Integrated biovalorization of wine and olive mill by-products to produce enzymes of industrial interest and soil amendments

  • Rocio Reina CSIC-EEZ, Dept. Soil Microbiology and Symbiotic Systems. Prof. Albareda 1, 18008 Granada
  • René Ullrich Dresden University of Technology, International Institute Zittau, Dept. Bio and Environmental Sciences. Markt 23, 02763 Zittau
  • Inmaculada García-Romera CSIC-EEZ, Dept. Soil Microbiology and Symbiotic Systems. Prof. Albareda 1, 18008 Granada http://orcid.org/0000-0001-6351-1885
  • Christiane Liers Dresden University of Technology, International Institute Zittau, Dept. Bio and Environmental Sciences. Markt 23, 02763 Zittau
  • Elisabet Aranda University of Granada, Water Research Institute, Dept. Microbiology. Edificio Fray Luis, Ramón y Cajal 4, 18004 Granada http://orcid.org/0000-0001-5915-2445

Abstract

An integral and affordable strategy for the simultaneous production of lignin-modifying and carbohydrate active enzymes and organic amendment, with the aid of a saprobe fungus was developed by using olive oil and wine extraction by-products. The polyporal fungus Trametes versicolor was cultivated in soy or barley media supplemented with dry olive mill residue (DOR) as well as with grape pomace and stalks (GPS) in solid state fermentation (SSF). This strategy led to a 4-fold increase in the activity of laccase, the principal enzyme produced by SFF, in DOR-soy media as compared to controls. T. versicolor managed to secrete lignin-modifying enzymes in GPS, although no stimulative effect was observed. GPS-barley media turned out to be the appropriate medium to elicit most of the carbohydrate active enzymes. The reuse of exhausted solid by-products as amendments after fermentation was also investigated. The water soluble compound polymerization profile of fermented residues was found to correlate with the effect of phytotoxic depletion. The incubation of DOR and GPS with T. versicolor not only reduced its phytotoxicity but also stimulated the plant growth. This study provides a basis for understanding the stimulation and repression of two groups of enzymes of industrial interest in the presence of different carbon and nitrogen sources from by-products, possible enzyme recovery and the final reuse as soil amendments.

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References

Alburquerque JA, Gonzálvez J, García D, Cegarra J, 2004. Agrochemical characterisation of "alperujo", a solid by-product of the two-phase centrifugation method for olive oil extraction. Bioresource Technol 91: 195-200. http://dx.doi.org/10.1016/S0960-8524(03)00177-9

Amore A, Giacobbe S, Faraco V, 2013. Regulation of cellulase and hemicellulase gene expression in fungi. Curr Genomics 14: 230-249. http://dx.doi.org/10.2174/1389202911314040002

Aranda E, Sampedro I, Ocampo JA, García-Romera I, 2006. Phenolic removal of olive-mill dry residues by laccase activity of white-rot fungi and its impact on tomato plant growth. Int Biodeter Biodegr 58: 176-179. http://dx.doi.org/10.1016/j.ibiod.2006.06.006

Buswell J, 1991. Fungal degradation of lignin. In: Handbook of Applied Mycology Vol. 1. Soil and Plants; Arora AK, Rai B, Mukerji G, Knudsen G (eds.), pp: 425-480. Marcel Dekker Inc, New York.

Carabajal M, Kellner H, Levin L, Jehmlich N, Hofrichter M, Ullrich R, 2013. The secretome of Trametes versicolor grown on tomato juice medium and purification of the secreted oxidoreductases including a versatile peroxidase. J Biotechnol 168: 15-23. http://dx.doi.org/10.1016/j.jbiotec.2013.08.007

Cordova M, Nemmaoui M, Isamili-Alaoui A, Morin S, Roussos M, Raimbault B, Benjilali B, 1998. Lipase production by solid state fermentation of olive cake and sugar cane bagasse. J Mol Catal B: Enzym 5: 75-78. http://dx.doi.org/10.1016/S1381-1177(98)00067-8

Coughlan MP, 1985. The properties of fungal and bacterial cellulases with comment on their production and application. Biotechnol Genet Eng 3: 39-110. http://dx.doi.org/10.1080/02648725.1985.10647809

Delabona PDS, Pirota RDPB, Codima CA, Tremacoldi CR, Rodrigues A, Farinas CS, 2012. Using amazon forest fungi and agricultural residues as a strategy to produce cellulolytic enzymes. Biomass Bioenerg 37: 243-250. http://dx.doi.org/10.1016/j.biombioe.2011.12.006

Dermeche S, Nadour M, Larroche, C, Moulti-mati F, Michaud P, 2013. Olive mill wastes: Biochemical characterizations and valorization strategies. Process Biochem 48: 1532-1552. http://dx.doi.org/10.1016/j.procbio.2013.07.010

Díaz R, Saparrat MCN, Jurado M, García-Romera I, Ocampo JA, Martínez MJ, 2010. Biochemical and molecular characterization of Coriolopsis rigida laccases involved in transformation of the solid waste from olive oil production. Appl Microbiol Biotechnol 88: 133-142. http://dx.doi.org/10.1007/s00253-010-2723-z

Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F, 1956. Colorimetric method for determination of sugars and related substances. Anal Chem 28: 350-356. http://dx.doi.org/10.1021/ac60111a017

Elisashvili V, Kachlishvili E, 2009. Physiological regulation of laccase and manganese peroxidase production by white-rot Basidiomycetes. J Biotechnol 144: 37-42. http://dx.doi.org/10.1016/j.jbiotec.2009.06.020

Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martínez AT, Otillar R, Spatafora JW, Yadav JS et al., 2012. The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336: 1715-1719. http://dx.doi.org/10.1126/science.1221748

Hamman OB, De La Rubia T, Martínez J, 1999. The effect of manganese on the production of Phanerochaete flavido-alba ligninolytic peroxidases in nitrogen limited cultures. FEMS Microbiol Lett 177: 137-142. http://dx.doi.org/10.1111/j.1574-6968.1999.tb13724.x

Jiménez A, Rodríguez R, Fernández-Caro I, Guillén R, Fernández-Bolaños J, Heredia A, 2000. Olive fruit cell wall: degradation of pectic polysaccharides during ripening. J Agric Food Chem 49: 409-415. http://dx.doi.org/10.1021/jf000235u

Kaal EEJ, Field JA, Joyce TW, 1995. Increasing ligninolytic enzyme activities in several white-rot Basidiomycetes by nitrogen-sufficient media. Bioresource Technol 53: 133-139. http://dx.doi.org/10.1016/0960-8524(95)00066-N

Kapich AN, Prior BA, Botha A, Galkin S, Lundell T, Hatakka A, 2004. Effect of lignocellulose-containing substrates on production of ligninolytic peroxidases in submerged cultures of Phanerochaete chrysosporium ME-446. Enzyme Microbiol Tech 34: 187-195. http://dx.doi.org/10.1016/j.enzmictec.2003.10.004

Kirk TK, Farrell RL, 1987. Enzymatic "combustion": the microbial degradation of lignin. Ann Rev Microbiol 41: 465-505. http://dx.doi.org/10.1146/annurev.mi.41.100187.002341

Kirsten WJ, Grunbaum BW, 1955. Dumas nitrogen determination on decimilligram scale. Anal Chem 27: 1806-1809. http://dx.doi.org/10.1021/ac60107a039

Lahjouji K, Storms R, Xiao Z, Joung K-B, Zheng Y, Powlowski J, Tsang A, Varin L, 2007. Biochemical and molecular characterization of a cellobiohydrolase from Trametes versicolor. Appl Microbiol Biotechnol 75: 337-346. http://dx.doi.org/10.1007/s00253-006-0824-5

Liers C, Arnstadt T, Ullrich R, Hofrichter M, 2011. Patterns of lignin degradation and oxidative enzyme secretion by different wood- and litter-colonizing basidiomycetes and ascomycetes grown on beech-wood. FEMS Microbiol Ecol 78: 91-102. http://dx.doi.org/10.1111/j.1574-6941.2011.01144.x

Mateo JJ, Maicas S, 2015. Valorization of winery and oil mill wastes by microbial technologies. Food Res Int 73: 13-25. http://dx.doi.org/10.1016/j.foodres.2015.03.007

McDougall GJ, Fry SC, 1989. Structure-activity relationships for xyloglucan oligosaccharides with antiauxin activity. Plant Physiol 89: 883-887. http://dx.doi.org/10.1104/pp.89.3.883

Moredo N, Lorenzo M, Domínguez A, Moldes D, Cameselle C, Sanroman A, 2003. Enhanced ligninolytic enzyme production and degrading capability of Phanerochaete chrysosporium and Trametes versicolor. World J Microb Biot 19: 665-669. http://dx.doi.org/10.1023/A:1025198917474

Papadopoulos A, 2012. Sorption of acetylated pine wood decayed by brown rot, white rot and soft rot: different fungi-different behaviours. Wood Sci Technol 46: 919-926. http://dx.doi.org/10.1007/s00226-011-0450-y

Pazarlioǧlu NK, Sariişik M, Telefoncu A, 2005. Laccase: production by Trametes versicolor and application to denim washing. Process Bioche 40: 1673-1678. http://dx.doi.org/10.1016/j.procbio.2004.06.052

Reina R, Liers C, Ocampo JA, García-Romera I, Aranda E, 2013. Solid state fermentation of olive mill residues by wood- and dung-dwelling Agaricomycetes: Effects on peroxidase production, biomass development and phenol phytotoxicity. Chemosphere 93: 1406-1412. http://dx.doi.org/10.1016/j.chemosphere.2013.07.006

Reina R, Kellner H, Jehmlich N, Ullrich R, García-Romera I, Aranda E, Liers C, 2014. Differences in the secretion pattern of oxidoreductases from Bjerkandera adusta induced by a phenolic olive mill extract. Fungal Genet Biol 72: 99-105. http://dx.doi.org/10.1016/j.fgb.2014.07.009

Rejón-Palomares A, García-Garrido J, Ocampo JA, García-Romera I, 1996. Presence of xyloglucan-hydrolyzing glucanases (xyloglucanases) in arbuscular mycorrhizal symbiosis. Symbiosis 21: 249-261.

Ribéreau-Gayon P, Gautheret RJ, Dunod A, 1968. Les composés phénoliques des végétaux. Dunod Paris.

Romero I, Sánchez S, Moya M, Castro E, Ruiz E, Bravo V, 2007. Fermentation of olive tree pruning acid-hydrolysates by Pachysolen tannophilus. Biochem Eng J 36: 108-115. http://dx.doi.org/10.1016/j.bej.2007.02.006

Salgado JM, Abrunhosa L, Venancio A, Dominguez JM, Belo I, 2014. Integrated use of residues from olive mill and winery for lipase production by solid state fermentation with Aspergillus sp. Appl Biochem Biotechnol 172: 1832-1845. http://dx.doi.org/10.1007/s12010-013-0613-4

Sampedro I, Romero C, Ocampo JA, Brenes M, García I, 2004. Removal of monomeric phenols in dry mill olive residue by saprobic fungi. J Agric Food Chem 52: 4487-4492. http://dx.doi.org/10.1021/jf0400563

Sampedro I, D'Annibale A, Federici F, García-Romera I, Siles JA, Petruccioli M, 2012. Non-supplemented aqueous extract from dry olive mill residues: A possible medium for fungal manganese peroxidase production. Biochem Eng J 65: 96-99. http://dx.doi.org/10.1016/j.bej.2012.03.011

Sánchez C, 2009. Lignocellulosic residues: Biodegradation and bioconversion by fungi. Biotechnol Adv 27: 185-194. http://dx.doi.org/10.1016/j.biotechadv.2008.11.001

Schlosser D, Grey R, Fritsche W, 1997. Patterns of ligninolytic enzymes in Trametes versicolor. Distribution of extra- and intracellular enzyme activities during cultivation on glucose, wheat straw and beech wood. Appl Microbiol Biotechnol 47: 412-418. http://dx.doi.org/10.1007/s002530050949

Spigno G, Pizzorno T, De Faveri DM, 2008. Cellulose and hemicelluloses recovery from grape stalks. Bioresource Technol 99: 4329-4337. http://dx.doi.org/10.1016/j.biortech.2007.08.044

Spigno G, Maggi L, Amendola D, Dragoni M, De Faveri DM, 2013. Influence of cultivar on the lignocellulosic fractionation of grape stalks. Ind Crop Prod 46: 283-289. http://dx.doi.org/10.1016/j.indcrop.2013.01.034

Swamy J, Ramsay JA, 1999. Effects of Mn2+ and NH+4 concentrations on laccase and manganese peroxidase production and Amaranth decoloration by Trametes versicolor. Appl Microbiol Biotechnol 51: 391-396. http://dx.doi.org/10.1007/s002530051408

Tani S, Kawaguchi T, Kobayashi T, 2014. Complex regulation of hydrolytic enzyme genes for cellulosic biomass degradation in filamentous fungi. Appl Microbiol Biotechnol 98: 4829-4837. http://dx.doi.org/10.1007/s00253-014-5707-6

Ten Have R, Teunissen PJM, 2001. Oxidative mechanisms involved in lignin degradation by white-rot fungi. Chem Rev 101: 3397-3413. http://dx.doi.org/10.1021/cr000115l

Ullrich R, Liers C, Schimpke S, Hofrichter M, 2009. Purification of homogeneous forms of fungal peroxygenase. Biotechnol J 4: 1619-1626. http://dx.doi.org/10.1002/biot.200900076

Viniegra-González G, Favela-Torres E, Aguilar CN, Rómero-Gomez SDJ, Díaz-Godínez G, Augur C, 2003. Advantages of fungal enzyme production in solid state over liquid fermentation systems. Biochem Eng J 13: 157-167. http://dx.doi.org/10.1016/S1369-703X(02)00128-6

Wan C, Li Y, 2012. Fungal pretreatment of lignocellulosic biomass. Biotechnol Adv 30: 1447-1457. http://dx.doi.org/10.1016/j.biotechadv.2012.03.003

Wang F, Hu JH, Guo C, Liu CZ, 2014. Enhanced laccase production by Trametes versicolor using corn steep liquor as both nitrogen source and inducer. Biores Technol 166: 602-605. http://dx.doi.org/10.1016/j.biortech.2014.05.068

Wariishi H, Valli K, Gold MH, 1992. Manganese(II) oxidation by manganese peroxidase from the basidiomycete Phanerochaete chrysosporium: Kinetic mechanism and role of chelators. J Biol Chem 267: 23688-23695.

Wolfenden BS, Willson RL, 1982. Radical-cations as reference chromogens in kinetic studies of one-electron transfer reactions: Pulse radiolysis studies of 2,2′-azinobis-(3-ethylbenzthiazoline-6-sulphonate). J Chem Soc Perk T 2: 805-812. http://dx.doi.org/10.1039/P29820000805

Kirsten WJ, Hesselius GU, 1983. Rapid, automatic, high capacity dumas determination of nitrogen. Microchem J 28: 529-547. http://dx.doi.org/10.1016/0026-265X(83)90011-5

Zeng X, Cai Y, Liao X, Zeng X, Li W, Zhang D, 2011. Decolorization of synthetic dyes by crude laccase from a newly isolated Trametes trogii strain cultivated on solid agro-industrial residue. J Hazard Mater 187: 517-525. http://dx.doi.org/10.1016/j.jhazmat.2011.01.068

Published
2016-08-31
How to Cite
Reina, R., Ullrich, R., García-Romera, I., Liers, C., & Aranda, E. (2016). Integrated biovalorization of wine and olive mill by-products to produce enzymes of industrial interest and soil amendments. Spanish Journal of Agricultural Research, 14(3), e0205. https://doi.org/10.5424/sjar/2016143-8961
Section
Agricultural engineering