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Applied Microbiology and Biotechnology

, Volume 84, Issue 5, pp 803–810 | Cite as

Occurrence, properties, and applications of feruloyl esterases

  • Takuya KosekiEmail author
  • Shinya Fushinobu
  • Ardiansyah
  • Hitoshi Shirakawa
  • Michio Komai
Mini-Review

Abstract

Feruloyl esterases hydrolyze the ester linkages of ferulic and diferulic acids present in plant cell walls. This interesting group of enzymes also has a potentially broad range of applications in the pharmaceutical and agri-food industries. An overview of the current knowledge of fungal feruloyl esterases focusing on the diverse of substrate specificity and potential applications is presented in this review. Furthermore, biological functions of ferulic acid are discussed.

Keywords

Feruloyl esterases Ferulic acid Fungi Substrate specificity Diversity Applications 

References

  1. Ardiansyah, Shirakawa H, Koseki T, Komai M (2008) Novel effects of a single administration of ferulic acid on the regulation of blood pressure and the hepatic lipid metabolic profile in stroke-prone spontaneously hypertensive rats. J Agric Food Chem 56:2825–2830CrossRefGoogle Scholar
  2. Bartolomé B, Faulds CB, Kroon PA, Waldron K, Gilbert HJ, Hazlewood G, Wiiliamson G (1997) An Aspergillus niger esterase (ferulic acid esterase III) and a recombinant Pseudomonas fluorescens subsp. cellulosa esterase (XylD) release a 5–5′ ferulic dehydrodimer (diferulic acid) from barley and wheat cell walls. Appl Environ Microbiol 63:208–212Google Scholar
  3. Benoit I, Navarro D, Marnet N, Rakotomanomana N, Lesage-Meessen L, Sigoillot J-C, Asther M (2006) Feruloyl esterases as a tool for the release of phenolic compounds from agro-industrial by-products. Carbohydr Res 341:1820–1827CrossRefGoogle Scholar
  4. Benoit I, Danchin EGJ, Bleichrodt RJ, de Vries RP (2008) Biotechnological applications and potential of fungal feruloyl esterases based on prevalence, classification and biochemical diversity. Biotechnol Lett 30:387–396CrossRefGoogle Scholar
  5. Blum DL, Kataeva IA, Li XL, Ljungdahl LG (2000) Feruloyl esterase activity of the Clostridium thermocellum cellulosome can be attributed to previously unknown domains of XynY and XynZ. J Bacteriol 182:1346–1351CrossRefGoogle Scholar
  6. Borneman WS, Ljungdahl LG, Hartley RD, Akin DE (1991) Isolation and partial characterization of p-coumaroyl esterase from the anaerobic fungus Neocallimastix strain MC-2. Appl Environ Microbiol 57:2337–2344Google Scholar
  7. Borneman WS, Ljungdahl LG, Hartley RD, Akin DE (1992) Purification and partial characterization of two feruloyl esterases from the anaerobic fungus Neocallimastix strain MC-2. Appl Environ Microbiol 58:3762–3766Google Scholar
  8. Bourne Y, Hasper AA, Chahinian H, Juin M, de Graaff LH, Marchot P (2004) Aspergillus niger protein EstA defines a new class of fungal esterases within α/β hydrolase fold superfamily of proteins. Structure 12:677–687CrossRefGoogle Scholar
  9. Colquhoun U, Ralet MC, Thibault JF, Faulds CB, Williamson G (1994) Feruloylated oligosaccharides from cell wall polysaccharides. Part II: Structure and identification of feruloylated oligosaccharides from sugar beet pulp by NMR spectroscopy. Carbohydr Res 263:243–256CrossRefGoogle Scholar
  10. Crepin VF, Faulds CB, Connerton IF (2003a) A non-modular type B feruloyl esterase from Neurospora crassa exhibits concentration-dependent substrate inhibition. Biochem J 370:417–427CrossRefGoogle Scholar
  11. Crepin VF, Faulds CB, Connerton IF (2003b) Production and characterization of the Talaromyces stipitatus feruloyl esterase FaeC in Pichia pastoris: identification of the nucleophilic serine. Protein Expr Purifi 29:176–184Google Scholar
  12. Crepin VF, Faulds CB, Connerton IF (2004a) Identification of a type-D feruloyl esterase from Neurospora crassa. Appl Microbiol Biotechnol 63:567–570CrossRefGoogle Scholar
  13. Crepin VF, Faulds CB, Connerton IF (2004b) Functional classification of the microbial feruloyl esterases. Appl Microbiol Biotechnol 63:647–652CrossRefGoogle Scholar
  14. de Vries RP, Visser J (1999) Regulation of the feruloyl esterase (faeA) gene from Aspergillus niger. Appl Environ Microbiol 65:5500–5503Google Scholar
  15. de Vries RP, Michelsen B, Poulsen CH, Kroon PA, van den Heuvel RH, Faulds CB, Williamson G, van den Hombergh JP, Visser J (1997) The faeA genes from Aspergilus niger and Aspergillus tubingesis encode ferulic acid esterases involved in degradation of complex cell wall polysaccharides. Appl Environ Microbiol 63:4638–4644Google Scholar
  16. de Vries RP, van Kuyk PA, Kester HCM, Visser J (2002) The Aspergillus niger faeB gene encodes a second feruloyl esterase involved in pectin and xylan degradation and is specifically induced in the presence of aromatic compounds. Biochem J 363:377–386CrossRefGoogle Scholar
  17. Donaghy J, McKay AM (1995) Production of feruloyl/p-coumaroyl esterase activity by Penicillium expansum, Penicillium brevicompactum and Aspergillus niger. J Appl Bacteriol 79:657–662Google Scholar
  18. Donaghy J, McKay AM (1997) Purification and characterisation of a feruloyl esterase from the fungus Penicillium expansum. J Appl Microbiol 83:718–726CrossRefGoogle Scholar
  19. Farrell AE, Plevin RJ, Turner BT, Jones AD, O'Hare M, Kammen DM (2006) Ethanol can contribute to energy and environmental goals. Science 311(5760):506–508CrossRefGoogle Scholar
  20. Faulds CB, Williamson G (1993) Ferulic acid esterase from Aspergillus niger: purification and partial characterization of two forms from a commercial source of pectinase. Biotechnol Appl Biochem 17:349–359Google Scholar
  21. Faulds CB, Williamson G (1994) Purification and characterization of a ferulic acid esterase (FAE-III) from Aspergillus niger: specificity for the phenolic moiety and binding to microcrystalline cellulose. Microbiology 140:779–787CrossRefGoogle Scholar
  22. Faulds CB, de Vries RP, Kroon PA, Visser J, Williamson G (1997) Influence of ferulic acid on the production of feruloyl esterase by Aspergillus niger. FEMS Microbiol Lett 157:239–244CrossRefGoogle Scholar
  23. Ferreira LMA, Wood TM, Williamson G, Faulds CB, Hazlewood G, Gilbert HJ (1993) A modular esterase from Pseudomonas fluorescens subsp. cellulosa contains a non-catalytic binding domain. Biochem J 294:349–355Google Scholar
  24. Fillingham IJ, Kroon PA, Williamson G, Gilbert HJ, Hazlewood GP (1999) A modular cinnamoyl ester hydrolase from the anaerobic fungus Piromyces equi acts synergistically with xylanase and is part of a multiprotein cellulose-binding cellulose-hemicellulose complex. Biochem J 343:215–224CrossRefGoogle Scholar
  25. Fry SC (1986) Cross-linking matrix polymers in the growing cell walls of angiosperms. Annu Rev Plant Physiol 37:165–186CrossRefGoogle Scholar
  26. Garcia-Conesa MT, Crepin VF, Goldson AJ, Williamson G, Cummings NJ, Connerton IF, Faulds CB, Kroon PA (2004) The feruloyl esterase system of Talaromyces stipitatus: production of three discrete feruloyl esterases, including a novel enzyme, TsFaeC, with a broad substrate specificity. J Biotechnol 108:227–241CrossRefGoogle Scholar
  27. Grabber JH, Ralph J, Hatfield RD (1998) Ferulate cross-links limit the enzymatic degradation of synthetically lignified primary walls of maize. J Agric Food Chem 46:2609–2614CrossRefGoogle Scholar
  28. Guglielmetti S, de Noni I, Caracciolo F, Molinari F, Parini C, Mora D (2008) Bacterial cinnamoyl esterase activity screening for the production of a novel functional food product. Appl Environ Microbiol 74:1284–1288CrossRefGoogle Scholar
  29. Harhangi HR, Akhmanova A, Steenbakkers PJM, Jetten MSM, van de Drift C, Op den Camp HJM (2003) Genomic DNA analysis of genes encoding (hemi-)cellulolytic enzymes of the anaerobic fungus Piromyces sp. E2. Gene 314:73–80CrossRefGoogle Scholar
  30. Hermoso JA, Sanz-Aparicio J, Molina R, Juge N, Gonzalez R, Faulds CB (2004) The crystal structure of feruloyl esterase A from Aspergillus niger suggests evolutive functional convergence in feruloyl esterase family. J Mol Biol 338:494–506CrossRefGoogle Scholar
  31. Iiyama K, Lam TBT, Stone BA (1994) Covalent cross-links in the cell wall. Plant Physiol 104:315–320Google Scholar
  32. Ishii T (1991) Isolation and characterization of a diferuloyl arabinoxylan hexasaccharides from bamboo shoot cell-walls. Carbohydr Res 219:15–22CrossRefGoogle Scholar
  33. Ishii T (1997) Structure and functions of feruloylated polysaccharides. Plant Sci 127:111–127CrossRefGoogle Scholar
  34. Kamisaka S, Takeda S, Takahashi K, Shibuya K (1990) Diferulic and ferulic acid in the plant cell wall of Avena coleoptiles—their relationship to mechanical properties of the cell wall. Physiol Plant 78:1–7CrossRefGoogle Scholar
  35. Koseki T, Ito Y, Furuse S, Ito K, Iwano K (1996) Conversion of ferulic acid into 4-vinylguaiacol, vanillin and vanillic acid in model solutions of shochu. J Ferment Bioeng 82:46–50CrossRefGoogle Scholar
  36. Koseki T, Furuse S, Iwano K, Matsuzawa H (1998) Purification and characterization of a feruloyl esterase from Aspergillus awamori. Biosci Biotechnol Biochem 62:2032–2034CrossRefGoogle Scholar
  37. Koseki T, Takahashi K, Fushinobu S, Iefuji H, Iwano K, Hashizume K, Matsuzawa H (2005) Mutational analysis of a feruloyl esterase from Aspergillus awamori involved in substrate discrimination and pH dependence. Biochim Biophys Acta 1722:200–208Google Scholar
  38. Koseki T, Mimasaka N, Hashizume K, Shiono Y, Murayama T (2007) Stimulatory effect of ferulic acid on the production of extracellular xylanolytic enzymes by Aspergillus kawachii. Biosci Biotechnol Biochem 71:1785–1787CrossRefGoogle Scholar
  39. Koseki T, Hori A, Seki S, Murayama T, Shiono Y (2009) Characterization of two distinct feruloyl esterases, AoFaeB and AoFaeC, from Aspergillus oryzae. Appl Microbiol Biotechnol 83:689–696CrossRefGoogle Scholar
  40. Kroon PA, Faulds CB, Williamson G (1996) Purification and characterization of a novel esterase induced by growth of Aspergillus niger on sugar-beet pulp. Biotechnol Appl Biochem 23:255–262Google Scholar
  41. Kroon PA, Garcia-Conesa MT, Fillingham IJ, Hazlewood GP, Williamson G (1999) Release of ferulic acid dehydrogimers from plant cell walls by feruloyl esterases. J Sci Food Agric 79:428–434CrossRefGoogle Scholar
  42. Kroon PA, Williamson G, Fish NM, Archer DB, Belshaw NJ (2000) A modular esterase from Penicillium funiculosum which releases ferulic acid from plant cell walls and binds crystalline cellulose contains a carbohydrate binding module. Eur J Biochem 267:6740–6752CrossRefGoogle Scholar
  43. Lafay S, Gil-Izquierdo A, Manach C, Morand C, Besson C, Scalbert A (2006) Chlorogenic acid is absorbed in its intact form in the stomach of rats. J Nutr 136:1192–1197Google Scholar
  44. Lequart C, Nuzillard JM, Kurek B, Debeire P (1999) Hydrolysis of wheat bran and straw by an endoxylanase: production and structural characterization of cinnamoly-oligosaccharides. Carbohydr Res 319:102–111CrossRefGoogle Scholar
  45. Lesage-Meessen L, Delattre M, Haon M, Thibault JF, Ceccaldi BC, Brunerie P, Asther M (1996) A two-step bioconversion process for vanillin production from ferulic acid combining Aspergillus niger and Pycnoporus cinnabarinus. J Biotechnol 50:107–113CrossRefGoogle Scholar
  46. Levasseur A, Benoit I, Asther M, Asther M, Record E (2004a) Homologous expression of the feruloyl esterase B gene from Aspergillus niger and characterization of the recombinant enzyme. Protein Expr Purif 37:126–133CrossRefGoogle Scholar
  47. Levasseur A, Pagès S, Fierobe HP, Navarro D, Punt P, Belaïch JP, Asther M, Record E (2004b) Design and production in Aspergillus niger of a chimeric protein associating a fungal feruloyl esterase and a clostridial dockerin domain. Appl Environ Microbiol 70:6984–6991CrossRefGoogle Scholar
  48. Levasseur A, Navarro D, Punt PJ, Belaïch JP, Asther M, Record E (2005) Construction of engineered bifunctional enzymes and their overproduction in Aspergillus niger for improved enzymatic tools to degrade agricultural by-products. Appl Environ Microbiol 71:8132–8140CrossRefGoogle Scholar
  49. Levasseur A, Saloheimo M, Navarro D, Andberg M, Monot F, Nakari-Setälä T, Asther M, Record E (2006) Poduction of a chimeric enzyme tool associating the Trichoderma reesei swollenin with the Aspergillus niger feruloyl esterase A for release of ferulic acid. Appl Microbiol Biotechnol 73:872–880CrossRefGoogle Scholar
  50. MacAdam JW, Grabber JH (2002) Relationship of growth cessation with the formation of diferulate cross-links and p-coumaroylated lignins in tall fescue leaf blades. Planta 215:785–793CrossRefGoogle Scholar
  51. MacKenzie CR, Bilous D (1988) Ferulic acid esterase activity from Schizophyllum commune. Appl Environ Microbiol 54:1170–1173Google Scholar
  52. Mathew S, Abraham TE (2004) Ferulic acid: an antioxidant found naturally in plant cell walls and feruloyl esterases involved in its release and their applications. Crit Rev Biotechnol 24:59–83CrossRefGoogle Scholar
  53. McAuley K, Svendsen A, Patkar SA, Wilson KS (2004) Structure of a feruloyl esterase from Aspergillus niger. Acta Crystallogr D Biol Crystallogr 60:878–887CrossRefGoogle Scholar
  54. McCrae SI, Leith KM, Gordon AH, Wood TM (1994) Xylan-degrading enzyme system produced by the fungus Aspergillus awamori: isolation and characterization of a feruloyl esterase and a p-coumaroyl esterase. Enzyme Microbial Technol 16:826–834CrossRefGoogle Scholar
  55. Micard V, Renard CMGC, Colquhoun IJ, Thibault JF (1997a) End-products of enzymic saccharification of beet pulp, with a special attention to feruloylated oligosaccharides. Carbohydr Polym 32:283–292CrossRefGoogle Scholar
  56. Micard V, Grabber JH, Ralph J, Renard CMGC, Thibault JT (1997b) Dehydrodiferulic acids from sugar-beet pulp. Phytochemistry 44:1365–1368CrossRefGoogle Scholar
  57. Moukouli M, Topakas E, Christakopoulos P (2008) Cloning, characterization and functional expression of an alkalitorelant type C feruloyl esterase from Fusarium oxysporum. Appl Microbiol Biotechnol 79:245–254CrossRefGoogle Scholar
  58. Mueller-Harvey I, Hartley RD, Harris J, Curzon EH (1986) Linkage of p-coumaroyl feruloyl groups to cell-wall polysaccharides of barley straw. Carbohydr Res 148:71–85CrossRefGoogle Scholar
  59. Nardini M, Dijkstra BW (1999) α/β Hydrolase fold enzymes: the family keeps growing. Curr Opin Struct Biol 9:732–737CrossRefGoogle Scholar
  60. Oddou J, Stentelaire C, Lesage-Meesen L, Asther M, Ceccaldi BC (1999) Improvement of ferulic acid bioconversion into vanillin by use of high-density cultures of Pycnoporus cinnabarinus. Appl Microbiol Biotechnol 53:1–6CrossRefGoogle Scholar
  61. Prates JAM, Tarbouriech N, Charnock SJ, Fontes CMGA, Ferreira LMA, Davies GJ (2001) The structure of the feruloyl esterase module of xylanase 10B from Clostridium thermocellum provides insights into substrate recognition. Structure 9:1183–1190CrossRefGoogle Scholar
  62. Puchart V, Vršanská M, Mastihubová M, Topakas E, Vafiadi C, Faulds CB, Tenkanen M, Christakopoulos P, Biely P (2007) Substrate and positional specificity of feruloyl esterases for monoferuloylated and monoacetylated 4-nitrophenyl glycoside. J. Biotechnol 127:235–243CrossRefGoogle Scholar
  63. Record E, Asther M, Sigoillot C, Pagès S, Punt PJ, Delattre M, Haon M, van den Hondel CAMJJ, Sigoillot J-C, Lesage-Meessen L, Asther M (2003) Overproduction of the Aspergillus niger feruloyl esterase for pulp bleaching application. Appl Microbiol Biotechnol 62:349–355CrossRefGoogle Scholar
  64. Rumbold K, Biely P, Mastihubova M, Gudelj M, Guebitz G, Robra KH, Prior BA (2003) Purifiction and properties of a feruloyl esterase involved in lignocellulose degradation by Aureobasidium pullulans. Appl Environ Microbiol 69:5622–5626CrossRefGoogle Scholar
  65. Sakamoto T, Nishimura S, Kato T, Sunagawa Y, Tsuchiyama M, Kawasaki H (2005) Efficient extraction of ferulic acid from sugar beet pulp using the culture supernatant of Penicillium chrysogenum. J Appl Glycosci 52:115–120Google Scholar
  66. Saulnier L, Thibault JF (1999) Ferulic acid and diferulic acid as components of sugar-beet pectins and maize bran heteroxylans. J Sci Food Agric 79:396–402CrossRefGoogle Scholar
  67. Schubot FD, Kataeva IA, Blum DL, Shah AK, Ljunggahl LG, Rose JP, Wang BC (2001) Structural basis for the substrate specificity of the feruloyl esterase domain of the cellulosomal xylanase Z from Clostridium thermocellum. Biochemistry 40:12524–12532CrossRefGoogle Scholar
  68. Shibuya N (1984) Phenolic acids and their carbohydrate esters in rice endosperm cell walls. Phytochemistry 23:2233–2237CrossRefGoogle Scholar
  69. Shin HD, Chen RR (2007) A type B feruloyl esterase from Aspergillus nidulans with broad pH applicability. Appl Microbiol Biotechnol 73:1323–1330CrossRefGoogle Scholar
  70. Sigoillot C, Camarero S, Vidal T, Record E, Asther M, Pèrez-Boada M, Martínez MJ, Sigoillot J-C, Asther M, Colom JF, Martínez ÁT (2005) Comparison of different fungal enzymes for bleaching high-quality paper pulps. J Biotechnol 115:333–343CrossRefGoogle Scholar
  71. Smith MM, Hartley RD (1983) Occurrence and nature of ferulic acid substitution of cell-wall polysaccharides in graminaceous plants. Carbohydr Res 118:65–80CrossRefGoogle Scholar
  72. Suzuki A, Kagawa D, Fujii A, Ochiai R, Tokimitsu I, Saito I (2002) Short and long term effect of ferulic acid on blood pressure in spontaneously hypertensive rats. Am J Hypertens 15:351–357CrossRefGoogle Scholar
  73. Tenkanen M, Schuseil J, Puls J, Poutanen K (1991) Production, purification and characterization of an esterase liberating phenolic acids from lignocellulosics. J Biotechnol 18:69–84CrossRefGoogle Scholar
  74. Topakas E, Kalogeris E, Ketos D, Macris BJ, Christakopoulos P (2003a) Pruduction and partial characterization of a feruloyl esterase by Sporotrichum thermophile under solid-state fermentation. Proc Biochem 38:1539–1543CrossRefGoogle Scholar
  75. Topakas E, Stamatis H, Mastihubova M, Biely P, Ketos D, Macris BJ, Christakopoulos P (2003b) Purification and characterization of a Fusarium oxysporum feruloyl esterase (FoFAE-I) catalyzing transesterification of phenolic acid esters. Enzyme Microb Technol 33:729–737CrossRefGoogle Scholar
  76. Topakas E, Stamatis H, Biely P, Ketos D, Macris BJ, Christakopoulos P (2003c) Purification and characterization of a feruloyl esterase from Fusarium oxysporum catalyzing esterification of phenolic acids in ternary water-organic solvent mixture. J Biotechnol 102:33–44CrossRefGoogle Scholar
  77. Topakas E, Stamatis H, Biely P, Christakopoulos P (2004) Purification and characterization of a type B feruloyl esterase (StFAE-A) from the thermophilic fungus Sporotrichum thermophile. Appl Microbiol Biotechnol 63:686–690CrossRefGoogle Scholar
  78. Topakas E, Vafiadi C, Stamatis H, Christakopoulos P (2005) Sporotricum thermophile type C feruloyl esterase (StFaeC): purification, characterization, and its use for phenolic acid (sugar) ester synthesis. Enzyme Microb Technol 36:729–736CrossRefGoogle Scholar
  79. Topakas E, Vafiadi C, Christakopoulos P (2007) Microbial production, characterization and applications of feruloyl esterases. Process Biochem 42:497–509CrossRefGoogle Scholar
  80. Tsuchiyama M, Sakamoto T, Tanimori S, Murata S, Kawasaki H (2007) Enzymatic synthesis of hydroxycinnamic acid glycerol esters using type A feruloyl esterase from Aspergillus niger. Biosci Biotechnol Biochem 71:2606–2609CrossRefGoogle Scholar
  81. van Peiji NN, Visser J, de Graaff LH (1998a) Isolation and analysis of xlnR, encoding a transcriptional activator co-ordinating xylanolytic expression in Aspergillus niger. Mol Microbiol 27:131–142CrossRefGoogle Scholar
  82. van Peiji NN, Gielkens MM, de Vries RP, Visser J, de Graaff LH (1998b) The transcriptional activator XlnR regulates both xylanolytic and endoglucanase gene expression in Aspergillus niger. Appl Environ Microbiol 64:3615–3619Google Scholar
  83. Williamson G, Kroon PA, Faulds CB (1998) Hairy plant polysaccharides: a close shave with microbial esterases. Microbiology 144:2011–2023CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Takuya Koseki
    • 1
    Email author
  • Shinya Fushinobu
    • 2
  • Ardiansyah
    • 3
  • Hitoshi Shirakawa
    • 3
  • Michio Komai
    • 3
  1. 1.Department of Bioresource Engineering, Faculty of AgricultureYamagata UniversityTsuruokaJapan
  2. 2.Department of BiotechnologyThe University of TokyoTokyoJapan
  3. 3.Department of Science of Food Function and Health, Graduate School of Agricultural ScienceTohoku UniversitySendaiJapan

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