Abstract
The combination of a laccase–hydroxybenzotriazole (HBT) mediator system with/without cellobiose dehydrogenase (CDH) or an additional Fenton reaction step for the elimination and/or detoxification of phenolic compounds in dry olive mill residues (DOR) and liquid olive mill wastewaters (OMW) was evaluated. The laccase–HBT–CDH and laccase–HBT–CDH–Fenton system were the most effective, removing at least 69 and 72 % of phenolic compounds from a total of 698 and 683 mg in OMW and DOR, respectively, in 12 h. The efficient removal of phenolic compounds was also accompanied by >80 % reduction in biochemical oxygen demand and chemical oxygen demand in both DOR and OMW. Microbial community analysis using single-strand conformation polymorphism (SSCP) gels showed that biogas reactors supplemented with untreated and laccase–HBT–CDH–Fenton-treated DOR and OMW strongly inhibited growth of microorganisms. In contrast, the laccase–HBT- and laccase–HBT–CDH-pretreated OMW and DOR were detoxified as evidenced by SSCP analysis, which also indicated a distinct sensitivity of the individual members of the anaerobic population toward the toxicants. Further, although the laccase–HBT–CDH–Fenton system was effective in bleaching and removing phenolic compounds in both OMW and DOR, it was not able to support methane production. However, laccase–HBT and laccase–HBT–CDH indeed supported biogas production. This study therefore shows that the laccase–HBT–CDH system has a potential for the detoxification of olive mill residues, which can be potentially used as substrates for downstream processes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abadulla E, Tzanov T, Costa S, Robra K, Cavaco-Paulo A, Gübitz GM (2000) Decolorization and detoxification of textile dyes with a Laccase from Trametes hirsuta. Appl Environ Microbiol 66:3357–3362
Afify AS, Mahmoud MA, Emara HA, Abdelkreem KL (2009) Phenolic compounds and COD removal from olive mill wastewater by chemical and biological procedures. AJBAS 3:1087–1095
Alcalde M (2007) Laccases: biological functions, molecular structure and industrial applications. In: Polaina J, MacCabe A (eds) Industrial enzymes: structure, function and applications. Springer, Netherlands, pp 461–476
Almansa E, Kandelbauer A, Pereira L, Cavaco-Paulo A, Guebitz GM (2004) Influence of structure on dye degradation with laccase mediator systems. Biocatal Biotransform 22:315–324
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Aranda E, García-Romera I, Ocampo JA, Carbone V, Mari A, Malorni A, Sannino F, De Martino A, Capasso R (2007) Chemical characterization and effects on Lepidium sativum of the native and bioremediated components of dry olive mill residue. Chemosphere 69:229–239
Aranda E, Sampedro I, Daaz R, Garcia-Sa¡nchez M, Arriagada CA, Ocampo JA, Garcia-Romera I (2009) The effects of the arbuscular mycorrhizal fungus Glomus deserticola on growth of tomato plants grown in the presence of olive mill residues modified by treatment with saprophytic fungi. Symbiosis 47:133–140
Aranda E, Sampedro I, Díaz R, García-Sánchez M, Siles JA, Ocampo JA, García-Romera I (2010) Dry matter and root colonization of plants by indigenous arbuscular mycorrhizal fungi with physical fractions of dry olive mill residue inoculated with saprophytic fungi. Span J Agric Res 8:S79–S85
Baminger U, Nidetzky B, Kulbe KD, Haltrich D (1999) A simple assay for measuring cellobiose dehydrogenase activity in the presence of laccase. J Microbiol Methods 35:253–259
Bassam BJ, Caetano-Anollés G, Gresshoff PM (1991) Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem 196:80–83
Blika PS, Stamatelatou K, Kornaros M, Lyberatos G (2009) Anaerobic digestion of olive mill wastewater. Glob NEST J 11:364–372
Dermeche S, Nadoura M, Larroche C, Moulti-Matia F, Michaud P (2013) Olive mill wastes: biochemical characterizations and valorization strategies. Process Biochem 48:1532–1552
Durão P, Bento I, Fernandes A, Melo E, Lindley P, Martins L (2006) Perturbations of the T1 copper site in the CotA laccase from Bacillus subtilis: structural, biochemical, enzymatic and stability studies. JBIC 11:514–526
Eaton AD, Clesceri LS, Rice EW, Greenberg AE (2005) Standard methods for the examination of water and wastewater. APHA, Washington, DC
Field JA, Lettinga G (1989) The effect of oxidative coloration on the methanogenic toxicity and anaerobic biodegradability of phenols. Biol Wastes 29:161–179
Flitsch A, Nugroho Prasetyo E, Sygmund C, Ludwig R, Nyanhongo GS, Guebitz GM (2013) Cellulose oxidation and bleaching processes based on recombinant Myriococcum thermophilum cellobiose dehydrogenase. Enzyme Microb Technol 52:60–67
Friedmann H, Görtz G, Helm M, Kaltschmitt M, Knopf U, Kretschmer A, Kübler H, Langhans G, Linke B, Pätz R, Rosenwinkel K, Shan M, Weiland P, Wendler D, Zellmann H, Konstantinidou E (2004) Vergärung organischer Stoffe (VDI 4630). In: Ingenieure VD (ed) VDI-Handbuch Energietechnik. Beuth Publishing, Berlin, Düsseldorf, Germany, pp 1–48
Gelegenis J, Georgakakis D, Angelidaki I, Christopoulou N, Goumenaki M (2007) Optimization of biogas production from olive-oil mill wastewater, by codigesting with diluted poultry-manure. Appl Energy 84:646–663
Kudanga T, Burton S, Nyanhongo GS, Guebitz GM (2012) Versatility of oxidoreductases in the remediation of environmental pollutants. Front Biosci 4:1127–1149
Ludwig R, Harreither W, Tasca F, Gorton L (2010) Cellobiose dehydrogenase: a versatile catalyst for electrochemical applications. ChemPhysChem 11:2674–2697
Martin-Laurent F, Philippot L, Hallet S, Chaussod R, Germon JC, Soulas G, Catroux G (2001) DNA extraction from soils: old bias for new microbial diversity analysis methods. Appl Environ Microbiol 67:2354–2359
Martirani L, Giardina P, Marzullo L, Sannia G (1996) Reduction of phenol content and toxicity in olive oil mill waste waters with the ligninolytic fungus Pleurotus ostreatus. Water Res 30:1914–1918
Ntougias S, Baldrian P, Ehaliotis C, Nerud F, Antoniou T, Merhautová V, Zervakis GI (2012) Biodegradation and detoxification of olive mill wastewater by selected strains of the mushroom genera Ganoderma and Pleurotus. Chemosphere 88:620–626
Nugroho Prasetyo E, Kudanga T, Østergaard L, Rencoret J, Gutiérrez A, del Río JC, Ignacio Santos J, Nieto L, Jiménez-Barbero J, Martínez AT, Li J, Gellerstedt G, Lepifre S, Silva C, Kim SY, Cavaco-Paulo A, Seljebakken Klausen B, Lutnaes BF, Nyanhongo GS, Guebitz GM (2010) Polymerization of lignosulfonates by the laccase–HBT (1-hydroxybenzotriazole) system improves dispersibility. Bioresour Technol 101:5054–5062
Nyanhongo GS, Gomes J, Gübitz GM, Zvauya R, Read J, Steiner W (2002) Decolorization of textile dyes by laccases from a newly isolated strain of Trametes modesta. Water Res 36:1449–1456
Nyanhongo GS, Sygmund C, Ludwig R, Nugroho Prasetyo E, Guebitz GM (2013) An antioxidant regenerating system for continuous quenching of free radicals in chronic wounds. Eur J Pharm Biopharm 83(3):396–404
Osono T, Takeda H (1999) Decomposing ability of interior and surface fungal colonizers of beech leaves with reference to lignin decomposition. Eur J Soil Biol 35:51–56
Ouzounidou G, Zervakis GI, Gaitis F (2010) Raw and microbiologically detoxified olive mill waste and their impact on plant growth. Terres Aqua Environ Toxicol 4:21–38
Paraskeva P, Diamadopoulos E (2006) Technologies for olive mill wastewater (OMW) treatment: a review. J Chem Technol Biotechnol 81:1475–1485
Peschel W, Sánchez-Rabaneda F, Diekmann W, Plescher A, Gartzía I, Jiménez D, Lamuela-Raventós R, Buxaderas S, Codina C (2006) An industrial approach in the search of natural antioxidants from vegetable and fruit wastes. Food Chem 97:137–150
Ramosa P, Santos SAO, Guerraa AR, Guerreiro O, Felício L, Jerónimo E, Silvestre AJD, Neto CP, Duarte M (2013) Valorization of olive mill residues: Antioxidant and breast cancer antiproliferative activities of hydroxytyrosol-rich extracts derived from olive oil by-products. Ind Crops Prod 46:359–368
Rodríguez Couto S, Sanromán M, Gübitz GM (2005) Influence of redox mediators and metal ions on synthetic acid dye decolourization by crude laccase from Trametes hirsuta. Chemosphere 58:417–422
Sampedro I, D’Annibale A, Ocampo JA, Stazi SR, García-Romera I (2007a) Solid-state cultures of Fusarium oxysporum transform aromatic components of olive-mill dry residue and reduce its phytotoxicity. Bioresour Technol 98:3547–3554
Sampedro I, Marinari S, D’Annibale A, Grego S, Ocampo JA, García-Romera I (2007b) Organic matter evolution and partial detoxification in two-phase olive mill waste colonized by white-rot fungi. Int Biodeterior Biodegrad 60:116–125
Sampedro I, Aranda E, Díaz R, García-Sanchez M, Ocampo JA, García-Romera I (2008) Saprobe fungi decreased the sensitivity to the toxic effect of dry olive mill residue on arbuscular mycorrhizal plants. Chemosphere 70:1383–1389
Sampedro I, Cajthaml T, Marinari S, Petruccioli M, Grego S, D’Annibale A (2009) Organic matter transformation and detoxification in dry olive mill residue by the saprophytic fungus Paecilomyces farinosus. Process Biochem 44:216–225
Schmidhalter DR, Canevascini G (1993) Isolation and characterization of the cellobiose dehydrogenase from the brown-rot fungus Coniophora puteana (Schum ex Fr.) Karst. Arch Biochem Biophys 300:559–563
Schwieger F, Tebbe CC (1998) A new approach to utilize PCR–single-strand-conformation polymorphism for 16S rRNA gene-based microbial community analysis. Appl Environ Microbiol 64:4870–4876
Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomoly diphosphotungstic acid reagents. Am J Enol Viticult 16:144–158
Volante A, Lingua G, Cesaro P, Cresta A, Puppo M, Ariati L, Berta G (2005) Influence of three species of arbuscular mycorrhizal fungi on the persistence of aromatic hydrocarbons in contaminated substrates. Mycorrhiza 16:43–50
Acknowledgments
The authors are grateful for the financial support given by the K-project “Future Lignin and Pulp Processing Research” (FLIPPR).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nugroho Prasetyo, E., Rodríguez, R.D., Lukesch, B. et al. Laccase–cellobiose dehydrogenase-catalyzed detoxification of phenolic-rich olive processing residues. Int. J. Environ. Sci. Technol. 12, 1343–1352 (2015). https://doi.org/10.1007/s13762-014-0526-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13762-014-0526-y