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Biosynthesis of single-cell biomass from olive mill wastewater by newly isolated yeasts

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Abstract

The aim of this study was to assess the potential of newly isolated yeast strains Schwanniomyces etchellsii M2 and Candida pararugosa BM24 to produce yeast biomass on olive mill wastewater (OMW). Maximum biomass yield was obtained at 75 % (v/v) OMW, after 96 h of incubation at 30 °C and 5 % (v/v) inoculum size. The optimal carbon/nitrogen (C/N) ratio was in the range of 8:1 to10:1, and ammonium chloride was selected as the most suitable nitrogen source. Under these conditions, a maximum biomass production of 15.11 and 21.68 g L−1 was achieved for Schwanniomyces etchellsii M2 and Candida pararugosa BM24, respectively. Proteins were the major constituents of yeast cells (35.9–39.4 % dry weight), lipids were 2.8–5 % dry weight, and ash ranged from 4.8 to 9.5 % dry weight. Besides biomass production, yeast strains were also able to reduce toxicity and polluting parameter levels of the spent OMW-based medium. The practical results presented show that pH rose from initial value of 5.5 to 7.24–7.45 after fermentation. Approximately 23.1–41.4 % of the chemical oxygen demand (COD) and 15.4–19.2 % of the phenolic compounds were removed. The removal of phenolic compounds was associated with their biodegradation and their partial adsorption on yeast cells.

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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 Phanerochaete chrysosporium. Process Biochem 41:1148–1154

    Article  CAS  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 Biodeter Biodegr 68:45–50

    Article  CAS  Google Scholar 

  • American Public Health Association (1992) Standard methods for the examination of water and waste water, 18th edn. American Public Health Association, Washington

    Google Scholar 

  • APHA, AWWA, WPCF (1989) Standard methods for the examination of water and wastewater, 17th edn. APHA, AWWA, WPCF, Washington

    Google Scholar 

  • Arnold JL, Knapp JS, Johnson CL (2000) The use of yeasts to reduce polluting potential of silage effluent. Water Res 34:3699–3708

    Article  CAS  Google Scholar 

  • Aziz NH, Farag SE, Mousa LAA, Abo-Zaid MA (1998) Comparative antibacterial and antifungal effects of some phenolic compounds. Microbios 374:43–54

    Google Scholar 

  • Bamforth CW (2005) Food, fermentation and microorganisms. Blackwell Science, Oxford

    Book  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 41:74–78

    Article  CAS  Google Scholar 

  • Boskou D (2006) Sources of natural phenolic antioxidants. Trends Food Sci Technol 17:505–512

    Article  Google Scholar 

  • Botes A, Todorov S, von Mollendorff JW, Botha A, Dicks LMT (2007) Identification of lactic acid bacteria and yeast from boza. Process Biochem 42:267–270

    Article  CAS  Google Scholar 

  • Brown MR, Barrett SM, Volkma JK, Nearhos SP, Nell JA, Allan GL (1996) Biochemical composition of new yeasts and bacteria as food for bivalve aquaculture. Aquaculture 143:341–360

    Article  CAS  Google Scholar 

  • Choi MH, Park YH (2002) Production of yeast biomass using waste Chinese cabbage. Biomass Bioenergy 25:221–226

    Article  Google Scholar 

  • Choi MH, Ji GE, Koh KH, Ryu YW, Jo DH, Park HY (2002) Use of waste Chinese cabbage as a substrate for yeast biomass production. Bioresour Technol 83:251–253

    Article  CAS  Google Scholar 

  • Chtourou M, Ammar E, Nasri M, Medhioub K (2004) Isolation of a yeast, Trichosporon cutaneum, able to use low molecular weight phenolic compounds: application to olive mill waste water treatment. J Chem Technol Biotechnol 79:869–878

    Article  CAS  Google Scholar 

  • El Hajjouji H, Bailly JR, Winterton P, Merlina G, Revel JC, Hafidi M (2008) Chemical and spectrophotometric analysis of olive mill wastewater during a biological treatment. Bioresour Technol 99:4958–4965

    Article  Google Scholar 

  • Ercoli E, Ertola R (1983) SCP production from olive black water. Biotechnol Lett 7:457–462

    Article  Google Scholar 

  • Felipe MGA, Vitolo M, Mancilha IM, Silva SS (1997) Fermentation of sugar cane bagasse hemicellulosic hydrolysate for xylitol production: effect of pH. Biomass Bioenergy 13:11–14

    Article  CAS  Google Scholar 

  • Folch J, Lees M, Sloane-Stanley G (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 199:833–841

    Google Scholar 

  • Gharsallah N (1993) Production of single cell protein from olive mill wastewater by yeasts. Environ Technol 14:391–395

    Article  CAS  Google Scholar 

  • Giammanco GM, Melilli D, Piuseppe G (2004) Candida pararugosa isolation from the oral cavity of an Italian denture wearer. Res Microbiol 155:571–574

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gutiérrez A, Chiva R, Sancho M, Beltran G, Arroyo-López FN, Guillamon JM (2012) Nitrogen requirements of commercial wine yeast strains during fermentation of a synthetic grape must. Food Microbiol 31:25–32

    Article  Google Scholar 

  • Hachicha S, Chtourou M, Medhioub K, Ammar E (2006) Compost of poultry manure and olive mill wastes as an alternative fertilizer. Agron Sustain Dev 26:135–142

    Article  Google Scholar 

  • Hainal AR, Ignat I, Volf I, Popa VI (2011) Transformation of polyphenols from biomass by some yeast species. Cellul Chem Technol 45:211–219

    CAS  Google Scholar 

  • Halasz A, Lasztity R (1990) Use of yeast biomass in food production. CRC Press, USA

    Google Scholar 

  • Han IK, Hochstetler HW, Scott ML (1976) Metabolizable energy values of some poultry feeds determined by various methods and their estimation using metabolizability of the dry matter. Poult Sci 55:1335–1342

  • Harder W, Brooke AC (1990) Methylotrophic yeasts. In: Verachtert H, De Mot R (eds) Yeast biotechnology and biocatalysis. Marcel Dekker, New York, pp 395–428

    Google Scholar 

  • Jarboui R, Baati H, Fetoui F, Gargouri A, Gharsallah N, Ammar E (2011) Yeast performance in wastewater treatment: case study of Rhodotorula mucilaginosa. Environ Technol 33:951–960

    Article  Google Scholar 

  • Jensen SL, Umiker NL, Arneborg N, Edwards CG (2009) Identification and characterization of Dekkera bruxellensis, Candida pararugosa, and Pichia guilliermondii isolated from commercial red wines. Food Microbiol 26:915–921

    Article  CAS  Google Scholar 

  • Juszczyk P, Tomaszewska L, Kita A, Rymowicz W (2013) Biomass production by novel strains of Yarrowia lipolytica using raw glycerol, derived from biodiesel production. Bioresour Technol 137:124–131

    Article  CAS  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 74:339–348

    Article  CAS  Google Scholar 

  • Koutsoumanis K, Tassou CC, Taoukis PS, Nychas GJ (1998) Modelling the effectiveness of a natural antimicrobial on Salmonella enteritidis as a function of concentration, temperature and pH, using conductance measurements. J Appl Microbiol 84:981–987

    Article  CAS  Google Scholar 

  • Kurtzman CP, Fell JW, Boekhout T (2011) The yeasts: a taxonomic study. Elsevier Science BV, Amsterdam

    Google Scholar 

  • Lanciotti R, Gianotti A, Baldi D, Angrisani R, Suzzi G, Mastrocola D, Guerzoni ME (2005) Use of Yarrowia lipolytica strains for the treatment of olive mill wastewater. Bioresour Technol 96:317–322

    Article  CAS  Google Scholar 

  • Lee K, Lee S (1996) Continuous process for yeast biomass production from sugar beet stillage by a novel strain of Candida rugosa and protein profile of the yeast. J Chem Technol Biotechnol 66:349–354

    Article  CAS  Google Scholar 

  • Lee C, Yamakwa T, Komada T (1993) Rapid growth of thermotolerant yeast on palm oil. World J Microbiol Biotechnol 9:187–190

    Article  CAS  Google Scholar 

  • Lopes M, Araújo C, Aguedo M, Gomes N, Gonçalves C, Teixeira JA, Belo I (2009) The use of olive mill wastewater by wild type Yarrowia lipolytica strains: medium supplementation and surfactant presence effect. J Chem Technol Biotechnol 84:533–537

    Article  CAS  Google Scholar 

  • Martinez-Garcia G, Johnson AC, Bachmann RT , Williams CJ, Burgoyne A, Edyvean RGJ (2007) Two-stage biological treatment of olive mill wastewater with whey as co-substrate. Inter Biodeter Biodeg 59:273–282

  • Matsheka MI, Mpuchane S, Gashe BA, Allotey J, Khonga EB, Coetzee SB, Murindamombe G (2014) Microbial quality assessment and predominant microorganism of biltong produced in butcheries in Gaborone, Botswana. Food Nutr Sci 5:1668–1678

    Article  CAS  Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugars. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  • Miller BM, Litsky W (1976) Single cell protein in microbiology. McGrow-Hill Book Co, New York

    Google Scholar 

  • Moyo M, Mutare E, Chigondo F, Nyamunda BC (2012) Removal of phenol from aqueous solution by adsorption on yeast, Saccharomyces cerevisiae. IJRRAS 11:486–494

    Google Scholar 

  • Nakagawa Y, Robert V, Kawarazakai J, Epping W, Smith MT, Poot GA, Mizuguchi I, Kanbe T, Doi M (2004) Recurrent isolation of an uncommon yeast, Candida pararugosa, from a sarcoma patient. Med Mycol 42:267–271

    Article  CAS  Google Scholar 

  • Nasseri AT, Rasoul-Amini S, Morowvat MH, Ghasemi Y (2011) Single cell protein: production and process. Am J Food Technol 6:103–116

    Article  CAS  Google Scholar 

  • Nigam JN (1998) Single cell protein from pineapple cannery effluent. World J Microbiol Biotechnol 14:693–696

    Article  CAS  Google Scholar 

  • Papanikolaou S, Galiotou-Panayotou M, Fakas S, Komaitis M, Aggelis G (2008) Citric acid production by Yarrowia lipolytica cultivated on olive-mill wastewater-based media. Bioresour Technol 99:2419–2428

    Article  CAS  Google Scholar 

  • Pennacchia C, Blaiotta G, Pepe O, Villani F (2008) Isolation of Saccharomyces cerevisiae strains from different food matrices and their preliminary selection for a potential use as probiotics. J Appl Microbiol 105:1919–1928

    Article  CAS  Google Scholar 

  • Petkov K, Rymowicz W, Musiał I, Kinal S, Biel W (2002) Nutritive value of protein Yarrowia lipolytica, yeast obtained on various lipid substrates. Folia Univ Agri Stetin, Zootechnica 227:95–100

    CAS  Google Scholar 

  • Reade AE, Gregory KF (1975) High temperature production of protein enriched feed from cassava by fungi. Appl Microbiol 30:897–903

    CAS  Google Scholar 

  • Reiser V, Gasperik J (1995) Purification and characterization of the cell-wall associated and extracellular α-glucosidases from Saccharomycopsis fibuligera. Biochem J 308:753–760

    Article  CAS  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 Microbiol 61:1098–1103

    CAS  Google Scholar 

  • Schaffer S, Podstawa M, Visioli F, Bogani P, Muller WE, Eckert GP (2007) Hydroxytyrosol-rich olive mill wastewater extract protects brain cells in vitro and ex vivo. J Agric Food Chem 55:5043–5049

    Article  CAS  Google Scholar 

  • Scioli C, Vollaro L (1997) The use of Yarrowia lipolytica to reduce pollution in olive mill wastewaters. Water Res 31:2520–2524

    Article  CAS  Google Scholar 

  • Spanamberg A, Hartfelder C, Fuentefria AM, Valente P (2004) Diversity and enzyme production by yeasts isolated from raw milk in Southern Brazil. Acta Sci Vet 32:195–199

    Google Scholar 

  • Tassou CC, Nychas GJE (1995) Inhibition of Salmonella enteritidis by oleuropein in broth and in a model food system. Lett Appl Microbiol 20:120–124

    Article  CAS  Google Scholar 

  • Torija MJ, Rozès N, Poblet M, Guillamón JM, Mas A (2003) Effects of fermentation temperature on the strain population of Saccharomyces cerevisiae. Int J Food Microbiol 80:47–53

    Article  CAS  Google Scholar 

  • Vagelas I, Kalorizou H, Papachatzis A, Botu M (2009) Bioactivity of olive oil mill wasterwater against plant pathogens and post harvest diseases. Biotechnol Biotechnol Equip 23:1217–1219

    Article  Google Scholar 

  • Vega MP, Da Silva Leite R, de Oliveira MA CL (2007) Mathematical modeling of single cell protein and ethanol production by Kluyveromyces cicerisporus fermentation on whey. In: Plesu V, Agachi PS (eds) 17th European symposium on computer aided process engineering-ESCAPE 17

    Google Scholar 

  • Wallecha A, Mishra S (2003) Purification and characterization of two β-glucosidases from a thermo-tolerant yeast Pichia etchellsii. Biochim Biophys Acta 1649:74–84

    Article  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfland DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Wolfe K, Wu X, Lu RH (2003) Antioxidant activity of apple peel. J Agric Food Chem 51:609–614

    Article  CAS  Google Scholar 

  • Wu L, Ge G, Wan J (2009) Biodegradation of oil wastewater by free and immobilized Yarrowia lipolytica W29. J Environ Sci 21:237–242

    Article  CAS  Google Scholar 

  • Zheng S, Yang M, Yang Z (2005a) Biomass production of isolate from salad oil manufacturing wastewater. Bioresour Technol 96:1183–1187

    Article  CAS  Google Scholar 

  • Zheng S, Yang M, Yang Z, Yang Q (2005b) Biomass production from glutamate fermentation wastewater by the co-culture of Candida halophila and Rhodotorula glutinis. Bioresour Technol 96:1522–1524

    Article  CAS  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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Acknowledgments

The authors would like to thank Mr. Abdel Majid Dammak for revising the language of the manuscript.

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Authors and Affiliations

  1. Laboratory of Enzyme Engineering and Microbiology, National School of Engineers of Sfax, University of Sfax, BP 1173, 3038, Sfax, Tunisia

    Fatma Arous, Hela Zouari-Mechichi, Moncef Nasri & Tahar Mechichi

  2. Laboratory of Valorization, Security and Food Analysis, National School of Engineers of Sfax, University of Sfax, Sfax, Tunisia

    Samia Azabou

  3. Laboratoire Microorganismes et Biomolécules Actives, Faculté des Sciences de Tunis, Université Tunis El Manar, Campus Universitaire, 2092, Tunis, Tunisia

    Atef Jaouani

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  1. Fatma Arous
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  2. Samia Azabou
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  3. Atef Jaouani
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  4. Hela Zouari-Mechichi
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  5. Moncef Nasri
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Correspondence to Tahar Mechichi.

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Arous, F., Azabou, S., Jaouani, A. et al. Biosynthesis of single-cell biomass from olive mill wastewater by newly isolated yeasts. Environ Sci Pollut Res 23, 6783–6792 (2016). https://doi.org/10.1007/s11356-015-5924-2

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