Filamentous fungi isolated from Tunisian olive mill wastes: use of solid-state fermentation for enzyme production

  • Hanen ZAIER Laboratory of Integrated Olive Production, Olive Tree Institute, Hedi Karray Street, P.O. Box 208, 2080, Ariana (TN)
  • Sameh MAKTOUF Laboratory of Sustainability of Olive Growing in Semi-Arid and Arid Regions: Improvement of Olive Productivity and Product Quality, Olive Tree Institute, Sfax (TN)
  • Sevastianos ROUSSOS Aix Marseille University, Avignon University, CNRS, IRD, IMBE, Marseille (FR)
  • Ali RHOUMA Laboratory of Integrated Olive Production, Olive Tree Institute, Hedi Karray Street, P.O. Box 208, 2080, Ariana (TN)
Keywords: biotechnological applications; enzymes; fungi; olive oil wastes; solid-state fermentation (SSF); valorization

Abstract

Olive mill wastewaters and olive cake are effluents generated during olive oil production process. They represent a major disposal and potentially severe pollution problem for the industry, also promising source of substances of high value. The aim of this study is the valorization of olive mill wastes (OMWW, olive cake, olive twigs and leaves) to produce enzymes with high industrial and biotechnological potential, by the solid-state fermentation technique (SSF), from isolated fungi present in olive mill wastewater and olive cake. A total of 47 strains were isolated and purified from these two residues. The metabolic potential of isolated strains was study by testing the hydrolytic enzymes activities of lipase, protease, amylase, cellulase, invertase, phytase and tannase on agar plate media containing different substrate. The monitoring of SSF has shown that the metabolic activity of these strains is extremely rapid using this technique. Our fungi collection contains a diversity of strains capable to producing a variety of enzymes of biotechnological interest.

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References

Adrio JL, Demain AL (2014). Microbial enzymes: tools for biotechnological processes. Biomolecules 4:117-139. https://doi.org/10.3390/biom4010117

Ainsworth GC, Sparrow FK, Sussman AS (1973). The fungi. Academic Press, New York, pp 504-621.

Aissam H, Penninckx M, Benlemlih M (2007). Reduction of phenolics content and COD in olive oil mill wastewaters by indigenous yeasts and fungi. World Journal of Microbiology and Biotechnology 23:1203-1208. https://doi.org/10.1007/s11274-007-9348-0

Altieri R, Esposito A (2008). Olive orchard amended with two experimental olive mill wastes mixtures: Effects on soil organic carbon, plant growth and yield. Bioresource Technology 99:8390-8393. https://doi.org/10.1016/j.biortech.2008.02.048

Arvanitoyannis IS, Kassaveti A, Stefanatos S (2007). Olive oil waste treatment: a comparative and critical presentation of methods, advantages and disadvantages. Critical Reviews in Food Science and Nutrition 47:187-229. https://doi.org/10.1080/10408390600695300

Attili DS, de Hoog Sybren AA, Kleiner P (1998). RDNA-RFLP and ITS I sequencing of species of the genus Fonsecaea, agents of chromoblastomycosis. Medical Mycology 36:219-225. https://doi.org/10.1080/02681219880000331

Baffi MA, Romo-Sanchez S, Ubeda-Iranzo J (2012). Fungi isolated from olive ecosystems and screening of their potential biotechnological use. New Biotechnology 29:451-456. https://doi.org/10.1016/j.nbt.2011.05.004

Barnett HL, Hunter BB (1972). Illustrated genera of imperfect fungi. 3rd edition, Burgess Publishing Co pp 273.

Benyahia N, Zein K (2003). Analyse des problèmes de l’industrie de l’huile d’olive et solutions récemment développées. [A special look at the waste problems of the olive oil industry and the latest viable solutions]. Contribution spéciale de Sustainable Business Associates (Suisse) à SESEC II pp 2-7.

Berne C, Carboué Q, Fabresse C (2013). Etat physiologique et virulence du champignon filamenteux Trichoderma harzianum. Master. Faculté des sciences. Et techniques Saint Jerome. Aix-Marseille Université pp 20.

Botton B, Breton A, Févre, M, Gauthier S (1990). Les Moisissures Utiles et Nuisibles: Importance Industrielle., 2ndEd. Masson pp 426.

Brahmbhatt D, Modi HA (2015). Comparative Studies on methods of tannase assay. International Journal for Research in Applied Science and Engineering Technology (IJRASET) 3:715-720.

Calvo AM, Wilson RA, Bok JW, Keller NP (2002). Relationship between secondary metabolism and fungal development. Microbiology and Molecular Biology Reviews 66:447-459. https://doi.org/10.1128/MMBR.66.3.447-459.2002

Castilho LR, Polato CMS, Baruque EA, Sant’anna GL, Freire DMG (2000). Economic analysis of lipase production by Penicillium restrictum in solid-state and submerged fermentations. Biochemical Engineering Journal 4:239-247.

Cegarra J, Alburquerque JA, Gonzálvez J, Tortosa G, Chaw D (2006). Effects of the forced ventilation on composting of a solid olive-mill by-product (‘‘alperujo’’) managed by mechanical turning. Waste Management 26:1377-1383.

Christen P, Angeles N, Farres A, Revah S (1998). Comparison of production of lipase from Rhizopus delemar by submerged and solid-state fermentation. J. Orstom pp 321-334.

D'Annibale A, Sermanni GG, Federici F, Petruccioli M (2006). Olive-mill wastewaters: a promising substrate for microbial lipase production. Bioresource Technology 97:1828-1833.

de Vries RP, Visser J (2001). Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiology and Molecular Biology Reviews 65:497-522. https://doi.org/10.1128/MMBR.65.4.497-522.2001

Engelen AJ, Heeft FC, Randsdorp PHG, Somers WAC, Schaefer J, van der Vat BJ (2001). Determination of phytase activity in feed by a colorimetric enzymatic method: collaborative interlaboratory study. Journal of AOAC International 84:629-633.

Falony G, Armas JC, Julio C, Mendoza D, Jose L, Hermandez M (2006). Production of extracellular lipase from Aspergillus niger by solid-state fermentation. Food Technology and Biotechnology 44:235-240.

Fernández-Bolaños J, Guillermo R, Rocío R, Guillén R, Jiménez A (2006). Extraction of interesting organic compounds from olive oil waste. Grasas Y Aceites 57:95-106. https://doi.org/10.3989/gya.2006.v57.i1.25

Gargova S, Sariyska M (2003). Effect of culture conditions on the biosynthesis of Aspergillus niger phytase and acid phosphatase. Enzyme and Microbial Technology 32:231-235. https://doi.org/10.1016/S0141-0229(02)00247-8

Geoffry K, Achur RN (2018). Screening and production of lipase from fungal organisms. Biocatalysis and Agricultural Biotechnology 14: 241-253. https://doi.org/10.1016/J.BCAB.2018.03.009

Ghose TK (1987). Measurement of cellulase activities. Pure and Applied Chemistry 59:257-268. https://doi.org/10.1351/pac198759020257

Gombert AK, Pinto AL, Castilho LR, Freire DMG (1999). Lipase production by Penicillium restrictum in solid-state fermentation using babassu oil cake as substrate. Process Biochemistry 35:85-89. https://doi.org/10.1385/abab:84-86:1-9:1137

Hafidi M, Amir S, Revel JC (2005). Structural characterization of olive mill waste-water after aerobic digestion using elemental analysis, FTIR and 13C NMR. Process Biochemistry 40:2615-2622. https://doi.org/10.1016/j.procbio.2004.06.062

Hankin L, Anagnostakis SL (1975). The Use of solid media for detection of enzyme production by fungi. Mycologia 67:597-607. https://doi.org/10.2307/3758395

Hassi M, Haggoud A, EL Mzibri M, Ibnsouda S, Houari A, Iraqui M (2007). Isolation and identification of a staphylococcal strain with an anti-mycobacterial activity and study of its mode of action. Annals of Microbiology 57:651-656. https://doi.org/10.1007/BF03175368

Hassouni H, Ismaili-Alaoui M, Perraud-Gaime I, Augur C, Roussos S (2006a). Effect of culture media and fermentation parameters on phytase production by the thermophilic fungus Myceliophthora thermophila in solid state fermentation. Micologia Aplicada International 18:29-36.

Hassouni H, Ismaili-Alaoui M, Lamrani K, Perraud-Gaime I, Augur C, Roussos S (2006 b). Spore germination of filamentous fungi in solid state fermentation under different culture conditions. Micologia Aplicada International 19:1-9.

Jahangeer S, Khan N, Sohali M, Shahzad S, Ahmad A, Khan S (2005). Screening and characterization of fungal cellulases isolated from the native environmental source. Pakistan Journal of Botany 37:739-748.

Kamini NR, Mala JGS, Puvanakrishnan D (1998). Lipase production from Aspergillus niger by solid-state fermentation using gingelly oil cake. Process Biochemistry 33:505-511. https://doi.org/10.1016/S0032-9592(98)00005-3

Kar B, Banerjee R, Bhattacharya BC (1999). Microbial production of gallic acid by modified solid-state fermentation. The Journal of Industrial Microbiology and Biotechnology 23:173-177. https://doi.org/10.1038/sj.jim.2900713

Kim DS, Godber JS, Kim SW (1999). Culture conditions for a new phytase producing fungus. Biotechnology Letters 21:1077-1081. https://doi.org/10.1023/A:1005696829168

Kumar A, Shamsher SK (2012). Lipase production in solid-state fermentation (SSF): recent developments and biotechnological applications. Dynamic Biochemistry, Process Biotechnology and Molecular Biology 6:13-27.

Kumar DS, Ray S (2014). Fungal lipase production by solid state fermentation-an overview. Journal of Analytical and Bioanalytical Techniques 6:1-10.

Lamrani K (2009). Etude de la biodiversité des moisissures nuisibles et utiles isolées à partir des Maâsra du Maroc. Thèse de doctorat d’état, pp 154-155.

Lamrani K, Ismaili-Alaoui M, Cheheb M, Kammas N, Iraqi-Houssaini L, Hassouni H, … Roussos S (2006). Distribution écologique des champignons filamenteux thermophiles isolés à partir des principales Maâsra du Maroc. In: Biotechnologies et qualité des produits de l’olivier dans le bassin méditerranéen. Actes Editions, Rabat, pp 293- 306.

Leite P, Salgado JM, Venȃncio A (2016). Ultrasounds pretreatment of olive pomace to improve xylanase and cellulase production by solid-state fermentation. Bioresource Technology 214:737-746. https://doi.org/10.1016/j.biortech.2016.05.028

Lekha PK, Lonsane BK (1997). Production and application of tanin acyl hydrolase: State of the art. Advances in Applied Microbiology 44:215-260. https://doi.org/10.1016/s0065-2164(08)70463-5

Liu BL, Rafiq A, Tzeng YM, Rob A (1998). The induction and characterization of phytase and beyond. Enzyme and Microbial Technology 22:415-424. https://doi.org/10.1016/S0141-0229(97)00210-X

Lobedanz S, Damhus T, Borchert TV, Hansen TT, Lund H, Lai W, … Kirk O (2016). Enzymes in industrial biotechnology. Kirk-Othmer Encyclopedia of Chemical Technology 1-73. https://doi.org/10.1002/0471238961.0914042114090512.a01.pub3

Madhav K, Verma S, Tanta R (2011). Isolation of amylase producing Bacillus species, from soil sample of different regions in Dehradun and to check the effect of pH and temperature on their amylase activity. Journal of Pharmaceutical and Biomedical Sciences 12:1-8.

Mahadik ND, Puntambekar US, Bastawde KB, khire JM, Gokhale DV (2002). Production of acidic lipase by Aspergillus niger in solid state fermentation. Process Biochemistry 38:715-721.

Maheshwari R, Bharadwaj G, Bhat MK (2000). Thermophilic fungi: their physiology and enzymes. Microbiology and Molecular Biology Reviews 64:461-88. https://doi.org/10.1128/mmbr.64.3.461-488.2000

Millán B, Lucas R, Robles A, García T, Álvarez de Cienfuegos G, Gálvez A (2000). A study on the microbiotica from olive-mill wastewater (OMW) disposal lagoons, with emphasis on filamentous fungi and their biodegradative potential. Microbiological Research 155:143-147. https://doi.org/10.1016/s0944-5013(00)80027-0

Miller GL (1959). Use of dinitrosalicylic acid reagent for determination of reducing sugar. Analytical Chemistry 31:426-428. https://doi.org/10.1021/ac60147a030

Mirzaakhmedov SY, Ziyavitdinov ZF, Akhmedova ZR, Saliev AB, Ruzmetova DT, Ashurov K, … Lametti S (2007). Isolation, purification, and enzymatic activity of cellulase components of the fungus Aspergillus terreus. Chemistry of Natural Compounds 43:594-597.

Mitchell DB, Vogel K, Weimann BJ, Pasamontes L, van Loon AP (1997). The phytase subfamily of histidine acid phosphatases: isolation of genes for two novel phytases from the fungi Aspergillus terreus and Myceliophtora thermophila. Microbiology 143:245-252. https://doi.org/10.1099/00221287-143-1-245

Morillo JA, Antizar-Ladislao B, Monteoliva-Sánchez M, Ramos-Cormenzana A, Russell NJ (2009). Bioremediation and biovalorisation of olive-mill wastes. Applied Microbiology and Biotechnology 82:25-39. https://doi.org/10.1007/s00253-008-1801-y

Nampoothiri K, Madhavan T, Jino G, Krishnan R, Szakacs G, Nagy V, … Pandey A (2004). Thermostable phytase production by Thermoascus aurantiacus in submerged fermentation. Applied Biochemistry and Biotechnology 118:205-214. https://doi.org/10.1385/ABAB:118:1-3:205

Nefzaoui A (1995). Feeding value of Mediterranean ruminant feed resources. Advanced course Syria, March pp 12-23.

Niaounakis M, Halvadakis CP (2006). Physical processes. In: Olive Processing Waste Management: Literature Review and Patent Survey (2nd Edn), Elsevier, Amsterdam, the Netherlands pp 107-113.

Nigam PN (2013). Microbial Enzymes with special characteristics for biotechnological applications. Biomolecules 3:597-611. https://doi.org/10.3390/biom3030597

Office National de l’Huile (ONH) (2016). http://www.onh.com.tn/index.php/fr/2016-05-23-14-44-46/la-production.

Office National de l’Huile (ONH) (2018). http://www.onh.com.tn/index.php/fr/commercialisation/positionnement-sur-le-marche-mondial.

Ozturkoglu-Budak S, Wiebenga A, Bron PA, de Vries RP (2016). Protease and lipase activities of fungal and bacterial strains derived from an artisanal raw ewe’s milk cheese. International Journal of Food Microbiology 237:17-27. https://doi.org/10.1016/j.ijfoodmicro.2016.08.007

Gianni P, Keskos D, Macris BJ, Christakopoulos P (2003). Production of cellulolytic and xylanolytic enzymes by Fusarium oxysporum on corn stover in solid state fermentation. Industrial Crops and Products 18:37-45. https://doi.org/10.1016/S0926-6690(03)00018-9

Penttila M, Lehtovaara P, Nevalainen H, Bhikhabhai R, Knowles J (1986). Homology between cellulase genes of Trichoderma reesei: complete nucleotide sequence of the endoglucanase I gene. Gene 45:253-263. https://doi.org/10.1016/0378-1119(86)90023-5

Raimbault M (1980). Fermentation en milieu solide. Croissance de champignons filamenteux sur substrat amylacé. Thèse d’Etat. Université Paul Sabatier, Toulouse, France pp 291.

Ramachandran S, Roopesh K, Nampoothiri KM, Szakas G, Pandey A (2005). Mixed substrate fermentation for the production of phytase by Rhizopus spp. Using oilcakes as substrates. Process Biochemystry 40:1749-1754. https://doi.org/10.1016/j.procbio.2004.06.040

Ramond JB, Welz PJ, Tuffin MI, Burton SG, Cowan DA (2013). Assessment of temporal and spatial evolution of bacterial communities in a biological sand filter mesocosm treating winery wastewater. Journal of Applied Microbiology 115:91-101. https://doi.org/10.1111/jam.12203

Raper KB, Fennel DI (1977). The Genus Aspergillus. Krieger Publishing company. New York pp 686.

Robinson PK (2015). Enzymes: principles and biotechnological applications. Essays Biochemistry 59:1-41. https://doi.org/10.1042/bse0590001

Rodrìguez Couto S, Sanromán M (2006). Application of solid-state fermentation to food industry. Journal of Food Engineering 76:291–302. https://doi.org/10.1016/j.jfoodeng.2005.05.022

Romo-Sánchez S, Alves-Baffi M, Arévalo-Villena M, Úbeda-Iranzo J, Briones-Pérez A (2010). Yeast biodiversity from oleic ecosystems: study of their biotechnological properties. Food Microbiology 27:487-492. https://doi.org/10.1016/j.fm.2009.12.009

Roopesh K, Ramachandran S, Nampoothiri KM, Szakacs G, Pandey A (2006). Comparison of phytase production on wheat bran and oil cakes in solid-state fermentation by Mucor racemosus. Bioresource Technology 97:506-511. https://doi.org/10.1016/j.biortech.2005.02.046

Roussos S (1985). Croissance de Trichoderma harzianum par fermentation en milieu solide: Physiologie, sporulation et production de cellulase. Thèse d’Etat, Université de Provence, Marseille, pp 193.

Roussos S, Raimbault M (1982). Hydrolyse de la cellulose par les moisissures: Screening des souches cellulolytiques. Annales de Microbiologie 133:455-464.

Roussos S, Zaouia N, Salih G, Tantaoui-Elaraki A, Lamrani K, Cheheb M, … Ismaili-Alaoui M (2006). Characterization of filamentous fungi isolated from Moroccan olive and olive cake: Toxinogenic potential of Aspergillus strains. Molecular Nutrition and Food Research 50:500-506. https://doi.org/10.1002/mnfr.200600005

Sánchez S, Demain A (2017). Useful microbial enzymes-an introduction. In book: Biotechnology of Microbial Enzymes. https://doi.org/10.1016/B978-0-12-803725-6.00001-7

Santos MM, Rosa AS, Dal’boit S, Mitchell DA, Kriger N (2004). Thermal denaturation: is solid state fermentation really a good technology for the production of enzymes? Bioresource Technolgy 93:261-268. https://doi.org/10.1016/j.biortech.2003.11.007

Sato K, Sudo S (1999). Small-scale solid-state fermentation. In: Demain AL, Davies JE (Eds.). Manual of industrial microbiology and biotechnology. 2ed pp 61-79.

Saucedo-Castaneda G (1991). Contrôle du métabolisme de Schwanniomyces castellii cultivé sur support solide. Thèse de doctorat, Université de Montpellier II pp 212.

Sharma S, Bhat TK, Dawra RK (2000). A spectrophotometric method for assay of tannase using rhodanine. Analytical Biochemistry 279:85-89. https://doi.org/10.1006/abio.1999.4405

Singhania RR, Sukumaran RK, Patel AK, Larroche C, Pandey A (2010). Advancement and comparative profiles in the production technologies using solid-state and submerged fermentation for microbial cellulases. Enzyme and Microbial Technology 46:541-549. https://doi.org/10.1016/j.enzmictec.2010.03.010

Thomas L, Larroche C, Pandey A (2013). Current developments in solid-state fermentation. Biochemical Engineering Journal 81:146-161.

Tomme P, VanTilbeurgh H, Pettersson G, VanDamme J, Vandekerchhove J, Knowles J, … Claeyssens M (1988). Studies of the cellulolytic system of Trichoderma reesei QM 9414. Analysis of domain function in two cellobiohydrolases by limited proteolysis. European Journal of Biochemistry 170:575-581. https://doi.org/10.1111/j.1432-1033.1988.tb13736.x

Idrees S, Rajoka MI (2002). Production of lipases by Rhizopus oligosporous by solid-state fermentation. Process Biochemistry 37:637-641. https://doi.org/10.1016/S0032-9592(01)00252-7

Virupakshi S, Gireesh Babu K, Gaikwad SR, Naik GR (2005). Production of a xylanolytic enzyme by a thermoalkaliphilic Bacillus sp. JB-99 in solid state fermentation. Process Biochemistry 40:431-435. https://doi.org/10.1016/J.PROCBIO.2004.01.027

von Arx JA (1974). The genera of fungi sporulating in pure culture. 2nd Cramer: Vaduz pp 315.

White TJ, Bruns T, Lee S, Taylor J (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, (Eds). PCR Protocols: a guide to methods and applications. Academic Press, New York, pp 315-322.

Published
2021-01-04
How to Cite
ZAIER, H., MAKTOUF, S., ROUSSOS, S., & RHOUMA, A. (2021). Filamentous fungi isolated from Tunisian olive mill wastes: use of solid-state fermentation for enzyme production. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(1), 12125. https://doi.org/10.15835/nbha49112125
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Research Articles
CITATION
DOI: 10.15835/nbha49112125