumpus J.A.: Biodegradation of azo dyes by fungi, pp. 457–469 in D.K. Arora (ed.): Fungal Biotechnology in Agricultural, Food, and Environmental Applications. Marcel Dekker, New York-Basel 2004.

    Google Scholar 

  • Capalash N., Prince S.H.A.R.: Biodegradation of textile azo-dyes by Phanerochaete chrysosporium. World J.Microbiol.Biotechnol. 8, 309–312 (1992).

    Article  CAS  Google Scholar 

  • Casieri L.: Biodegradation and biosorption of synthetic dyes by fungi. PhD Thesis. Department of Plant Biology, University of Turin (Italy) 2005.

    Google Scholar 

  • Cecal A., Popa K.: T1-204(+) ions adsorption from the low radioactivity solutions on Lemna minor. Revista Chim. 52, 382–385 (2001).

    CAS  Google Scholar 

  • Cleuvers M.: Aquatic ecotoxicity of pharmaceuticals including the assessment of combination effects. Toxicol.Lett. 142, 185–194 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Cleuvers M., Ratte H.T.: Phytotoxicity of coloured substances: is Lemna duckweed an alternative to the algal growth inhibition test? Chemosphere 49, 9–15 (2002).

    Article  PubMed  CAS  Google Scholar 

  • Couto S.R., Gundin M., Lorenzo M., Sanroman M.N.: Screening of supports and inducers for laccase production by Trametes versicolor in semi-solid-state conditions. Proc.Biochem. 38, 249–255 (2002).

    Article  CAS  Google Scholar 

  • Couto S.R., Sanroman M.A., Hofer D., Gubitz G.M.: Production of laccase by Trametes hirsuta grown in an immersion bioreactor and its application in the decolorization of dyes from a leather factory. Eng.Life Sci. 4, 233–238 (2004).

    Article  CAS  Google Scholar 

  • Easton J.R.: The dye maker’s view, in color in dyehouse effluent, pp. 9–21 in P. Cooper (Ed.): Society of Dyers and Colourists. The Alden Press, Oxford (UK) 1995.

    Google Scholar 

  • Frankart C., Eullaffroy P., Vernet G.: Comparative effects of four herbicides on non-photochemical fluorescence quenching in Lemna minor. Environ.Exper.Bot. 49, 159–168 (2003).

    Article  CAS  Google Scholar 

  • Fu Y.Z., Viraraghavan T.: Fungal decolorization of dye wastewaters; review. Biores.Technol. 79, 251–262 (2001).

    Article  CAS  Google Scholar 

  • Galhaup C., Wagner H., Hinterstoisser B., Haltrich D.: Increased production of laccase by the wood-degrading basidiomycete Trametes pubescens. Enzyme Microb.Technol. 30, 529–536 (2002).

    Article  CAS  Google Scholar 

  • Gottlieb A., Shaw C., Smith A., Wheatley A., Forsythe S.: The toxicity of textile reactive azo dyes after hydrolysis and decolorization. J.Biotechnol. 101, 49–56 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Hofrichter M.: Lignin conversion by manganese peroxidase (MnP); review. Enzyme Microb.Technol. 30, 454–466 (2002).

    Article  CAS  Google Scholar 

  • Hu T.L.: Kinetics of azoreductase and assessment of toxicity of metabolic products from azo dyes by Pseudomonas luteola. Water Sci.Technol. 43, 261–269 (2001).

    PubMed  CAS  Google Scholar 

  • Isik M., Sponza D.T.: Effect of oxygen on decolorization of azo dyes by Escherichia coli and Pseudomonas sp. and fate of aromatic amines. Proc.Biochem. 38, 1183–1192 (2003).

    Article  CAS  Google Scholar 

  • ISO (International Standards Organization) Standards ISO/WD 20079: Water quality — duckweed growth inhibition; determination of the toxic effect of water constituents and waste water to duckweed (Lemna minor) 2001.

  • Jaouani A., Sayadi S., Vanthournhout M., Penninckx M.J.: Potent fungi for decolorization of olive oil mill wastewaters. Enzyme Microb.Technol. 33, 802–809 (2003).

    Article  CAS  Google Scholar 

  • Jarosz-Wilkolazka A., Kochmanska-Rdest J., Malarczyk E., Wardas W., Leonowicz A.: Fungi and their ability to decolorize azo and anthraquinonic dyes. Enzyme Microb.Technol. 30, 566–572 (2002).

    Article  CAS  Google Scholar 

  • Kasinath A., Novotný Č., Svobodová K., Patel K.C., Šašek V.: Decolorization of synthetic dyes by Irpex lacteus in liquid cultures and packed-bed bioreactor. Enzyme Microb.Technol. 32, 167–173 (2003).

    Article  CAS  Google Scholar 

  • Knapp J.S., Newby P.S., Reece L.P.: Decolorization of dyes by wood-rotting basidiomycete fungi. Enzyme Microb.Technol. 17, 664–668 (1995).

    Article  CAS  Google Scholar 

  • Kuhad R.C., Sood N., Tripathi K.K., Singh A., Ward O.P.: Developments in microbial methods for the treatment of dye effluents. Adv.Appl.Microbiol. 56, 185–213 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Li D., Alic M., Gold M.H.: Nitrogen regulation of lignin peroxidase gene-transcription. Appl.Environ.Microbiol. 60, 3447–3449 (1994).

    PubMed  CAS  Google Scholar 

  • Liu W.X., Chao Y.P., Yang X.Q., Bao H.B., Qian S.J.: Biodecolorization of azo, anthraquinonic and triphenylmethane dyes by white-rot fungi and a laccase-secreting engineered strain. J.Industr.Microbiol.Biotechnol. 31, 127–132 (2004).

    Article  CAS  Google Scholar 

  • Malachová K., Pavlíčková Z., Novotný Č., Svobodová K., Lednická S., Musílková E.: Reduction in the mutagenicity of synthetic dyes by successive treatment with activated sludge and the ligninolytic fungus Irpex lacteus. Environ.Mol.Mutagen. 47, 533–540 (2006).

    Article  PubMed  CAS  Google Scholar 

  • Maximo C., Amorim M.T.P., Costa-Ferreira M.: Biotransformation of industrial reactive azo dyes by Geotrichum sp. CCMI 1019. Enzyme Microb.Technol. 32, 145–151 (2003).

    Article  CAS  Google Scholar 

  • McMullan G., Meehan C., Conneely A., Kirby N., Robinson T., Nigam P., Banat I.M., Marchant R., Smyth W.E.: Microbial decolourisation and degradation of textile dyes. Appl.Microbiol.Biotechnol. 56, 81–87 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Milagres A.M.F., Arantes V., Medeiros C.L., Machuca A.: Production of metal chelating compounds by white and brown-rot fungi and their comparative abilities for pulp bleaching. Enzyme Microb.Technol. 30, 562–565 (2002).

    Article  CAS  Google Scholar 

  • Minussi R.C., XXXde Moraes S.G., Pastore G.M., Duran N.: Biodecolorization screening of synthetic dyes by four white-rot fungi in a solid medium: possible role of siderophores. Lett.Appl.Microbiol. 33, 21–25 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Mohan B.S., Hosetti B.B.: Potential phytotoxicity of lead and cadmium to Lemna minor grown in sewage stabilization ponds. Environ.Pollut. 98, 233–238 (1997).

    Article  CAS  Google Scholar 

  • Nachiyar C.V., Rajakumar G.S.: Mechanism of Navitan Fast Blue S5R degradation by Pseudomonas aeruginosa. Chemosphere 57, 165–169 (2004).

    Article  CAS  Google Scholar 

  • Nerud F., Baldrian P., Eichlerová I., Merhautová V., Gabriel J., Homolka L.: Decolorization of dyes using white-root fungi and radical-generating reactions. Biocatal.Biotransform. 22, 325–330 (2004).

    Article  CAS  Google Scholar 

  • Niku-Paavola M.L., Karhunen E., Salola P., Raunio V.: Ligninolytic enzymes of the white-rot fungus Phlebia radiata. Biochem.J. 254, 877–884 (1988).

    PubMed  CAS  Google Scholar 

  • Novotný Č., Svobodová K., Kasinath A., Erbanová P.: Biodegradation of synthetic dyes by Irpex lacteus under various growth conditions. Internat.Biodeter.Biodegrad. 54, 215–223 (2004).

    Article  CAS  Google Scholar 

  • Novotný Č., Svobodová K., Sklenář J., Erbanová P., Kováčová N., Schoeberl P., Fuchs W., Řehořek A., Pavko A.: Irpex lacteus: selection and application to bioremediation of contaminated water, pp. 239–243 in W. Meyer, C. Pearse (Eds): 8th Internat. Mycological Congress, Cairns (Australia) 2005; Medimond International Proceedings, Medimond S.r.l., Bologna (Italy) 2006.

  • Palmieri G., Giardina P., Sannia G.: Laccase-mediated Remazol Brilliant Blue R decolorization in a fixed-bed bioreactor. Biotechnol.Progr. 21, 1436–1441 (2005).

    Article  CAS  Google Scholar 

  • Pandey A.: Solid-state fermentation. Biochem.Eng.J. 13, 81–84 (2003).

    Article  CAS  Google Scholar 

  • Pandey A., Selvakumar P., Soccol C.R., Nigam P.: Solid state fermentation for the production of industrial enzymes. Curr.Sci. 77, 149–162 (1999).

    CAS  Google Scholar 

  • Paterson R.R.M., Bridge P.D.: Enzymatic activities on solid media. Ligninase activity, pp. 23–24 in R.R.M. Paterson, P.D. Bridge (Eds): Biochemical Techniques for Filamentous Fungi. CAB International, Wallington-Oxon (UK) 1994.

    Google Scholar 

  • Rabinovich M.L., Bolobova A.V., Vasil’chenko L.G.: Fungal decomposition of natural aromatic structures and xenobiotics; review. Appl.Biochem.Microbiol. 40, 1–17 (2004).

    Article  CAS  Google Scholar 

  • Robinson T., McMullan G., Marchant R., Nigam P.: Remediation of dyes in textile effluent: a critical review on current treatment technologies with a proposed alternative. Biores.Technol. 77, 247–255 (2001).

    Article  CAS  Google Scholar 

  • Rodriguez E., Nuero O., Guillen F., Martinez A.T., Martinez M.J.: Degradation of phenolic and non-phenolic aromatic pollutants by four Pleurotus species: the role of laccase and versatile peroxidase. Soil Biol.Biochem. 36, 909–916 (2004).

    Article  CAS  Google Scholar 

  • Saparrat M.C.N., Guillén F.: Ligninolytic ability and potential biotechnology application of the South American fungus Pleurotus laciniatocrenatus. Folia Microbiol. 50, 155–160 (2005).

    Article  CAS  Google Scholar 

  • Šašek V., Vitásek J., Chromcová D., Prokopová I., Brožek J., Náhlík J.: Biodegradation of synthetic polymers by composting and fungal treatment. Folia Microbiol. 51, 425–430 (2006).

    Article  Google Scholar 

  • Selvam K., Swaminathan K., Chae K.S.: Microbial decolorization of azo dyes and dye industry effluent by Fomes lividus. World J.Microbiol.Biotechnol. 19, 591–593 (2003).

    Article  CAS  Google Scholar 

  • Severi A.: Aluminium toxicity in Lemna minor L.: effects of citrate and kinetin. Environ.Exp.Bot. 37, 53–61 (1997).

    Article  CAS  Google Scholar 

  • Severi A.: Toxicity of selenium to Lemna minor in relation to sulfate concentration. Physiol.Plant. 113, 523–532 (2001).

    Article  CAS  Google Scholar 

  • Shin M., Nguyen T., Ramsay J.A.: Evaluation of support materials for the surface immobilization and decolorization of amaranth by Trametes versicolor. Appl.Microbiol.Biotechnol. 60, 218–223 (2002).

    Article  PubMed  CAS  Google Scholar 

  • Šnajdr J., Baldrian P.: Production of lignocellulose-degrading enzymes and changes in soil bacterial communities during the growth of Pleurotus ostreatus in soil with different carbon content. Folia Microbiol. 51, 579–590 (2006).

    Article  Google Scholar 

  • Šnajdr J., Baldrian P.: Temperature affects the production, activity and stability of ligninolytic enzymes in Pleurotus ostreatus and Trametes versicolor. Folia Microbiol. 52, 498–502 (2007).

    Article  Google Scholar 

  • Svobodová K., Erbanová P., Sklenář J., Novotný Č.: The role of Mn-dependent peroxidase in dye decolorization by static and agitated cultures of Irpex lacteus. Folia Microbiol. 51, 573–578 (2006).

    Article  Google Scholar 

  • Swamy J., Ramsay J.A.: Effects of glucose and NH4 + concentrations on sequential dye decoloration by Trametes versicolor. Enzyme Microb.Technol. 25, 278–284 (1999).

    Article  CAS  Google Scholar 

  • Tavčar M., Svobodová K., Kuplenk J., Novotný Č., Pavko A.: Biodegradation of organic azo dye R016 in various types of reactors with immobilized Irpex lacteus. Acta Chim.Sloven. 53, 338–343 (2006).

    Google Scholar 

  • Tekere M., Zvauya R., Read J.S.: Ligninolytic enzyme production in selected sub-tropical white rot fungi under different culture conditions. J.Basic Microbiol. 41, 115–129 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Tien M., Kirk T.K.: Lignin peroxidase of Phanerochaete chrysosporium. Methods Enzymol. 161, 238–249 (1988).

    Article  CAS  Google Scholar 

  • Tkalec M., Vidakovic-Cifrek Z., Regula I.: The effect of oil industry “high density brines” on duckweed Lemna minor L. Chemosphere 37, 2703–2715 (1998).

    Article  CAS  Google Scholar 

  • Tychanowicz G.K., Zilly A., De Souza C.G.M., Peralta R.M.: Decolorization of industrial dyes by solid-state cultures of Pleurotus pulmonarius. Proc.Biochem. 39, 855–859 (2004).

    Article  CAS  Google Scholar 

  • Vandevivere P.C., Bianchi R., Verstraete W.: Treatment and reuse of wastewater from the textile wet-processing industry: review of emerging technologies. J.Chem.Technol.Biotechnol. 72, 289–302 (1998).

    Article  CAS  Google Scholar 

  • Verma P., Madamwar D.: Decolorization of synthetic textile dyes by lignin peroxidase of Phanerochaete chrysosporium. Folia Microbiol. 47, 283–286 (2002).

    Article  CAS  Google Scholar 

  • Vidakovic-Cifrek Z., Tkalec M., Horvatic J., Regula I.: Effects of oil industry high density brines in miniaturized algal growth bioassay and Lemna test. Phyton-Annal.Rei Botan. 39, 193–197 (1999).

    CAS  Google Scholar 

  • Vyas B.R.M., Volc J., Šašek V.: Effects of temperature on the production of manganese peroxidase and lignin peroxidase by Phanerochaete chrysosporium. Folia Microbiol. 39, 19–22 (1994).

    Article  CAS  Google Scholar 

  • Wang Y.X., Yu J.: Adsorption and degradation of synthetic dyes on the mycelium of Trametes versicolor. Water Sci.Technol. 38, 233–238 (1998).

    Article  CAS  Google Scholar 

  • Waters B.D.: The regulator’s view, in color in dyehouse effluent, pp. 22–30 in P. Cooper (Ed.): Society of Dyers and Colorists. The Alden Press, Oxford (UK) 1995.

    Google Scholar 

  • Wesenberg D., Kyriakides I., Agathos S.N.: White-rot fungi and their enzymes for the treatment of industrial dye effluents. Biotechnol.Adv. 22, 161–187 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Yang F.C., Yu J.T.: Development of a bioreactor system using an immobilized white rot fungus for decolorization. 1. Cell immobilization and repeated-batch decolorization tests. Bioproc.Eng. 15, 307–310 (1996).

    Article  Google Scholar 

  • Yesilada O., Cing S., Asma D.: Decolorization of the textile dye Astrazon Red FBL by Funalia trogii pellets. Biores.Technol. 81, 155–157 (2002).

    Article  CAS  Google Scholar 

  • Yesilada O., Asma D., Cing S.: Decolorization of textile dyes by fungal pellets. Proc.Biochem. 38, 933–938 (2003).

    Article  CAS  Google Scholar 

  • Zhao X.H., Lu Y.P., Hardin I.: Determination of biodegradation products from sulfonated dyes by Pleurotus ostreatus using capillary electrophoresis coupled with mass spectrometry. Biotechnol.Lett. 27, 69–72 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Zheng Z.X., Levin R.E., Pinkham J.L., Shetty K.: Decolorization of polymeric dyes by a novel Penicillium isolate. Proc.Biochem. 34, 31–37 (1999).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant Biology, University of Turin, Mycotheca Universitatis Taurinensis, 10125, Turin, Italy

    L. Casieri, G. C. Varese, A. Anastasi, V. Prigione & V. Filippelo Marchisio

  2. Laboratory of Experimental Mycology, Institute of Microbiology, Academy of Sciences of the Czech Republic, 142 20, Prague, Czechia

    K. Svobodová & Č. Novotný

Authors
  1. L. Casieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. C. Varese
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Anastasi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. V. Prigione
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. K. Svobodová
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. V. Filippelo Marchisio
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Č. Novotný
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. Casieri.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Casieri, L., Varese, G.C., Anastasi, A. et al. Decolorization and detoxication of reactive industrial dyes by immobilized fungi Trametes pubescens and Pleurotus ostreatus . Folia Microbiol 53, 44–52 (2008). https://doi.org/10.1007/s12223-008-0006-1

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12223-008-0006-1

Keywords

Search

Navigation