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Enhanced reduction of phenol content and toxicity in olive mill wastewaters by a newly isolated strain of Coriolopsis gallica

Abstract

The search for novel microorganisms able to degrade olive mill wastewaters (OMW) and withstand the toxic effects of the initially high phenolic concentrations is of great scientific and industrial interest. In this work, the possibility of reducing the phenolic content of OMW using new isolates of fungal strains (Coriolopsis gallica, Bjerkandera adusta, Trametes versicolor, Trichoderma citrinoviride, Phanerochaete chrysosporium, Gloeophyllum trabeum, Trametes trogii, and Fusarium solani) was investigated. In vitro, all fungal isolates tested caused an outstanding decolorization of OMW. However, C. gallica gave the highest decolorization and dephenolization rates at 30 % v/v OMW dilution in water. Fungal growth in OMW medium was affected by several parameters including phenolic compound concentration, nitrogen source, and inoculum size. The optimal OMW medium for the removal of phenolics and color was with the OMW concentration (in percent)/[(NH4)2SO4]/inoculum ratio of 30:6:3. Under these conditions, 90 and 85 % of the initial phenolic compounds and color were removed, respectively. High-pressure liquid chromatography analysis of extracts from treated and untreated OMW showed a clear and substantial reduction in phenolic compound concentrations. Phytotoxicity, assessed using radish (Raphanus sativus) seeds, indicated an increase in germination index of 23–92 % when a 30 % OMW concentration was treated with C. gallica in different dilutions (1/2, 1/4, and 1/8).

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References

  • Ahmadi M, Vahabzadeh F, Bonakdarpour B, Mehranian M (2006) Empirical modeling of olive oil mill wastewater treatment using loofa-immobilized. Process Biochem 41(5):1148–1154

    CAS  Article  Google Scholar 

  • Aktas ES, Imra S, Ersoy L (2001) Characterization and lime treatment of olive mill wastewater. Water Res 35(9):2336–2340

    CAS  Article  Google Scholar 

  • Alaoui SM, Merzouki M, Penninckx MJ, Benlemlih M (2008) Relationship between cultivation mode of white rot fungi and their efficiency for olive oil mill wastewaters treatment. Electron J Biotechnol 11:1–8

    Google Scholar 

  • Aloui F, Abid N, Roussos S, Sayadi S (2007) Decolorization of semisolid olive residues of “alperujo” during the solid state fermentation by Phanerochaete chrysosporium, Trametes versicolor, Pycnoporus cinnabarinus and Aspergillus niger. Biochem Eng J 35(2):120–125

    CAS  Article  Google Scholar 

  • Amaral C, Lucas MS, Sampaio A, Peres JA, Dias AA, Peixoto F, Anjos MDR, Pais C (2012) Biodegradation of olive mill wastewaters by a wild isolate of Candida oleophila. Int Biodeterior Biodegrad 68(6):45–50

    CAS  Article  Google Scholar 

  • APHA, AWWA, WEF (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Health Association, Washington, DC

    Google Scholar 

  • Arvanitoyannis IS, Kassaveti A, Stefanatos S (2007) Olive oil waste treatment: a comparative and critical presentation of methods, advantages disadvantages. Crit Rev Food Sci 47(3):187–229

    CAS  Article  Google Scholar 

  • Asfi M, Ouzounidou G, Moustakas M (2012) Evaluation of olive oil mill wastewater toxicity on spinach. Environ Sci Pollut Res 19(6):2363–2371

    CAS  Article  Google Scholar 

  • Atanassova D, Kefalas P, Petrakis C, Mantzavinos D, Kalogerakis N, Psillakis E (2005) Sonochemical reduction of the antioxidant activity of olive mill wastewater. Environ Int 31(2):275–280

    CAS  Article  Google Scholar 

  • Aytar P, Gedikli S, Çelikdemir M, Uzuner S, Farizoğlu B, Şam M, Çabuk A, Sağlam N (2011) Dephenolization of olive mill wastewater by pellets of some white rot fungi. Hacet J Biol Chem 39(4):379–390

    Google Scholar 

  • Baldrian P, Zervakis GI, Merhautová V, Ntougias S, Ehaliotis C, Nerud F (2006) The use of hydroxyl-radical-generating systems for the treatment of olive mill wastewaters. Folia Microbiol 51(4):337–341

    Google Scholar 

  • Ben-Sassi A, Boularbah A, Jaouad A, Walker G, Boussaid A (2006) A comparison of olive oil mill wastewaters (OMW) from three different processes in Morocco. Process Biochem 41(1):74–78

    CAS  Article  Google Scholar 

  • Box JD (1983) Investigation of the Folin–Ciocalteu phenol reagent for the determination of polyphenolic substances in natural waters. Water Res 17(5):511–525

    CAS  Article  Google Scholar 

  • Cabana H, Jiwan JL, Rozenberg R, Elisashvili V, Penninckx M, Agathos SN, Jones JP (2007) Elimination of endocrine disrupting chemicals nonylphenol and bisphenol A and personal care product ingredient triclosan using enzyme preparation from the white rot fungus Coriolopsis polyzona. Chemosphere 67(4):770–778

    CAS  Article  Google Scholar 

  • Casa R, D’Annibale A, Pieruccetti F, Stazi SR, Sermanni GG, Lo Cascio B (2003) Reduction of the phenolic components in olive-mill wastewater by an enzymatic treatment and its impact on durum wheat (Triticum durum Desf.) germinability. Chemosphere 50(8):959–966

    CAS  Article  Google Scholar 

  • Clesceri LS, Greenberg AE, Eaton AD (1998) Standard methods for the examination of water and wastewater. American Public Health Association (APHA), Washington, DC

    Google Scholar 

  • Coskun T, Debik E, Demir NM (2010) Treatment of olive mill wastewaters by nanofiltration and reverse osmosis membranes. Desalination 259(1–3):65–70

    CAS  Article  Google Scholar 

  • D’Annibale A, Brozzoli V, Crognale S, Gallo AM, Federici F, Petruccioli M (2006) Optimisation by response surface methodology of fungal lipase production on olive mill wastewater. J Chem Technol Biotechnol 81(9):1586–1593

    Article  Google Scholar 

  • Dhouib A, Aloui F, Hamad N, Sayadi S (2006) Pilot-plant treatment of olive mill wastewaters by Phanerochaete chrysosporium coupled to anaerobic digestion and ultrafiltration. Process Biochem 41(1):159–167

    CAS  Article  Google Scholar 

  • Díaz R, Saparrat MCN, Jurado M (2010) Biochemical and molecular characterization of Coriolopsis rigida laccases involved in transformation of the solid waste from olive oil production. Appl Microbiol Biol 88(1):133–142

    Article  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith P (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356

    CAS  Article  Google Scholar 

  • El Hajjouji H, Barje F, Pinelli E, Bailly JR, Richard C, Winterton P, Revel JC, Hafidi M (2008) Photochemical UV/TiO2 treatment of olive mill wastewater (OMW). Bioresource Technol 99(15):7264–7269

    Article  Google Scholar 

  • El-Abbassi A, Hafidi A, Khayet M, García-Payo MC (2012) Integrated direct contact membrane distillation for olive mill wastewater treatment. Desalination 323:31–38

    Google Scholar 

  • Ergul FE, Sarging S, Ongen G, Sukan FV (2009) Dephenolisation of olive mill wastewater using adapted Trametes versicolor. Int Biodeterior Biodegrad 63(1):1–6

    CAS  Article  Google Scholar 

  • Fadil K, Chahlaoui A, Ouahbi A, Zaid A, Borja R (2003) Aerobic biodegradation and detoxification of wastewaters form the olive oil industry. Int Biodeterior Biodegrad 51(1):37–41

    CAS  Article  Google Scholar 

  • Fenice M, Sermanni GG, Federici F, D’Annibale A (2003) Submerged and solid-state bioprocesses for laccase and manganese-peroxidase production by Panus tigrinus on olive-mill wastewater-based media. J Biotechnol 100:77–85

    CAS  Article  Google Scholar 

  • Fezzani B, Cheikh RB (2008) Implementation of IWA anaerobic digestion model no. 1 (ADM1) for simulating the thermophilic anaerobic co-digestion of olive mill wastewater with olive mill solid waste in a semi-continuous tubular digester. Chem Eng J 141(1–3):75–88

    CAS  Article  Google Scholar 

  • Fountoulakis MS, Dokianakis SN, Kornaros ME, Aggelis GG, Lyberatos G (2002) Removal of phenolics in olive mill wastewaters using the white-rot fungus Pleurotus ostreatus. Water Res 36(19):4735–4744

    CAS  Article  Google Scholar 

  • Gonçalves C, Lopes M, Ferreira JP, Belo I (2009) Biological treatment of olive mill wastewater by non-conventional yeasts. Bioresour Technol 100(15):3759–3763

    Article  Google Scholar 

  • Hamdi M, Garcia JL, Ellouz R (1992) Integrated biological process for olive mill wastewater treatment. Bioprocess Eng 8(1–2):79–84

    CAS  Article  Google Scholar 

  • Hodaifa G, Martinez ME, Orpez R, Sanchez S (2012) Inhibitory effects of industrial olive-oil mill wastewater on biomass production of Scenedesmus obliquus. Ecol Eng 42:30–34

    Article  Google Scholar 

  • Hytiris N, Kapellakis IE, de la Roij R, Tsagarakis KP (2004) The potential use of olive mill sludge in solidification process. Resour Conserv Recycl 40(2):129–139

    Article  Google Scholar 

  • IOOC (International Olive Oil Council) (2008) Available at http://www.internationaloliveoil.org

  • Jaouani A, Sayadi S, Vanthournhout M, Penninckx MJ (2003) Potent fungi for decolourisation of olive oil mill wastewaters. Enzyme Microb Technol 33(6):802–809

    CAS  Article  Google Scholar 

  • Kiril-Mert B, Yonar T, Yalili Kiliç M, Kestioǧlu K (2010) Pre-treatment studies on olive oil mill effluent using physicochemical, Fenton and Fenton-like oxidations processes. J Hazard Mater 174(1–3):122–128

    Article  Google Scholar 

  • Komilis DP, Karatzas E, Halvadakis CP (2005) The effect of olive mill wastewater on seed germination after various pretreatment techniques. J Environ Manage 74(4):339–348

    CAS  Article  Google Scholar 

  • Lakhtar H, Alaoui MI, Philippoussis A, Gaime IP, Roussos S (2010) Screening of strains of Lentinula edodes grown on model olive mill wastewater in solid and liquid state culture for polyphenol biodegradation. Int Biodeterior Biodegrad 64(1–2):167–172

    CAS  Article  Google Scholar 

  • Lee TH, Han YH (2005) Cultural Characteristics for the Enhanced Mycelial Growth of Ramaria botrytis. Mycobiology 33(1):12–14

    Google Scholar 

  • Lucas MS, Beltrán-Heredia J, Sanchez-Martin J, Garcia J, Peres JA (2013) Treatment of high strength olive mill wastewater by Fenton’s reagent and aerobic biological process. J Environ Sci Health, Part A: Tox Hazard Subst Environ Eng 48(8):954–962

    CAS  Article  Google Scholar 

  • McNamara CJ, Anastasious CC, O’Flaherty V, Mitchell R (2008) Bioremediation of olive mill wastewater. Int Biodeterior Biodegrad 6(2):127–134

    Article  Google Scholar 

  • Mwangi ESK, Gatebe EG, Ndungu MW (2012) Impact of nutritional (C:N ratio and source) on growth, oxalate accumulation, and culture pH by Sclerotinia sclerotiorum. J Biol Agri Healthc 2(10):2224–3208

    Google Scholar 

  • Niaounakis M, Halvadakis CP (2006) Olive processing waste management: literature review and patent survey, 2nd edn. Waste management series 5. Pergamon, Oxford, 514 pp

  • 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(5):620–626

    CAS  Article  Google Scholar 

  • Olivieri G, Russo ME, Giardina P, Marzocchella A, Sannia G, Salatino P (2012) Strategies for dephenolization of raw olive mill wastewater by means of Pleurotus ostreatus. J Ind Microbiol Biotechnol 39(5):719–729

    CAS  Article  Google Scholar 

  • Paraskeva P, Diamadopoulos E (2006) Technologies for olive mill wastewater (OMW) treatment: a review. J Chem Technol Biotechnol 81(9):1475–1485

    CAS  Article  Google Scholar 

  • Paredes C, Bernal MP, Cegarra J, Roig A (2002) Bio-degradation of olive mill wastewater sludge by its co-composting with agricultural wastes. Bioresour Technol 85(1):1–8

    CAS  Article  Google Scholar 

  • Paszczyński A, Crawford RL, Huynh VB (1988) Manganese peroxidase of Phanerochaete chrysosporium: purification. Method Enzymol 161(C):264–270

    Article  Google Scholar 

  • Piotrowska A, Rao MA, Scotti R, Gianfreda L (2011) Changes in soil chemical and biochemical properties following amendment with crude and dephenolized olive mill waste water (OMW). Geoderma 161(1–2):8–17

    CAS  Article  Google Scholar 

  • Piperidou C, Chaidou C, Stalikas C, Soulti K, Pilidis G, Balis C (2000) Bioremediation of olive oil mill wastewater: chemical alterations induced by Azotobacter vinelandii. J Agric Food Chem 48(5):1941–1948

    CAS  Article  Google Scholar 

  • Rinaldi M, Rana G, Introna M (2003) Olive mill wastewater spreading in southern Italy: effect on a durum wheat crop. Field Crop Res 84(3):319–326

    Article  Google Scholar 

  • Sampedro I, Marinari S, Ocampo JA, García-Romera I, Petruccioli M, Federici F, D’Annibale A (2008) The use of immobilized white-rot fungi reduces the time requirements and improves detoxification of two-phase dry olive mill residue. In: Electronic Proceedings of the 4th European Bioremediation Conference, Chania, Greece, ID071

  • Saparrat MCN, Martínez MJ, Tournier HA, Cabello MN, Arambarri AM (2000) Production of ligninolytic enzymes by Fusarium solani strains isolated from different substrata. World J Microbiol Biotechnol 16(8–9):799–803

    CAS  Article  Google Scholar 

  • Sarika R, Kalogerakis N, Mantzavinos D (2005) Treatment of olive mill effluents: part II. Complete removal of solids by direct flocculation with poly-electrolytes. Environ Int 31(2):297–304

    CAS  Article  Google Scholar 

  • Sayadi S, Ellouz R (1995) Roles of lignin peroxidase and manganese peroxidase from Phanerochaete chrysosporium in the decolorization of olive mill wastewaters. Appl Environ Microb 61(3):1098–1103

    CAS  Google Scholar 

  • Senent FR, Gutíerrez GR, Munoz AL, Bolanos JF (2012) New phenolic compounds hydrothermally extracted from the olive oil byproduct alperujo and their antioxidative activities. J Agric Food Chem 60(5):1175–1186

    Article  Google Scholar 

  • Sinigaglia M, Di Benedetto N, Bevilacqua A, Rosari Corbo M, Capece A, Romano P (2010) Yeasts isolated from olive mill wastewaters from southern Italy: technological characterization and potential use for phenol removal. Appl Microbiol Biotechnol 87(6):2345–2354

    CAS  Article  Google Scholar 

  • 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(8):2280–2284

    CAS  Article  Google Scholar 

  • Tsagaraki EV, Lazarides HN (2012) Fouling analysis and performance of tubular ultrafiltration on pretreated olive mill waste water. Food Bioproc Technol 5(2):584–592

    CAS  Article  Google Scholar 

  • Tsioulpas A, Dimou D, Iconomou D, Aggelis G (2002) Phenolic removal in olive oil mill wastewater by strains of Pleurotus spp. in respect to their phenol oxidase (laccase) activity. Bioresour Technol 84(3):251–257

    CAS  Article  Google Scholar 

  • Turano E, Curcio S, De Paola MG, Calabrò V, Iorio G (2002) An integrated centrifugation ultrafiltration system in the treatment of olive mill wastewater. J Membr Sci 209(2):519–531

    CAS  Article  Google Scholar 

  • Vassilev N, Fenice M, Federici F, Azcon R (1997) Olive mill waste water treatment by immobilized cells of Aspergillus niger and its enrichment with soluble phosphate. Process Biochem 32(7):617–620

    CAS  Article  Google Scholar 

  • Yagüe S, Terrón MC, González T, Zapico E, Bocchini P, Galletti GC, González AE (2000) Biotreatment of tannin-rich beer-factory wastewater with white-rot basidiomycete Coriolopsis gallica monitored by pyrolysis/gas chromatography/mass spectrometry. Rapid Commun Mass Spectrom 14(10):905–910

    Article  Google Scholar 

  • Yaropolov AI, Skorobogatko OV, Vartanov SS, Varfolomeyev SD (1994) Laccase: properties, catalytic mechanism, and applicability. Appl Biochem Biotechnol 49(3):257–280

    CAS  Article  Google Scholar 

  • Yesilada O, Sik S, Sam M (1998) Biodegradation of olive oil mill waste-waters by Coriolus versicolor and Funalia trogii. World J Microbiol Biotechnol 14(1):37–42

    CAS  Article  Google Scholar 

  • Zucconi FA, Pera MF, de Bertoldi M (1981) Evaluating toxicity of immature compost. Biocycle 22:54–57

    Google Scholar 

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Correspondence to Tahar Mechichi.

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Daâssi, D., Belbahri, L., Vallat, A. et al. Enhanced reduction of phenol content and toxicity in olive mill wastewaters by a newly isolated strain of Coriolopsis gallica . Environ Sci Pollut Res 21, 1746–1758 (2014). https://doi.org/10.1007/s11356-013-2019-9

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  • DOI: https://doi.org/10.1007/s11356-013-2019-9

Keywords

  • Laccase
  • Coriolopsis gallica
  • Oil mill wastewater
  • Phenolic compounds