An Overview of Fungal Applications in the Valorization of Lignocellulosic Agricultural By-Products: The Case of Two-Phase Olive Mill Wastes

  • Rocío Reina
  • Mercedes García-Sánchez
  • Christiane Liers
  • Inmaculada García-Romera
  • Elisabet ArandaEmail author
Part of the Fungal Biology book series (FUNGBIO)


DOR (dry mill olive residue) is an agricultural by-product generated during two-phase olive oil extraction. It is a microtoxic and phytotoxic phenolic-rich lignocellulosic residue and is produced in high amounts in Mediterranean countries. Several techniques have been proposed for its valorization. Agaricomycetes are one of the most efficient lignin-modifying enzyme (LME) producers on Earth (e.g. laccases, peroxidases or the novel peroxygenases). The secretion of these enzymes varies according to the specific strain and also depends on other factors such as the presence of certain elicitors in the medium, like lignocellulosic materials or phenols, which may be crucial to stimulate LME secretion. Due to the enzymatic capability of fungi, numerous studies have been performed in order to valorize the DOR, such as its recent use as a medium for enzyme production or organic soil amendment. An improved valorization of these by-products and a better understanding of fungal enzyme production could lead to the development of biorefineries that utilize various components in biomass and their intermediates, thus maximizing the value derived from biomass feedstock. In this chapter, we summarize some studies performed on this topic (mainly based on the usage of white-rot fungi in the transformation of DOR), and we discuss possible trends, challenges and future prospects for the use of fungi in an environmentally sustainable scenario.


Lignin-modifying enzymes Basidiomycota Ascomycota Dry olive mill residue Phytotoxicity Phenolic compounds Valorization Lignocellulose 



Auxiliary activity


Aryl-alcohol oxidase


Aqueous extract of DOR


Alcohol oxidases


Carbohydrate active enzymes


Carbohydrate-binding modules


Cellobiose dehydrogenase


Carbohydrate esterase


Coprinopsis cinerea peroxidase




Cytochrome P450 monooxygenases


Dye-decolorizing peroxidases


Dry olive mill residue


Glycoside hydrolase


Glucose oxidase


Glyoxal oxidase


Glutathione reductase








Lignin peroxidase


Lignin-modifying enzyme


Lytic polysaccharide monooxygenase


Manganese peroxidase


Oxalate oxidase


Polysaccharide lyase


Class II peroxidases


Reactive oxygen species


Superoxide dismutase


Submerged fermentation


Solid-state fermentation


Two- phase olive mill waste


Unspecific peroxygenase


Versatile peroxidase


White-rot fungi



EA thanks the Ministry of Economy and Competitiveness (MINECO) and FEDER funds for co-funding the Ramón y Cajal contract (RYC-2013-12481). We also wish to thank Bart Mellebeek for proofreading the document.


  1. Alburquerque JA, Gonzálvez J, Garcia D, Cegarra J (2004) Agrochemical characterisation of “alperujo”, a solid by-product of the two-phase centrifugation method for olive oil extraction. Bioresour Technol 91(2):195–200PubMedCrossRefGoogle Scholar
  2. Anh DH, Ullrich R, Benndorf D, Svatoś A, Muck A, Hofrichter M (2007) The coprophilous mushroom Coprinus radians secretes a haloperoxidase that catalyzes aromatic peroxygenation. App Environ Microbiol 73(17):5477–5485CrossRefGoogle Scholar
  3. Aranda E, Sampedro I, Ocampo J, García-Romera I (2004) Contribution of hydrolytic enzymes produced by saprophytic fungi to the decrease in plant toxicity caused by water-soluble substances in olive mill dry residue. Appl Microbiol Biotechnol 64(1):132–135PubMedCrossRefGoogle Scholar
  4. 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 Biodeterior Biodegrad 58(3–4):176–179CrossRefGoogle Scholar
  5. 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(2):229–239PubMedCrossRefGoogle Scholar
  6. Aranda E, Sampedro I, García-Sanchez M, Reina R, Arriagada C, Ocampo JA, García-Romera I (2012) Reduced dry olive residue phytotoxicity in the field by the combination of physical and biological treatments. J Soil Sci Plant Nutr 12(4):631–635Google Scholar
  7. Araújo M, Pimentel FB, Alves RC, Oliveira MBP (2015) Phenolic compounds from olive mill wastes: health effects, analytical approach and application as food antioxidants. Trends Food Sci Technol 45(2):200–211CrossRefGoogle Scholar
  8. Arnstadt T, Hoppe B, Kahl T, Kellner H, Krüger D, Bässler C, Bauhus J, Hofrichter M (2016) Patterns of laccase and peroxidases in coarse woody debris of Fagus sylvatica, Picea abies and Pinus sylvestris and their relation to different wood parameters. Eur J Forest Res 135(1):109–124CrossRefGoogle Scholar
  9. Baldrian P (2006) Fungal laccases-occurrence and properties. FEMS Microbiol Rev 30(2):215–242PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bertozzi CR, Kiessling LL (2001) Chemical glycobiology. Science 291(5512):2357–2364PubMedCrossRefGoogle Scholar
  11. Biely P (2012) Microbial carbohydrate esterases deacetylating plant polysaccharides. Biotechnol Adv 30(6):1575–1588PubMedCrossRefGoogle Scholar
  12. Cadimaliev DA, Revin VV, Atykyan NA, Samuilov VD (2005) Extracellular oxidases of the lignin-degrading fungus Panus tigrinus. Biokhimiya 70(6):850–854Google Scholar
  13. Camarero S, Sarkar S, Ruiz-Dueñas FJ, Martínez MJ, Martínez AT (1999) Description of a versatile peroxidase involved in the natural degradation of lignin that has both manganese peroxidase and lignin peroxidase substrate interaction sites. J Biol Chem 274(15):10324–10330PubMedCrossRefGoogle Scholar
  14. Cambria MT, Ragusa S, Calabrese V, Cambria A (2011) Enhanced laccase production in white-rot fungus Rigidoporus lignosus by the addition of selected phenolic and aromatic compounds. Appl Biochem Biotechnol 163(3):415–422PubMedCrossRefGoogle Scholar
  15. Carbajo JM, Junca H, Terrón MC, González T, Yagüe S, Zapico E, González AE (2002) Tannic acid induces transcription of laccase gene cglcc1 in the white-rot fungus Coriolopsis gallica. Can J Microbiol 48(12):1041–1047PubMedCrossRefGoogle Scholar
  16. Choinowski T, Blodig W, Winterhalter KH, Piontek K (1999) The crystal structure of lignin peroxidase at 1.70 Å resolution reveals a hydroxy group on the C(β) of tryptophan 171: a novel radical site formed during the redox cycle. J Mol Biol 286(3):809–827PubMedCrossRefGoogle Scholar
  17. Collins PJ, Dobson ADW (1997) Regulation of laccase gene transcription in Trametes versicolor. Appl Environ Microbiol 63(9):3444–3450PubMedPubMedCentralGoogle Scholar
  18. Coradetti ST, Craig JP, Xiong Y, Shock T, Tian C, Glass NL (2012) Conserved and essential transcription factors for cellulase gene expression in ascomycete fungi. Proc Natl Acad Sci U S A 109(19):7397–7402PubMedPubMedCentralCrossRefGoogle Scholar
  19. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6(11):850–861PubMedCrossRefGoogle Scholar
  20. Daniel G (2003) Microview of wood under degradation by bacteria and fungi. ACS symposium series. In: Goodell B, Nicholas DD, Schultz TP (eds) Wood Deterioration and Preservation: Advances in Our Changing World. ACS Journals pp 34–72Google Scholar
  21. Dermeche S, Nadour M, Larroche C, Moulti-Mati F, Michaud P (2013) Olive mill wastes: biochemical characterizations and valorization strategies. Process Biochem 48(10):1532–1552CrossRefGoogle Scholar
  22. Di Bene C, Pellegrino E, Debolini M, Silvestri N, Bonari E (2013) Short- and long-term effects of olive mill wastewater land spreading on soil chemical and biological properties. Soil Biol Biochem 56:21–30CrossRefGoogle Scholar
  23. 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(1):133–142PubMedCrossRefGoogle Scholar
  24. Dong JL, Zhang YZ (2004) Purification and characterization of two laccase isoenzymes from a ligninolytic fungus Trametes gallica. Prep Biochem Biotech 34:179–194CrossRefGoogle Scholar
  25. Eudes A, Liang Y, Mitra P, Loqué D (2014) Lignin bioengineering. Curr Opin Biotechnol 26:189–198PubMedCrossRefGoogle Scholar
  26. Floudas D, Held BW, Riley R, Nagy LG, Koehler G, Ransdell AS, Younus H, Chow J, Chiniquy J, Lipzen A, Tritt A, Sun H, Haridas S, LaButti K, Ohm RA, Kües U, Blanchette RA, Grigoriev IV, Minto RE, Hibbett DS (2015) Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii. Fungal Genet Biol 76:78–92PubMedPubMedCentralCrossRefGoogle Scholar
  27. García-Sánchez M, Garrido I, IDJ C, Casero PJ, Espinosa F, García-Romera I, Aranda E (2012) Defence response of tomato seedlings to oxidative stress induced by phenolic compounds from dry olive mill residue. Chemosphere 89(6):708–716PubMedCrossRefGoogle Scholar
  28. García-Sánchez M, Palma JM, Ocampo JA, García-Romera I, Aranda E (2014a) Arbuscular mycorrhizal fungi alleviate oxidative stress induced by ADOR and enhance antioxidant responses of tomato plants. J Plant Physiol 171(6):421–428PubMedCrossRefGoogle Scholar
  29. García-Sánchez M, Paradiso A, García-Romera I, Aranda E, de Pinto MC (2014b) Bioremediation of dry olive-mill residue removes inhibition of growth induced by this waste in tomato plants. Int J Environ Sci Technol 11(1):21–32CrossRefGoogle Scholar
  30. Garrido I, García-Sánchez M, Casimiro I, Casero PJ, García-Romera I, Ocampo JA, Espinosa F (2012) Oxidative stress induced in sunflower seedling roots by aqueous dry olive-mill residues. PLoS One 7(9):e46137PubMedPubMedCentralCrossRefGoogle Scholar
  31. Girard V, Dieryckx C, Job C, Job D (2013) Secretomes: the fungal strike force. Proteomics 13(3–4):597–608PubMedCrossRefGoogle Scholar
  32. Gröbe G, Ullrich R, Pecyna MJ, Kapturska D, Friedrich S, Hofrichter M, Scheibner K (2011) High-yield production of aromatic peroxygenase by the agaric fungus Marasmius rotula. AMB Express 1(1):1–11CrossRefGoogle Scholar
  33. Hasunuma T, Okazaki F, Okai N, Hara KY, Ishii J, Kondo A (2013) A review of enzymes and microbes for lignocellulosic biorefinery and the possibility of their application to consolidated bioprocessing technology. Bioresour Technol 135:513–522PubMedCrossRefGoogle Scholar
  34. Hemsworth GR, Henrissat B, Davies GJ, Walton PH (2014) Discovery and characterization of a new family of lytic polysaccharide monooxygenases. Nat Chem Biol 10(2):122–126PubMedCrossRefGoogle Scholar
  35. Hildén K, Martínez AT, Hatakka A, Lundell T (2005) The two manganese peroxidases Pr-MnP2 and Pr-MnP3 of Phlebia radiata, a lignin-degrading basidiomycete, are phylogenetically and structurally divergent. Fungal Genet Biol 42:403–419PubMedCrossRefGoogle Scholar
  36. Hildén K, Mäkelä MR, Steffen KT, Hofrichter M, Hatakka A, Archer DB, Lundell TK (2014) Biochemical and molecular characterization of an atypical manganese peroxidase of the litter-decomposing fungus Agrocybe praecox. Fungal Genet Biol 72:131–136PubMedCrossRefGoogle Scholar
  37. Hofrichter M, Ullrich R, Pecyna MJ, Liers C, Lundell T (2010) New and classic families of secreted fungal heme peroxidases. Appl Microbiol Biotechnol 87(3):871–897PubMedCrossRefGoogle Scholar
  38. Hofrichter M, Kellner H, Pecyna MJ, Ullrich R (2015) Fungal unspecific peroxygenases: heme-thiolate proteins that combine peroxidase and cytochrome P450 properties, Monooxygenase, Peroxidase and Peroxygenase Properties and Mechanisms of Cytochrome P450. In: Hrycay EG, Bandiera SM (eds) Springer, Cham, pp 341–368Google Scholar
  39. Hovorka M, Száková J, García-Sánchez M, Acebal MB, García-Romera I, Tlustoš P (2016) Risk element sorption/desorption characteristics of dry olive residue: a technique for the potential immobilization of risk elements in contaminated soils. Environ Sci Pollut Res 23(22):22614–22622CrossRefGoogle Scholar
  40. Johansson T, Nyman PO (1993) Isozymes of lignin peroxidase and manganese (II) peroxidase from the white-rot basidiomycete Trametes versicolor: I. Isolation of enzyme forms and characterization of physical and catalytic properties. Arch Biochem Biophys 300(1):49–56PubMedCrossRefGoogle Scholar
  41. Johjima T, Ohkuma M, Kudo T (2003) Isolation and cDNA cloning of novel hydrogen peroxide-dependent phenol oxidase from the basidiomycete Termitomyces albuminosus. Appl Microbiol Biotechnol 61(3):220–225PubMedCrossRefGoogle Scholar
  42. Jung S, Song Y, Kim HM, Bae HJ (2015) Enhanced lignocellulosic biomass hydrolysis by oxidative lytic polysaccharide monooxygenases (LPMOs) GH61 from Gloeophyllum trabeum. Enzyme Microb Technol 77:38–45PubMedCrossRefGoogle Scholar
  43. Justino CIL, Pereira R, Freitas AC, Rocha-Santos TAP, Panteleitchouk TSL, Duarte AC (2012) Olive oil mill wastewaters before and after treatment: a critical review from the ecotoxicological point of view. Ecotoxicology 21(2):615–629PubMedCrossRefGoogle Scholar
  44. Kellner H, Luis P, Pecyna MJ, Barbi F, Kapturska D, Kruger D, Zak DR, Marmeisse R, Vandenbol M, Hofrichter M (2014) Widespread occurrence of expressed fungal secretory peroxidases in forest soils. PLoS One 9(4):e95557PubMedPubMedCentralCrossRefGoogle Scholar
  45. Keyser P, Kirk T, Zeikus J (1978) Ligninolytic enzyme system of Phanaerochaete chrysosporium: synthesized in the absence of lignin in response to nitrogen starvation. J Bacteriol 135(3):790–797PubMedPubMedCentralGoogle Scholar
  46. Kim SJ, Shoda M (1999) Purification and characterization of a novel peroxidase from Geotrichum candidum Dec 1 involved in decolorization of dyes. Appl Environ Microbiol 65(3):1029–1035PubMedPubMedCentralGoogle Scholar
  47. Kües U (2015) Fungal enzymes for environmental management. Curr Opin Biotechnol 33:268–278PubMedCrossRefGoogle Scholar
  48. Kuhad RC, Singh A (1993) Lignocellulose biotechnology. Current and future prospects. Crit Rev Biotechnol 13(2):151–172CrossRefGoogle Scholar
  49. Lechner B, Papinutti V (2006) Production of lignocellulosic enzymes during growth and fruiting of the edible fungus Lentinus tigrinus on wheat straw. Process Biochem 41(3):594–598CrossRefGoogle Scholar
  50. Leitner C, Hess J, Galhaup C, Ludwig R, Nidetzky B, Kulbe KD, Haltrich D (2002) Purification and characterization of a laccase from the white-rot fungus Trametes multicolor. Appl Biochem Biotech-A Enzyme Eng Biotechnol 98–100:497–507CrossRefGoogle Scholar
  51. Liers C, Ullrich R, Steffen K, Hatakka A, Hofrichter M (2006) Mineralization of 14C-labelled synthetic lignin and extracellular enzyme activities of the wood-colonizing ascomycetes Xylaria hypoxylon and Xylaria polymorpha. Appl Microbiol Biotechnol 69(5):573–579PubMedCrossRefGoogle Scholar
  52. Liers C, Ullrich R, Pecyna M, Schlosser D, Hofrichter M (2007) Production, purification and partial enzymatic and molecular characterization of a laccase from the wood-rotting ascomycete Xylaria polymorpha. Enzym Microb Technol 41(6):785–793CrossRefGoogle Scholar
  53. Liers C, Bobeth C, Pecyna M, Ullrich R, Hofrichter M (2010) DyP-like peroxidases of the jelly fungus Auricularia auricula-judae oxidize nonphenolic lignin model compounds and high-redox potential dyes. Appl Microbiol Biotechnol 85(6):1869–1879PubMedCrossRefGoogle Scholar
  54. 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(1):91–102PubMedCrossRefGoogle Scholar
  55. Liers C, Pecyna MJ, Kellner H, Worrich A, Zorn H, Steffen KT, Hofrichter M, Ullrich R (2013) Substrate oxidation by dye-decolorizing peroxidases (DyPs) from wood- and litter-degrading agaricomycetes compared to other fungal and plant heme-peroxidases. Appl Microbiol Biotechnol 97(13):5839–5849PubMedCrossRefGoogle Scholar
  56. Liese W (1970) Ultrastructural aspects of woody tissue disintegration. Annu Rev Phytopathol 8(1):231–258CrossRefGoogle Scholar
  57. Linares A (2003) Detoxification of semisolid olive-mill wastes and pine-chip mixtures using Phanerochaete flavido-alba. Chemosphere 51(9):887–891PubMedCrossRefGoogle Scholar
  58. Linde D, Ruiz-Dueñas FJ, Fernández-Fueyo E, Guallar V, Hammel KE, Pogni R, Martínez AT (2015) Basidiomycete DyPs: genomic diversity, structural–functional aspects, reaction mechanism and environmental significance. Arch Biochem Biophys 574:66–74PubMedCrossRefGoogle Scholar
  59. Lombard V, Bernard T, Rancurel C, Brumer H, Coutinho PM, Henrissat B (2010) A hierarchical classification of polysaccharide lyases for glycogenomics. Biochem J 432(3):437–444PubMedCrossRefGoogle Scholar
  60. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42(D1):D490–D4D5PubMedCrossRefGoogle Scholar
  61. Lopes V, Farias M, Belo I, Coelho M (2016) Nitrogen sources on TPOMW valorization through solid state fermentation performed by Yarrowia lipolytica. Braz J Chem Eng 33(2):261–270CrossRefGoogle Scholar
  62. López-Piñeiro A, Albarrán A, Nunes JMR, Barreto C (2008) Short and medium-term effects of two-phase olive mill waste application on olive grove production and soil properties under semiarid mediterranean conditions. Bioresour Technol 99(17):7982–7977PubMedCrossRefGoogle Scholar
  63. Lundell T (1993) Ligninolytic system of the white-rot fungus Phlebia radiata: lignin model compound studies. FAO [T. Lundell]Google Scholar
  64. Lyashenko AV, Bento I, Zaitsev VN, Zhukhlistova NE, Zhukova YN, Gabdoulkhakov AG, Morgunova EY, Voelter W, Kachalova GS, Stepanova EV, Koroleva OV, Lamzin VS, Tishkov VI, Betzel C, Lindley PF, Mikhailov AM (2006) X-ray structural studies of the fungal laccase from Cerrena maxima. J Biol Inorg Chem 11(8):963–973PubMedCrossRefGoogle Scholar
  65. Mac Donald MJ, Paterson A, Broda P (1984) Possible relationship between cyclic AMP and idiophasic metabolism in the white rot fungus Phanerochaete chrysosporium. J Bacteriol 160(1):470–472Google Scholar
  66. Madhavi V, Lele SS (2009) Laccase: properties and applications. BioResources 4(4):1694–1717Google Scholar
  67. Marx IJ, Van Wyk N, Smit S, Jacobson D, Viljoen-Bloom M, Volschenk H (2013) Comparative secretome analysis of Trichoderma asperellum S4F8 and Trichoderma reesei Rut C30 during solid-state fermentation on sugarcane bagasse. Biotechnol Biofuels 6(1):1CrossRefGoogle Scholar
  68. Mateo JJ, Maicas S (2015) Valorization of winery and oil mill wastes by microbial technologies. Food Res Int 73:13–25CrossRefGoogle Scholar
  69. McKendry P (2002) Energy production from biomass (part 1): overview of biomass. Bioresour Technol 83(1):37–46PubMedCrossRefGoogle Scholar
  70. Medie FM, Davies GJ, Drancourt M, Henrissat B (2012) Genome analyses highlight the different biological roles of cellulases. Nat Rev Microbiol 10(3):227–234CrossRefGoogle Scholar
  71. Michniewicz A, Ullrich R, Ledakowicz S, Hofrichter M (2006) The white-rot fungus Cerrena unicolor strain 137 produces two laccase isoforms with different physico-chemical and catalytic properties. Appl Microbiol Biotechnol 69(6):682–688PubMedCrossRefGoogle Scholar
  72. Moreira PR, Duez C, Dehareng D, Antunes A, Almeida-Vara E, Frère JM, Malcata FX, Duarte J (2005) Molecular characterisation of a versatile peroxidase from a Bjerkandera strain. J Biotechnol 118(4):339–352PubMedCrossRefGoogle Scholar
  73. Morillo JA, Antizar-Ladislao B, Monteoliva-Sanchez M, Ramos-Cormenzana A, Russell NJ (2009) Bioremediation and biovalorisation of olive-mill wastes. Appl Microbiol Biotechnol 82(1):25–39PubMedCrossRefGoogle Scholar
  74. Mosier N, Wyman C, Dale B, Elander R, Lee YY, Holtzapple M, Ladisch M (2005) Features of promising technologies for pretreatment of lignocellulosic biomass. Bioresour Technol 96(6):673–686CrossRefPubMedGoogle Scholar
  75. Moumen A, Yáñez-Ruiz DR, Martín-García I, Molina-Alcaide E (2008) Fermentation characteristics and microbial growth promoted by diets including two-phase olive cake in continuous fermenters. J Anim Physiol Anim Nutr 92(1):9–17Google Scholar
  76. Muñoz C, Guillén F, Martínez AT, Martínez MJ (1997) Induction and characterization of laccase in the ligninolytic fungus Pleurotus eryngii. Curr Microbiol 34(1):1–5PubMedCrossRefGoogle Scholar
  77. Nghi DH, Bittner B, Kellner H, Jehmlich N, Ullrich R, Pecyna MJ, Nousiainen P, Sipila J, Huong LM, Hofrichter M, Liers C (2012) The wood rot ascomycete Xylaria polymorpha produces a novel GH78 glycoside hydrolase that exhibits α-L-rhamnosidase and feruloyl esterase activities and releases hydroxycinnamic acids from lignocelluloses. Appl Environ Microbiol 78(14):4893–48901PubMedCentralCrossRefGoogle Scholar
  78. O’Sullivan AC (1997) Cellulose: the structure slowly unravels. Cellulose 4(3):173–207CrossRefGoogle Scholar
  79. Parati F, Altieri R, Esposito A, Lobianco A, Pepi M, Montesi L, Nair T (2011) Validation of thermal composting process using olive mill solid waste for industrial scale cultivation of Agaricus bisporus. Int Biodeterior Biodegrad 65(1):160–163CrossRefGoogle Scholar
  80. Polyakov KM, Fedorova TV, Stepanova EV, Cherkashin EA, Kurzeev SA, Strokopytov BV, Lamzin VS, Koroleva OV (2009) Structure of native laccase from Trametes hirsuta at 1.8 Å resolution. Acta Crystallogr Sect D: Struct Biol 65:611–617CrossRefGoogle Scholar
  81. Priego-Capote F, Ruiz-Jiménez J, Luque De Castro MD (2004) Fast separation and determination of phenolic compounds by capillary electrophoresis-diode array detection: application to the characterisation of alperujo after ultrasound-assisted extraction. J Chromatogr A 1045(1–2):239–246PubMedCrossRefGoogle Scholar
  82. Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz PF, Marita JM, Hatfield RD, Ralph SA, Christensen JH, Boerjan W (2004) Lignins: natural polymers from oxidative coupling of 4-hydroxyphenyl-propanoids. Phytochem Rev 3:29–60CrossRefGoogle Scholar
  83. 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(7):6CrossRefGoogle Scholar
  84. 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 72:99–105PubMedCrossRefGoogle Scholar
  85. 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. Span J Agric Res 14(3):0205CrossRefGoogle Scholar
  86. Reina R, Liers C, García-Romera I, Aranda E (2017) Enzymatic mechanisms and detoxification of dry olive-mill residue by Cyclocybe aegerita, Mycetinis alliaceus and Chondrostereum purpureum. Int Biodeterior Biodegrad 117:89–96CrossRefGoogle Scholar
  87. Roig A, Cayuela ML, Sánchez-Monedero MA (2006) An overview on olive mill wastes and their valorisation methods. Waste Manag 26(9):960–969PubMedCrossRefGoogle Scholar
  88. Roselló-Soto E, Koubaa M, Moubarik A, Lopes RP, Saraiva JA, Boussetta N, Grimi N, Barba FJ (2015) Emerging opportunities for the effective valorization of wastes and by-products generated during olive oil production process: non-conventional methods for the recovery of high-added value compounds. Trends Food Sci Technol 45(2):296–310CrossRefGoogle Scholar
  89. Roy BP, Paice MG, Archibald FS, Misra SK, Misiak LE (1994) Creation of metal-complexing agents, reduction of manganese dioxide, and promotion of manganese peroxidase-mediated Mn(III) production by cellobiose: quinone oxidoreductase from Trametes versicolor. J Biol Chem 269(31):19745–19750PubMedGoogle Scholar
  90. Rugolo M, Levin L, Lechner BE (2016) Flammulina velutipes: an option for “alperujo” use. Rev Iberoam Micol 33(4):242–247PubMedCrossRefGoogle Scholar
  91. Ruiz-Dueñas F, Camarero S, Perez-Boada M, Martínez M, Martínez A (2001) A new versatile peroxidase from Pleurotus. Biochem Soc Trans 29(Pt 2):116–122PubMedCrossRefGoogle Scholar
  92. Ruiz-Dueñas FJ, Morales M, Mate MJ, Romero A, Martínez MJ, Smith AT, Martínez AT (2008) Site-directed mutagenesis of the catalytic tryptophan environment in Pleurotus eryngii versatile peroxidase. Biochemistry 47(6):1685–1695PubMedCrossRefGoogle Scholar
  93. Ruiz-Rodríguez A, Polonia I, Soler-Rivas C, Wichers HJ (2011) Ligninolytic enzymes activities of Oyster mushrooms cultivated on OMW (olive mill waste) supplemented media, spawn and substrates. Int Biodeter Biodegr 65(2):285–293CrossRefGoogle Scholar
  94. Salgado JM, Moreira C, Abrunhosa L, Venâncio A, Domínguez JM, Belo I (2012) Evaluation of substrate composition for lignocellulolytic enzymes production by solid state fermentation of wastes from olive oil and wine industries. 1° CIAB Congreso Iberoamericano sobre BiorrefineriasGoogle Scholar
  95. 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(4):1832–1845PubMedCrossRefGoogle Scholar
  96. Salvachúa D, Prieto A, Martínez ÁT, Martínez MJ (2013a) Characterization of a novel dye-decolorizing peroxidase (DyP)-type enzyme from Irpex lacteus and its application in enzymatic hydrolysis of wheat straw. Appl Environ Microbiol 79(14):4316–4324PubMedPubMedCentralCrossRefGoogle Scholar
  97. Salvachúa D, Prieto A, Mattinen ML, Tamminen T, Liitiä T, Lille M, Willför S, Martínez AT, Martínez MJ, Faulds CB (2013b) Versatile peroxidase as a valuable tool for generating new biomolecules by homogeneous and heterogeneous cross-linking. Enzym Microb Technol 52(6–7):303–311CrossRefGoogle Scholar
  98. Sampedro I, Aranda E, Martín J, García-Garrido JM, García-Romera I, Ocampo JA (2004a) Saprobic fungi decrease plant toxicity caused by olive mill residues. Appl Soil Ecol 26(2):149–156CrossRefGoogle Scholar
  99. Sampedro I, Romero C, Ocampo JA, Brenes M, García I (2004b) Removal of monomeric phenols in dry mill olive residue by saprobic fungi. J Agric Food Chem 52(14):4487–4492PubMedCrossRefGoogle Scholar
  100. Sampedro I, D’Annibale A, Ocampo JA, Stazi SR, García-Romera I (2005) Bioconversion of olive-mill dry residue by Fusarium lateritium and subsequent impact on its phytotoxicity. Chemosphere 60(10):1393–1400PubMedCrossRefGoogle Scholar
  101. 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(18):3547–3554PubMedCrossRefGoogle Scholar
  102. 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 Biodeter Biodegr 60(2):116–125CrossRefGoogle Scholar
  103. 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(8):1383–1389PubMedCrossRefGoogle Scholar
  104. Sampedro I, Cajthaml T, Marinari S, Stazi SR, Grego S, Petruccioli M, Federici F, D’Annibale A (2009) Immobilized inocula of white-rot fungi accelerate both detoxification and organic matter transformation in two-phase dry olive-mill residue. J Agric Food Chem 57(12):5452–5460PubMedCrossRefGoogle Scholar
  105. Sampedro I, D’Annibale A, Federici F, Romera IG, Siles JA, Petruccioli M (2012) Non-supplemented aqueous extract from dry olive mill residue: a possible medium for fungal manganese peroxidase production. Biochem Eng J 65:96–99CrossRefGoogle Scholar
  106. Sánchez C (2009) Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnol Adv 27(2):185–194PubMedPubMedCentralCrossRefGoogle Scholar
  107. Saparrat MCN, Jurado M, Díaz R, Romera IG, Martínez MJ (2010) Transformation of the water soluble fraction from “alpeorujo” by Coriolopsis rigida: the role of laccase in the process and its impact on Azospirillum brasiliense survival. Chemosphere 78(1):72–76PubMedCrossRefGoogle Scholar
  108. Scheibner M, Hülsdau B, Zelena K, Nimtz M, de Boer L, Berger R, Zorn H (2008) Novel peroxidases of Marasmius scorodonius degrade β-carotene. Appl Microbiol Biotechnol 77(6):1241–1250PubMedCrossRefGoogle Scholar
  109. Siles JA, Cajthaml T, Hernández P, Pérez-Mendoza D, García-Romera I, Sampedro I (2015) Shifts in soil chemical properties and bacterial communities responding to biotransformed dry olive residue used as organic amendment. Microb Ecol 70(1):231–243PubMedCrossRefGoogle Scholar
  110. Sugiura M, Hirai H, Nishida T (2003) Purification and characterization of a novel lignin peroxidase from white-rot fungus Phanerochaete sordida YK-624. FEMS Microbiol Lett 224(2):285–290PubMedCrossRefGoogle Scholar
  111. Sun J, Tian C, Diamond S, Glass NL (2012) Deciphering transcriptional regulatory mechanisms associated with hemicellulose degradation in Neurospora crassa. Eukaryot Cell 11(4):482–493PubMedPubMedCentralCrossRefGoogle Scholar
  112. Sun S, Sun S, Cao X, Sun R (2016) The role of pretreatment in improving the enzymatic hydrolysis of lignocellulosic materials. Bioresour Technol 199:49–58PubMedCrossRefGoogle Scholar
  113. Sygmund C, Santner P, Krondorfer I, Peterbauer CK, Alcalde M, Nyanhongo GS, Guebitz GM, Ludwig R (2013) Semi-rational engineering of cellobiose dehydrogenase for improved hydrogen peroxide production. Microb Cell Factories 12:38CrossRefGoogle Scholar
  114. Tani S, Kawaguchi T, Kobayashi T (2014) Complex regulation of hydrolytic enzyme genes for cellulosic biomass degradation in filamentous fungi. Appl Microbiol Biotechnol 98(11):4829–4837PubMedCrossRefGoogle Scholar
  115. Teeri TT, Reinikainen T, Ruohonen L, Jones TA, Knowles JKC (1992) Domain function in Trichoderma reesei cellobiohydrolases. J Biotechnol 24(2):169–176CrossRefGoogle Scholar
  116. Tortosa G, Alburquerque JA, Ait-Baddi G, Cegarra J (2012) The production of commercial organic amendments and fertilisers by composting of two-phase olive mill waste (“alperujo”). J Clean Prod 26:48–55CrossRefGoogle Scholar
  117. Ullrich R, Nüske J, Scheibner K, Spantzel J, Hofrichter M (2004) Novel haloperoxidase from the agaric basidiomycete Agrocybe aegerita oxidizes aryl alcohols and aldehydes. Appl Environ Microbiol 70(8):4575–4581PubMedPubMedCentralCrossRefGoogle Scholar
  118. Ullrich R, Dung NL, Hofrichter M (2005) Laccase from the medicinal mushroom Agaricus blazei: production, purification and characterization. Appl Microbiol Biotechnol 67(3):357–363PubMedCrossRefGoogle Scholar
  119. Valadares F, Gonçalves TA, Gonçalves DSPO, Segato F, Romanel E, Milagres AMF, Squina FM, Ferraz A (2016) Exploring glycoside hydrolases and accessory proteins from wood decay fungi to enhance sugarcane bagasse saccharification. Biotechnol Biofuels 9(1):110PubMedPubMedCentralCrossRefGoogle Scholar
  120. Van Den Brink J, De Vries RP (2011) Fungal enzyme sets for plant polysaccharide degradation. Appl Microbiol Biotechnol 91(6):1477–1492PubMedPubMedCentralCrossRefGoogle Scholar
  121. Várnai A, Mäkelä MR, Djajadi DT, Rahikainen J, Hatakka A, Viikari L (2014) Carbohydrate-binding modules of fungal cellulases. Occurrence in nature, function, and relevance in industrial biomass conversion. Adv Appl Microbiol 88:103–165PubMedCrossRefGoogle Scholar
  122. Wymelenberg AV, Gaskell J, Mozuch M, Kersten P, Sabat G, Martínez D, Cullen D (2009) Transcriptome and secretome analyses of Phanerochaete chrysosporium reveal complex patterns of gene expression. Appl Environ Microbiol 75(12):4058–4068CrossRefGoogle Scholar
  123. Yang F, Jensen JD, Svensson B, Jorgensen HJ, Collinge DB, Finnie C (2012) Secretomics identifies Fusarium graminearum proteins involved in the interaction with barley and wheat. Mol Plant Pathol 13(5):445–453PubMedCrossRefGoogle Scholar
  124. Yaver DS, Xu F, Golightly EJ, Brown KM, Brown SH, Rey MW, Schneider P, Halkier T, Mondorf K, Dalbøge H (1996) Purification, characterization, molecular cloning, and expression of two laccase genes from the white rot basidiomycete Trametes villosa. Appl Environ Microbiol 62(3):834–841PubMedPubMedCentralGoogle Scholar
  125. Yoshida T, Tsuge H, Hisabori T, Sugano Y (2012) Crystal structures of dye-decolorizing peroxidase with ascorbic acid and 2, 6-dimethoxyphenol. FEBS Lett 586(24):4351–4356PubMedCrossRefGoogle Scholar
  126. Yu W, Liu W, Huang H, Zheng F, Wang X, Wu Y, Li K, Xie X, Jin Y (2014) Application of a novel alkali-tolerant thermostable DyP-type peroxidase from Saccharomonospora viridis DSM 43017 in biobleaching of eucalyptus kraft pulp. PloS One 9(10):e110319PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Rocío Reina
    • 1
  • Mercedes García-Sánchez
    • 3
    • 2
  • Christiane Liers
    • 4
  • Inmaculada García-Romera
    • 1
  • Elisabet Aranda
    • 5
    Email author
  1. 1.Department of Soil Microbiology and Symbiotic SystemsConsejo Superior de Investigaciones Científicas (CSIC), Estación Experimental del Zaidín (EEZ)GranadaSpain
  2. 2.UMR Eco&sols. Ecologie fonctionnelle & Biogéochimie des soils & Agro-écosystèmesMontpellier Cedex 2France
  3. 3.Environmental Chemistry and Plant Nutrition, Faculty of Agrobiology, Food and Natural ResourcesCzech University of Life SciencesSuchdolCzech Republic
  4. 4.Department of Bio and Environmental SciencesDresden University of Technology, International Institute ZittauZittauGermany
  5. 5.Department of MicrobiologyUniversity of Granada, Institute of Water ResearchGranadaSpain

Personalised recommendations