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Archives of Microbiology

, 191:133 | Cite as

Two glucuronoyl esterases of Phanerochaete chrysosporium

  • Miroslava Ďuranová
  • Silvia Špániková
  • Han A. B. Wösten
  • Peter BielyEmail author
  • Ronald P. de VriesEmail author
Original Paper

Abstract

The white-rot fungus Phanerochaete chrysosporium produces glucuronoyl esterase, a recently discovered carbohydrate esterase, during growth on sugar beet pulp. Two putative genes encoding this enzyme, ge1 and ge2, were isolated and cloned. Heterologous expression in Aspergillus vadensis, Pycnoporus cinnabarinus and Schizophyllum commune resulted in extracellular glucuronoyl esterase activity, demonstrating that these genes encode this enzymatic function. The amino acid sequence of GE1 was used to identify homologous genes in the genomes of twenty-four fungi. Approximately half of the genomes, both from ascomycetes and basidiomycetes, contained putative orthologues, but their presence could not be assigned to any of fungal class or subclass. Comparison of the amino acid sequences of identified and putative glucuronoyl esterases to other types of carbohydrate esterases (CE) confirmed that they form a separate family of CEs. These enzymes are interesting candidates for biotechnological applications such as the separation of lignin and hemicellulose.

Keywords

Glucuronoyl esterase Phanerochaete chrysosporium Lignin-carbohydrate complex 

Notes

Acknowledgments

The authors thank Dr. J. Hirsch (the Institute of Chemistry, Slovak Academy of Sciences, Slovakia) for the glucuronoyl esterase substrates, Dr. A. Alves (Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, The Netherlands) for help with the P. cinnabarinus transformation and Dr. L. G. Lugones (Microbiology, Utrecht University, The Netherlands) for help with the S. commune transformation. This work was supported by a grant from the Slovak Research and Development Agency under the Contract No. APVV-51-003805.

References

  1. Alves AMCR, Record E, Lomascolo A, Scholtmeijer K, Asther M, Wessels JGH, Wösten HAB (2004) Highly efficient production of laccase in the basidiomycete Pycnoporus cinnabarinus. Appl Environ Microbiol 70:6379–6384PubMedCrossRefGoogle Scholar
  2. Aro N, Pakula T, Penttilä M (2005) Transcriptional regulation of plant cell wall degradation by filamentous fungi. FEMS Microbiol Rev 29:719–739PubMedCrossRefGoogle Scholar
  3. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795PubMedCrossRefGoogle Scholar
  4. Black GW, Rixon JE, Clarke JH, Hazlewood GP, Theodorou MK, Morris P, Gilbert HJ (1996) Evidence that linker sequences and cellulose-binding domains enhance the activity of hemicellulases against complex substrates. Biochem J 319:515–520PubMedGoogle Scholar
  5. Bounias M (1980) N-(1-naphthyl)ethylenediamine dihydrochloride as a new reagent for nanomole quantification of sugars on thin-layer plates by a mathematical calibration process. Anal Biochem 106:291–295PubMedCrossRefGoogle Scholar
  6. Das NN, Das SC, Mukherjee AK (1984a) On the ester linkage between lignin and 4-O-methyl-d-glucurono-d-xylan in jute fiber (Corchorus capsularis). Carbohydr Res 127:345–348CrossRefGoogle Scholar
  7. Das NN, Das SC, Sarkar AK, Mukherjee AK (1984b) Lignin-xylan ester linkage in mesta fiber (Hibiscus cannabinus). Carbohydr Res 129:197–207CrossRefGoogle Scholar
  8. de Vries RP, Frisvad JC, van de Vondervoort PJI, Burgers K, Kuijpers AFA, Samson RA, Visser J (2005) Aspergillus vadensis, a new species of the group of black Aspergilli. Antonie Van Leeuwenhoek 87:195–203PubMedCrossRefGoogle Scholar
  9. de Vries RP, Burgers K, van de Vondervoort PJI, Frisvad JC, Samson RA, Visser J (2004) A new black Aspergillus species, A. vadensis, is a promising host for homologous and heterologous protein production. Appl Environ Microbiol 70:3954–3959PubMedCrossRefGoogle Scholar
  10. de Vries RP, van de Vondervoort PJI, Hendriks L, van de Belt M, Visser J (2002) Regulation of the α-glucuronidase encoding gene (aguA) from Aspergillus niger. Mol Genet Genomics 268:96–102PubMedCrossRefGoogle Scholar
  11. Dons JJM, de Vries OMH, Wessels JGH (1979) Characterization of the genome of the basidiomycete Schizophyllum commune. Biochim Biophys Acta 563:100–112PubMedGoogle Scholar
  12. Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395PubMedCrossRefGoogle Scholar
  13. Eriksson Ö, Goring DAI, Lindgren BO (1980) Structural studies on the chemical bonds between lignins and carbohydrates in spruce wood. Wood Sci Technol 14:267–279CrossRefGoogle Scholar
  14. Ferreira LAM, Wood TM, Williamson G, Faulds C, Hazlewood GP, Black GW, Gilbert HJ (1993) A modular esterase from Pseudomonas fluorescens subsp. cellulosa contains a non-catalytic cellulose-binding domain. Biochem J 294:349–355PubMedGoogle Scholar
  15. Gielkens MMC, Dekkers E, Visser J, de Graaff LH (1999) Two cellobiohydrolase-encoding genes from Aspergillus niger require d-xylose and the xylanolytic transcriptional activator XlnR for their expression. Appl Environ Microbiol 65:4340–4345PubMedGoogle Scholar
  16. Gilkes NR, Henrissat B, Kilburn DG, Miller RC Jr, Warren RAJ (1991) Domains in microbial β-1, 4-glycanases: sequence conservation, function, and enzyme families. Microbiol Rev 55:303–315PubMedGoogle Scholar
  17. Hirsch J, Koóš M, Kováč P (1998) Improved synthesis of an aldobiouronic acid related to hardwood xylans, and preparation of a derivative thereof suitable for linking to proteins. Carbohydr Res 310:145–149PubMedCrossRefGoogle Scholar
  18. Hirsch J, Langer V, Koóš M (2005) Synthesis and molecular structure of methyl 4-O-methyl-α-d-glucopyranuronate. Molecules 10:251–258PubMedCrossRefGoogle Scholar
  19. Imamura T, Watanabe T, Kuwahara M, Koshijima T (1994) Ester linkages between lignin and glucuronic acid in lignin-carbohydrate complexes from Fagus crenata. Phytochemistry 37:1165–1173PubMedCrossRefGoogle Scholar
  20. Jurasek L, Paice MG (1988) Xylanase A of Schizophyllum commune. Methods Enzymol 160:659–662CrossRefGoogle Scholar
  21. Kato M (2005) An overview of the CCAAT-box binding factor in filamentous fungi: assembly, nuclear translocation, and transcriptional enhancement. Biosci Biotechnol Biochem 69:663–672PubMedCrossRefGoogle Scholar
  22. Kulmburg P, Mathieu M, Dowzer C, Kelly J, Felenbok B (1993) Specific binding sites in the alcR and alcA promoters of the ethanol regulon for the CREA repressor mediating carbon catabolite repression in Aspergillus nidulans. Mol Microbiol 7:847–857PubMedCrossRefGoogle Scholar
  23. Kumar S, Tamura K, Nie M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  24. Kusters-van Someren MA, Harmsen JAM, Kester HCM, Visser J (1991) Structure of the Aspergillus niger pelA gene and its expression in Aspergillus niger and Aspergillus nidulans. Curr Genet 20:293–299PubMedCrossRefGoogle Scholar
  25. Li X-L, Špániková S, de Vries RP, Biely P (2007) Identification of genes encoding microbial glucuronoyl esteases. FEBS Lett 581:4029–4035PubMedCrossRefGoogle Scholar
  26. Linder M, Lindeberg G, Reinikainen T, Teeri TT, Pettersson G (1995) The difference in affinity between two fungal cellulose-binding domains is dominated by a single amino acid substitution. FEBS Lett 372:96–98PubMedCrossRefGoogle Scholar
  27. Lugones LG, Scholtmeijer K, Klootwijk R, Wessels JGH (1999) Introns are necessary for mRNA accumulation in Schizophyllum commune. Mol Microbiol 32:681–689PubMedCrossRefGoogle Scholar
  28. Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6PubMedCrossRefGoogle Scholar
  29. Obst JR (1982) Frequency and alkali resistance of lignin-carbohydrate bonds in wood. Tappi 65:109–112Google Scholar
  30. Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  31. Saloheimo M, Lehtovaara P, Pentilla M, Teeri TT, Ståhlberg J, Johansson G, Pettersson G, Claeyssens M, Tomme P, Knowles JKC (1988) EGIII, a new endoglucanase from Trichoderma reesei: the characterization of both gene and enzyme. Gene 63:11–22PubMedCrossRefGoogle Scholar
  32. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  33. Schuren FHJ, Wessels JGH (1994) Highly-efficient transformation of the homobasidiomycete Schizophyllum commune to phleomycin resistance. Curr Genet 26:179–183PubMedCrossRefGoogle Scholar
  34. Shoseyov O, Shani Z, Levy I (2006) Carbohydrate binding modules: biochemical properties and novel applications. Microbiol Mol Biol Rev 70:283–295PubMedCrossRefGoogle Scholar
  35. Špániková S, Biely P (2006) Glucuronoyl esterase––novel carbohydrate esterase produced by Schizophyllum commune. FEBS Lett 580:4597–4601PubMedCrossRefGoogle Scholar
  36. Špániková S, Poláková M, Joniak D, Hirsch J, Biely P (2007) Synthetic esters recognized by glucuronoyl esterase from Schizophyllum commune. Arch Microbiol 188:185–189PubMedCrossRefGoogle Scholar
  37. Tilburn J, Sarkar S, Widdick DA, Espeso EA, Orejas M, Mungroo J, Penalva MA, Arst HN Jr (1995) The Aspergillus PacC zinc finger transcription factor mediates regulation of both acidic- and alkaline-expressed genes by ambient pH. EMBO J 14:779–790PubMedGoogle Scholar
  38. van Peij NNME, Visser J, de Graaff LH (1998a) Isolation and analysis of XlnR, encoding a transcriptional activator coordinating xylanolytic expression in Aspergillus niger. Mol Microbiol 27:131–142PubMedCrossRefGoogle Scholar
  39. van Peij NNME, Gielkens MMC, 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 64:3615–3619PubMedGoogle Scholar
  40. Vishniac W, Santer M (1957) The thiobacilli. Bacteriol Rev 21:195–213PubMedGoogle Scholar
  41. Verdoes JC, Punt PJ, Stouthamer AH, van den Hondel CA (1994) The effect of multiple copies of the upstream region on expression of the Aspergillus niger glucoamylase-encoding gene. Gene 145:179–187PubMedCrossRefGoogle Scholar
  42. Watanabe T, Koshijima T (1988) Evidence for an ester linkage between lignin and glucuronic acid in lignin-carbohydrate complexes by DDQ-oxidation. Agric Biol Chem 52:2953–2955Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Miroslava Ďuranová
    • 1
  • Silvia Špániková
    • 1
  • Han A. B. Wösten
    • 2
  • Peter Biely
    • 1
    Email author
  • Ronald P. de Vries
    • 2
    Email author
  1. 1.Institute of Chemistry, Center for GlycomicsSlovak Academy of SciencesBratislavaSlovakia
  2. 2.Microbiology, Department of BiologyUniversity of UtrechtUtrechtThe Netherlands

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