Advertisement

Biotechnology Letters

, Volume 30, Issue 3, pp 387–396 | Cite as

Biotechnological applications and potential of fungal feruloyl esterases based on prevalence, classification and biochemical diversity

  • Isabelle Benoit
  • Etienne G. J. Danchin
  • Robert-Jan Bleichrodt
  • Ronald P. de Vries
Review

Abstract

Feruloyl esterases are part of the enzymatic spectrum employed by fungi and other microorganisms to degrade plant polysaccharides. They release ferulic acid and other aromatic acids from these polymeric structures and have received an increasing interest in industrial applications such as in the food, pulp and paper and bio-fuel industries. This review provides an overview of the current knowledge on fungal feruloyl esterases focussing in particular on the differences in substrate specificity, regulation of their production, prevalence of these enzymes in fungal genomes and industrial applications.

Keywords

Applications Feruloyl esterases Fungi Phylogeny Substrate specificity 

Notes

Acknowledgements

R.P. de Vries was supported by The Netherlands Technology Foundation (STW) VIDI project UGC.7063.

References

  1. Bach Tuyet Lam T, Iiyama K, Stone BA (1992) Cinnamic acid bridges between cell wall polymers in wheat and phalaris internodes. Phytochemistry 31:1179–1183CrossRefGoogle Scholar
  2. Bajpai P (1999) Application of enzymes in the pulp and paper industry. Biotechnol Prog 15:147–157PubMedCrossRefGoogle Scholar
  3. Benoit I, Navarro D, Marnet N et al (2006) Feruloyl esterases as a tool for the release of phenolic compounds from agro-industrial by-products. Carbohydr Res 341:1820–1827PubMedCrossRefGoogle Scholar
  4. Blum DL, Kataeva IA, Li XL et al (2000) Feruloyl esterase activity of the clostridium thermocellum cellulosome can be attributed to previously unknown domains of xyny and xynz. J Bacteriol 182:1346–1351PubMedCrossRefGoogle Scholar
  5. Bonnin E, Grange H, Lesage-Meessen L et al (2000) Enzymic release of cellobiose from sugar beet pulp, and its use to favour vanillin production in pycnoporus cinnabarinus from vanillic acid. Carbohydr Polym 41:143–151CrossRefGoogle Scholar
  6. Borneman WS, Ljungdahl LG, Hartley RD et al (1991) Isolation and partial characterization of p-coumaroyl esterase from the anaerobic fungus neocallimastix strain mc-2. Appl Environ Microbiol 57:2337–2344PubMedGoogle Scholar
  7. Borneman WS, Ljungdahl LG, Hartley RD et al (1992) Purification and partial characterization of two feruloyl esterases from the anaerobic fungus Neocallimastix strain mc-2. Appl Environ Microbiol 58:3762–3766PubMedGoogle Scholar
  8. Chen JH, Ho C-T (1997) Antioxidant activities of caffeic acid and its related hydroxycinnamic acid compounds. J Agric Food Chem 45:2374–2378CrossRefGoogle Scholar
  9. Crepin VF, Faulds CB, Connerton IF (2003a) A non-modular type b feruloyl esterase from neurospora crassa exhibits concentration-dependent substrate inhibition. Biochem J 370:417–427PubMedCrossRefGoogle Scholar
  10. 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 Purif 29:176–184PubMedGoogle Scholar
  11. Crepin VF, Faulds CB, Connerton IF (2004a) Functional classification of the microbial feruloyl esterases. Appl Microbiol Biotechnol 63:647–652PubMedCrossRefGoogle Scholar
  12. Crepin VF, Faulds CB, Connerton IF (2004b) Identification of a type-d feruloyl esterase from Neurospora crassa. Appl Microbiol Biotechnol 63:567–570PubMedCrossRefGoogle Scholar
  13. de Groot MJL, van de Vondervoort PJI, de Vries RP et al (2003) Isolation and characterization of two specific regulatory Aspergillus niger mutants shows antagonistic regulation of arabinan and xylan metabolism. Microbiology 149:1183–1191PubMedCrossRefGoogle Scholar
  14. de Vries RP, Michelsen B, Poulsen CH et al (1997) The faea genes from Aspergillus niger and Aspergillus tubingensis encode ferulic acid esterases involved in the degradation of complex cell wall polysaccharides. Appl Environ Microbiol 63:4638–4644PubMedGoogle Scholar
  15. de Vries RP, Visser J (1999) Regulation of the feruloyl esterase (faea) gene from Aspergillus niger. Appl Environ Microbiol 65:5500–5503PubMedGoogle Scholar
  16. de Vries RP, Kester HCM, vanKuyk PA et al (2002) The Aspergillus niger faeb gene encodes a second feruloyl esterase involved in pectin and xylan degradation, and is specifically induced on aromatic compounds. Biochem J 363:377–386PubMedCrossRefGoogle Scholar
  17. Desper R, Gascuel O (2002) Fast and accurate phylogeny reconstruction algorithms based on the minimum-evolution principle. J Comput Biol 9:687–705PubMedCrossRefGoogle Scholar
  18. Donaghy J, McKay AM (1997) Purification and characterisation of a feruloyl esterase from the fungus Penicillium expansum. J Appl Microbiol 83:718–726PubMedCrossRefGoogle Scholar
  19. Donaghy JA, McKay AM (1995) Production of feruloyl/rho-coumaroyl esterase activity by Penicillium expansum, Penicillium brevicompactum and Aspergillus niger. J Appl Bacteriol 79:657–662PubMedGoogle Scholar
  20. Edgar RC (2004a) Muscle: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113PubMedCrossRefGoogle Scholar
  21. Edgar RC (2004b) Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedCrossRefGoogle Scholar
  22. 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 17:349–359PubMedGoogle Scholar
  23. 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
  24. Faulds CB, de Vries RP, Kroon PA et al (1997) Influence of ferulic acid on the production of feruloyl esterases by Aspergillus niger. FEMS Microbiol Lett 157:239–244PubMedCrossRefGoogle Scholar
  25. Felsenstein J (1989) Phylip—phylogeny inference package (version 3.2). Cladistics 5:164–166Google Scholar
  26. Fillingham IJ, Kroon PA, Williamson G et al (1999) A modular cinnamoyl ester hydrolase from the anaerobic fungus piromyces equi acts synergistically with xylanase and is part of a multiprotein cellulose-binding cellulase-hemicellulase complex. Biochem J 343:215–224PubMedCrossRefGoogle Scholar
  27. Galtier N, Gouy M, Gautier C (1996) Seaview and phylo_win: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548PubMedGoogle Scholar
  28. Garcia-Conesa MT, Crepin VF, Goldson AJ et al (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 108:227–241PubMedCrossRefGoogle Scholar
  29. 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
  30. Grabber JH, Ralph J, Hatfield RD (2000) Cross-linking of maize walls by ferulate dimerization and incorporation into lignin. J Agric Food Chem 48:6106–6113PubMedCrossRefGoogle Scholar
  31. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  32. Harhangi HR, Akhmanova A, Steenbakkers PJ et al (2003) Genomic DNA analysis of genes encoding (hemi-)cellulolytic enzymes of the anaerobic fungus piromyces sp. E2. Gene 314:73–80PubMedCrossRefGoogle Scholar
  33. Ishii T (1991) Isolation and characterization of a diferuloyl arabinoxylan hexasaccharide from bamboo shoot cell-walls. Carbohydr Res 219:15–22PubMedCrossRefGoogle Scholar
  34. Kantelinen A, Ratto M, Sundquist J et al (1988) Hemicelluloses and their potential role in bleaching. In International pulp bleaching conference, pp 1–9Google Scholar
  35. Kikuzaki H, Hisamoto M, Hirose K et al (2002) Antioxidant properties of ferulic acid and its related compounds. J Agric Food Chem 50:2161–2168PubMedCrossRefGoogle Scholar
  36. Klinke HB, Ahring BK, Schmidt AS et al (2002) Characterization of degradation products from alkaline wet oxidation of wheat straw. Bioresour Technol 82:15–26PubMedCrossRefGoogle Scholar
  37. Koseki T, Furuse S, Iwano K et al (1998) Purification and characterization of a feruloylesterase from Aspergillus awamori. Biosci Biotechnol Biochem 62:2032–2034PubMedCrossRefGoogle Scholar
  38. Koseki T, Takahashi K, Fushinobu S et al (2005) Mutational analysis of a feruloyl esterase from Aspergillus awamori involved in substrate discrimination and pH dependence. Biochim Biophys Acta 1722:200–208PubMedGoogle Scholar
  39. Kroon PA, Faulds CB, Williamson G (1996) Purification and characterisation of a novel esterase induced by growth of Aspergillus niger on sugar-beet pulp. Biotechnol Appl Biochem 23:255–262PubMedGoogle Scholar
  40. Kroon PA, Faulds CB, Brezillon C et al (1997) Methyl phenylalkanoates as substrates to probe the active sites of esterases. Eur J Biochem 248:245–251PubMedCrossRefGoogle Scholar
  41. Kroon PA, Wiliamson G (1999) Hydroxycinnamates in plants and food: Current and future perspectives. J Sci Food Agric 79:355–361CrossRefGoogle Scholar
  42. Kroon PA, Williamson G, Fish NM et al (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 267:6740–6752PubMedCrossRefGoogle Scholar
  43. Lesage-Meessen L, Lomascolo A, Bonnin E et al (2002) A biotechnological process involving filamentous fungi to produce natural crystalline vanillin from maize bran. Appl Biochem Biotechnol 102–103:141–153PubMedCrossRefGoogle Scholar
  44. 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 215:785–793PubMedCrossRefGoogle Scholar
  45. Maillard MN, Berset C (1995) Evolution of antioxidant activity during kilning: Role of insoluble bound phenolic acids of barley and malt. J Agric Food Chem 43:1789–1793CrossRefGoogle Scholar
  46. Mayer AM, Staples RC (2002) Laccase: new functions for an old enzyme. Phytochemistry 60:551–565PubMedCrossRefGoogle Scholar
  47. McCrae SI, Leith KM, Gordon AH et al (1994) Xylan degrading enzyme system produced by the fungus Aspergillus awamori: isolation and characterization of a feruloyl esterase and a p-coumaroyl esterase. Enzyme Microbiol Technol 16:826–834CrossRefGoogle Scholar
  48. Milstein O, Vered Y, Shragina L et al (1983) Metabolism of lignin related aromatic compounds by Aspergillus japonicus. Arch Microbiol 135:147–154CrossRefGoogle Scholar
  49. Murakami A, Nakamura Y, Koshimizu K et al (2002) Fa15, a hydrophobic derivative of ferulic acid, suppresses inflammatory responses and skin tumor promotion: comparison with ferulic acid. Cancer Lett 180:121–129PubMedCrossRefGoogle Scholar
  50. Pel HJ, de Winde JH, Archer DB et al (2007) Genome sequence of Aspergillus niger strain cbs 513.88: a versatile cell factory. Nat Biotechnol 25:221–231PubMedCrossRefGoogle Scholar
  51. Peleg H, Naim M, Zehavi U et al (1992) Pathways of 4-vinylguaiacol formation from ferulic acid in model solutions of orange juice. J Agric Food Chem 40Google Scholar
  52. Ralet M-C, Faulds CB, Williamson G et al (1994) Degradation of feruloylated oligosaccharides from sugar beet pulp and wheat bran by ferulic acid esterases from Aspergillus niger. Carbohydr Res 263:257–269PubMedCrossRefGoogle Scholar
  53. Ralph J, Grabber JH, Hatfield RD (1995) Lignin-ferulate crosslinks in grasses: active incorporation of ferulate polysaccharide esters into ryegrass lignins. Carbohydr Res 275:167–178Google Scholar
  54. Record E, Asther M, Sigoillot C et al (2003) Overproduction of the Aspergillus niger feruloyl esterase for pulp bleaching application. Appl Microbiol Biotechnol 62:349–355PubMedCrossRefGoogle Scholar
  55. Rumbold K, Biely P, Mastihubova M et al (2003) Purification and properties of a feruloyl esterase involved in lignocellulose degradation by aureobasidium pullulans. Appl Environ Microbiol 69:5622–5626PubMedCrossRefGoogle Scholar
  56. Shin HD, Chen RR (2007) A type b feruloyl esterase from Aspergillus nidulans with broad pH applicability. Appl Microbiol Biotechnol 73:1323–1330PubMedCrossRefGoogle Scholar
  57. Sigoillot C, Camarero S, Vidal T et al (2005) Comparison of different fungal enzymes for bleaching high-quality paper pulps. J Biotechnol 115:333–343PubMedCrossRefGoogle Scholar
  58. Tabka MG, Herpoël-Gimberta I, Monod F et al (2006) Enzymatic saccharification of wheat straw for bioethanol production by a combined cellulase xylanase and feruloyl esterase treatment. Enzyme Microbiol Technol 39:897–902CrossRefGoogle Scholar
  59. Tapin S, Sigoillot J-C, Asther M et al (2006) Feruloyl esterase utilization for simultaneous processing of nonwood plants into phenolic compounds and pulp fibers. J Agric Food Chem 54:3697–3703CrossRefPubMedGoogle Scholar
  60. Tenkanen M, Schuseil J, Puls J et al (1991) Production, purification and characterisation of an esterase liberating phenolic acids from lignocellulosics. J Biotechnol 18:69–84CrossRefGoogle Scholar
  61. Topakas E, Stamatis H, Biely P et al (2003) Purification and characterization of a feruloyl esterase from fusarium oxysporum catalyzing esterification of phenolic acids in ternary water–organic solvent mixtures. J Biotechnol 102:33–44PubMedCrossRefGoogle Scholar
  62. Topakas E, Stamatis H, Biely P et al (2004) Purification and characterization of a type b feruloyl esterase (stfae-a) from the thermophilic fungus sporotrichum thermophile. Appl Microbiol Biotechnol 63:686–690PubMedCrossRefGoogle Scholar
  63. Vailhe MA, Provan GJ, Scobbie L et al (2000) Effect of phenolic structures on the degradability of cell walls isolated from newly extended apical internode of tall fescue (Festuca arundinacea schreb.). J Agric Food Chem 48:618–623PubMedCrossRefGoogle Scholar
  64. van Gorcom RFM, Boschloo JG, Kuijvenhoven A et al (1990) Isolation and molecular characterisation of the benzoate-para-hydroxylase gene (bpha) of Aspergillus niger: a member of a new gene family of the cytochrome p450 superfamily. Mol Gen Genet 233:192–197Google Scholar
  65. van Peij N, Gielkens MMC, de Vries RP et al (1998a) The transcriptional activator xlnr regulates both xylanolytic and endoglucanase gene expression in Aspergillus niger. Appl Environ Microbiol 64:3615–3619PubMedGoogle Scholar
  66. van Peij NNME, Visser J, de Graaff LH (1998b) Isolation and analysis of xlnr, encoding a transcriptional activator coordinating xylanolytic expression in Aspergillus niger. Mol Microbiol 27:131–142PubMedCrossRefGoogle Scholar
  67. Zheng L, Zheng P, Sun Z et al (2007) Production of vanillin from waste residue of rice bran oil by Aspergillus niger and Pycnoporus cinnabarinus. Bioresour Technol 98:1115–1119PubMedCrossRefGoogle Scholar
  68. Zmasek CM, Eddy SR (2001) Atv: display and manipulation of annotated phylogenetic trees. Bioinformatics 17:383–384PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Isabelle Benoit
    • 1
  • Etienne G. J. Danchin
    • 2
    • 4
  • Robert-Jan Bleichrodt
    • 3
  • Ronald P. de Vries
    • 3
  1. 1.Unité Génie Microbiologique et Enzymatique, SupAgro-INRAMontpellierFrance
  2. 2.Architecture et Fonction des Macromolecules Biologiques, UMR6098 CNRSUniversites Aix-Marseille I & IIMarseille cedex 9France
  3. 3.Microbiology, Science FacultyUtrecht UniversityUtrechtThe Netherlands
  4. 4.UMR INRA-CNRS-UNSASophia Antipolis CedexFrance

Personalised recommendations