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Cloning of a novel feruloyl esterase gene from rumen microbial metagenome and enzyme characterization in synergism with endoxylanases

  • Dominic W. S. WongEmail author
  • Victor J. Chan
  • Hans Liao
  • Mary J. Zidwick
Biocatalysis

Abstract

A feruloyl esterase (FAE) gene was isolated from a rumen microbial metagenome, cloned into E. coli, and expressed in active form. The enzyme (RuFae2) was identified as a type C feruloyl esterase. The RuFae2 alone released ferulic acid from rice bran, wheat bran, wheat-insoluble arabinoxylan, corn fiber, switchgrass, and corn bran in the order of decreasing activity. Using a saturating amount of RuFae2 for 100 mg substrate, a maximum of 18.7 and 80.0 μg FA was released from 100 mg corn fiber and wheat-insoluble arabinoxylan, respectively. Addition of GH10 endoxylanase (EX) synergistically increased the release of FA with the highest level of 6.7-fold for wheat bran. The synergistic effect of adding GH11 EX was significantly smaller with all the substrates tested. The difference in the effect of the two EXs was further analyzed by comparing the rate in the release of FA with increasing EX concentration using wheat-insoluble arabinoxylan as the substrate.

Keywords

Feruloyl esterase Ferulic acid esterase Ferulic acid Metagenomics Corn fiber Arabinoxylan 

Notes

Acknowledgments

Reference to a company and/or products is only for purposes of information and does not imply approval of recommendation of the product to the exclusion of others that may also be suitable. All programs and services of the U.S. Department of Agriculture are offered on a nondiscriminatory basis without regard to race, color, national origin, religion, sex, age, marital status, or handicap.

References

  1. 1.
    Akin DE (2007) Grass lignocellulose. Appl Biochem Biotechnol 136–140:3–15CrossRefGoogle Scholar
  2. 2.
    Akin DE (2008) Plant cell wall aromatics: influence on degradation of biomass. Biofuels Bioprod Bioref 2:303–386CrossRefGoogle Scholar
  3. 3.
    Akin DE, Morrison WH, Rigsby LL, Barton FE, Himmelsbach DS, Hicks KB (2006) Corn stover fractions and bioenergy. Appl Biochem Biotechnol 129–132:104–116PubMedCrossRefGoogle Scholar
  4. 4.
    Arnold K, Bordoli L, Kopp J, Schwede T (2006) The Swiss-model workspace: a web-based environment for protein structure homology modeling. Bioinformatics 22:195–201PubMedCrossRefGoogle Scholar
  5. 5.
    Barone E, Calabrese V, Mancuso C (2009) Ferulic acid and its therapeutic potential as a hormetin for aged-related diseases. Biogerontology 10:97–108PubMedCrossRefGoogle Scholar
  6. 6.
    Benoit I, Danchin EGJ, Blelchrodt R-J, de Vries RP (2008) Biotechnological applications and potential of fungal feruloyl esterases based on prevalence, classification and biochemical diversity. Biochemi Lett 30:387–396Google Scholar
  7. 7.
    Biely P, Vrsanska M, Tenkanen M, Kluepfel D (1997) Endo-β-1,4-xylanase families: differences in catalytic properties. J Biotechnol 57:151–166PubMedCrossRefGoogle Scholar
  8. 8.
    de Buanafina MMO (2009) Feruloylation in grasses: current and future perspectives. Mol Plant 2:861–872CrossRefGoogle Scholar
  9. 9.
    Courtin CM, Delcour JA (2001) Relative activity of endoxylanases towards water-extractable and water-unextractable arabinoxylan. J Cereal Sci 33:301–312CrossRefGoogle Scholar
  10. 10.
    Crepin VF, Faulds CB, Connerton IF (2004) Functional classification of the microbial feruloyl esterases. Appl Microbiol Biotechnol 63:647–652PubMedCrossRefGoogle Scholar
  11. 11.
    De Vries RP, Kester HCM, Poulsen CH, Benen JAE, Visser J (2000) Synergy between enzymes from Aspergillus involved in the degradation of plant cell wall polysaccharides. Carbohydr Res 327:401–410PubMedCrossRefGoogle Scholar
  12. 12.
    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
  13. 13.
    Faulds CB, Williamson G (1995) Release of ferulic acid from wheat bran by a ferulic acid esterase (FAE-III) from Aspergillus niger. Appl Microbiol Biotechnol 43:1082–1087PubMedCrossRefGoogle Scholar
  14. 14.
    Faulds CB, Mandaian G, Curto RBL, Bisignano G, Waldron KW (2006) Influence of the arabinoxylan composition on the susceptibility of mono- and dimeric ferulic acid release by Humicola insolens feruloyl esterases. J Sci Food Agric 86:1623–1630CrossRefGoogle Scholar
  15. 15.
    Fujimoto Z, Kaneko S, Kuno A, Kobayashi H, Kusakabe I, Mizuno H (2004) Crystal structures of decorated xylooligosaccharides bound to a family 10 xylanase from Streptomyces olivaceoviridis E-86. J Biol Chem 279:9606–9614PubMedCrossRefGoogle Scholar
  16. 16.
    Goldstone DC, Villas-Boas SG, Till M, Kelly WJ, Attwood GT, Arcus VL (2010) Structural and functional characterization of a promiscuous feruloyl esterasee [Est1E] from the rumen bacterium Butyrivibrio proteoclasticus. Proteins 78:1457–1469PubMedGoogle Scholar
  17. 17.
    Grohmann K, Mitchell DJ, Himmel ME, Dale BE, Schroeder HA (1989) The role of ester groups in resistance of plant cell wall polysaccharides to enzymatic hydrolysis. Appl Biochem Biotechnol 20:45–61CrossRefGoogle Scholar
  18. 18.
    Harris PJ, Trethewey JAK (2010) The distribution of ester-linked ferulic acid in the cell walls of angiosperms. Phytochem Rev 9:19–33CrossRefGoogle Scholar
  19. 19.
    Hartley RD, Ford CW (1989) Phenolic constituents of plant cell walls and wall biodegradability. In: Lewis NG, Paice MG (eds) Plant cell wall polymers: biogenesis and bioegradation. American Chemical Society, Washington, DC, pp 137–145CrossRefGoogle Scholar
  20. 20.
    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 338:495–506PubMedCrossRefGoogle Scholar
  21. 21.
    Kroon PA, Williamson G (1996) Release of ferulic acid from sugar-beet pulp by using arabinanase, arabinofuranosidase and an esterase from Aspergillus niger. Biotechnol Appl Biochem 23:263–267PubMedGoogle Scholar
  22. 22.
    Lai K–K, Stogios PJ, Vu C, Xu X, Cui H, Molloy S, Savchenko A, Yakunin A, Gonzalez CF (2011) An inserted α/β subdomain shapes the catalytic pocket of Lactobacillus johnsonii cinnamoyl esterase. PLoS ONE 6:e23269PubMedCrossRefGoogle Scholar
  23. 23.
    Mosier N, Wyman C, Dale B, Elander R, Lee YY, Holtzapple M, Ladisch M (2005) Features of promising technologies for pretreatment of lignocellulosic biomass. Bioresource Technol 96:673–686CrossRefGoogle Scholar
  24. 24.
  25. 25.
    Pell G, Taylor EJ, Gloster TM, Turkenburg JP, Fontes CM, Ferreira LM, Nagy T, Clark SJ, Davies GJ, Gilbert HJ (2004) The mechanism by which family 10 glycoside hydrolases bind decorated substrates. J Biol Chem 279:393–9597Google Scholar
  26. 26.
    Rouau X, Cheynier V, Surget A, Gloux D, Barron C, Meudec E, Louis-Montero J, Criton M (2003) A dehydrotrimer of ferulic acid from maize bran. Phytochem 63:899–903CrossRefGoogle Scholar
  27. 27.
    Topakas E, Vafiadi C, Christakopoulos P (2007) Microbial production, characterization and applications of feruloyl esterases. Process Biochem 42:497–509CrossRefGoogle Scholar
  28. 28.
    Vandermarliere E, Bourgois TM, Rombouts S, Van Campenhout S, Wolckaert G, Strelkov SV, Delcour JA, Rabijns A, Courtin CM (2008) Crystallographic analysis shows substrate binding at the −3 to +1 active-site subsites and at the surface of glycoside hydrolase family 11 endo-1,4-beta xylanases. Biochem J 410:71–79PubMedCrossRefGoogle Scholar
  29. 29.
    Vardakou M, Katapodis P, Topakas E, Kekos D, Macris BJ, Christakopoulos P (2004) Synergy between enzymes involved in the degradation of insoluble wheat flour arabinoxylan. Innovative Food Sci Emerging Technol 5:107–112CrossRefGoogle Scholar
  30. 30.
    Wong DWS (2006) Feruloyl esterase—a key enzyme in biomass degradation. Appl Biochem Biotechnol 133:87–112PubMedCrossRefGoogle Scholar
  31. 31.
    Wong DWS (2010) Application of metagenomics for industrial bioproducts. In: Marco D (ed) Metagenomics theory methods and applications. Caister Academic Press, Norfolk, UK, pp 141–158Google Scholar
  32. 32.
    Wong DWS, Chan VJ, Batt SB, Gautam S, Liao H (2011) Engineering Saccharomyces cerevisiae to produce feruloyl esterase for the release of ferulic acid from switchgrass. J Ind Microbiol Biotechnol 38:1961–1967PubMedCrossRefGoogle Scholar
  33. 33.
    Wong DWS, Chan VJ, McCormack AA (2009) Functional cloning and expression of a novel endo-α-1,5-l-arabinanase from a metagenomic library. Peptide Protein Lett 16:1435–1441CrossRefGoogle Scholar
  34. 34.
    Wong DWS, Chan VJ, McCormack AA, Batt SB (2008) Cloning and characterization of a novel exo-α-1,5-L-arabinanase gene and the enzyme. Appl Microbiol Biotechnol 79:941–949PubMedCrossRefGoogle Scholar
  35. 35.
    Wong DWS, Chan VJ, McCormack AA, Batt SB (2010) A novel xyloglucan-specific endo-β-1,4-glucanase: biochemical properties and inhibition studies. Appl Microbiol Biotechnol 86:1463–1471PubMedCrossRefGoogle Scholar
  36. 36.
    Wong DWS, Chan VJ, McCormack AA, Batt SB (2010) Cloning and characterization of an exo-xyloglucanase from rumenal microbial metagenome. Protein Peptide Lett 17:803–808CrossRefGoogle Scholar

Copyright information

© Springer-Verlag (outside the USA) 2013

Authors and Affiliations

  • Dominic W. S. Wong
    • 1
    Email author
  • Victor J. Chan
    • 1
  • Hans Liao
    • 2
  • Mary J. Zidwick
    • 3
  1. 1.Western Regional Research CenterUSDA-ARSAlbanyUSA
  2. 2.OPX BiotechnologiesBoulderUSA
  3. 3.Cargill Biotechnology Development CenterExcelsiorUSA

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