A chlorogenic acid esterase with a unique substrate specificity from Ustilago maydis

Applied and Environmental Microbiology

Volumn 81, Issue 5, 2015, Pages 1679-1688

  Nieter, Annabel ^a   Haase Aschoff, Paul ^a   Kelle, Sebastian ^a   Linke, Diana ^a   Krings, Ulrich ^a   Popper, Lutz ^b   Berger, Ralf G ^a  

^a LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^b SternEnzym GmbH and Co KG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AFFINITY CHROMATOGRAPHY; AMINO ACIDS; COLUMN CHROMATOGRAPHY; ELECTROPHORESIS; ENZYME ACTIVITY; ENZYMES; ESTERS; GENE ENCODING; HYDROPHOBIC CHROMATOGRAPHY; HYDROPHOBICITY; LIQUID CHROMATOGRAPHY; PROTEINS; PURIFICATION; SUBSTRATES;

ANION EXCHANGE CHROMATOGRAPHY; HYDROPHOBIC INTERACTION CHROMATOGRAPHY; ISOELECTRIC FOCUSING; MONOMERIC PROTEINS; NATURAL SUBSTRATES; PICHIA PASTORIS GS115; SEQUENCE ALIGNMENTS; SUBSTRATE SPECIFICITY;

CHROMATOGRAPHY;

AMINO ACID; BIOMASS; CHROMATOGRAPHY; ENZYME; FUNGUS; GENE EXPRESSION; HYDROPHOBICITY; ION EXCHANGE; PH; PROTEIN; REACTION KINETICS; SUBSTRATE;

PICHIA PASTORIS; TRITICUM AESTIVUM; USTILAGO; USTILAGO MAYDIS;

CAFFEIC ACID DERIVATIVE; CARBOXYLESTERASE; CHLOROGENIC ACID; CHLOROGENIC ACID ESTERASE; COUMARIC ACID; FERULIC ACID; FUNGAL DNA;

CHEMISTRY; DNA SEQUENCE; ENZYME SPECIFICITY; ENZYMOLOGY; GENE EXPRESSION; GENETICS; ISOELECTRIC FOCUSING; ISOLATION AND PURIFICATION; KINETICS; LIQUID CHROMATOGRAPHY; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; MOLECULAR WEIGHT; PH; PICHIA; POLYACRYLAMIDE GEL ELECTROPHORESIS; SEQUENCE HOMOLOGY; TEMPERATURE; USTILAGO;

CAFFEIC ACIDS; CARBOXYLIC ESTER HYDROLASES; CHLOROGENIC ACID; CHROMATOGRAPHY, LIQUID; CLONING, MOLECULAR; COUMARIC ACIDS; DNA, FUNGAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION; HYDROGEN-ION CONCENTRATION; ISOELECTRIC FOCUSING; KINETICS; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PICHIA; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; TEMPERATURE; USTILAGO;

EID: 84922895190     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02911-14     Document Type: Article

References (59)

1. Ishii T. 1997. Structure and function of feruloylated polysaccharides. Plant Sci 127:111-127. http://dx.doi.org/10.1016/S0168-9452(97)00130-1.
2. Cosgrove DJ. 2001. Wall structure and wall loosening. A look backwards and forwards. Plant Physiol 125:131-134. http://dx.doi.org/10.1104/pp.125.1.131.
3. Ralet MC, Faulds CB, Williamson G, Thibault JF. 1994. Degradation of feruloylated oligosaccharides from sugar-beet pulp and wheat bran by ferulic acid esterases from Aspergillus niger. Carbohydr Res 263:257-269. http://dx.doi.org/10.1016/0008-6215(94)00177-4.
4. Clifford MN. 1999. Chlorogenic acids and other cinnamates-nature, occurrence, dietary burden, absorption and metabolism. J Sci Food Agric 79:362-372.
5. Kroon PA, Garcia-Conesa MT, Fillingham IJ, Hazlewood GP, Williamson G. 1999. Release of ferulic acid dehydrodimers from plant cell walls by feruloyl esterases. J Sci Food Agric 79:428-434.
6. Williamson G, Faulds CB, Kroon PA. 1998. Specificity of ferulic acid (feruloyl) esterases. Biochem Soc Trans 26:205-209.
7. Wong DW. 2006. Feruloyl esterase: a key enzyme in biomass degradation. Appl Biochem Biotechnol 133:87-112. http://dx.doi.org/10.1385/ABAB:133:2:87.
8. Fazary AE, Ju YH. 2007. Feruloyl esterases as biotechnological tools: current and future perspectives. Acta Biochim Biophys Sin 39:811-828. http://dx.doi.org/10.1111/j.1745-7270.2007.00348.x.
9. Topakas E, Vafiadi C, Christakopoulos P. 2007. Microbial production, characterization and applications of feruloyl esterases. Process Biochem 42:497-509. http://dx.doi.org/10.1016/j.procbio.2007.01.007.
10. Crepin VF, Faulds CB, Connerton IF. 2004. Functional classification of the microbial feruloyl esterases. Appl Microbiol Biotechnol 63:647-652. http://dx.doi.org/10.1007/s00253-003-1476-3.
11. Schöbel B, Pollmann W. 1980. Further characterization of a chlorogenic acid hydrolase from Aspergillus niger. Z Naturforsch C 35:699-701.
12. Schöbel B, Pollmann W. 1980. Isolation and characterization of a chlorogenic acid esterase from Aspergillus niger. Z Naturforsch C 35:209-212.
13. Asther M, Estrada Alvarado MI, Haon M, Navarro D, Asther M, Lesage-Meessen L, Record E. 2005. Purification and characterization of a chlorogenic acid hydrolase from Aspergillus niger catalysing the hydrolysis of chlorogenic acid. J Biotechnol 115:47-56. http://dx.doi.org/10.1016/j.jbiotec.2004.07.009.
14. Benoit I, Asther M, Bourne Y, Navarro D, Canaan S, Lesage-Meessen L, Herweijer M, Coutinho PM, Asther M, Record E. 2007. Gene overexpression and biochemical characterization of the biotechnologically relevant chlorogenic acid hydrolase from Aspergillus niger. Appl Environ Microbiol 73:5624-5632. http://dx.doi.org/10.1128/AEM.00374-07.
15. Adachi O, Ano Y, Akakabe Y, Shinagawa E, Matsushita K. 2008. Coffee pulp koji of Aspergillus sojae as stable immobilized catalyst of chlorogenate hydrolase. Appl Microbiol Biotechnol 81:143-151. http://dx.doi.org/10.1007/s00253-008-1659-z.
16. Okamura S, Watanabe M. 1982. Purification and properties of hydroxycinnamic acid ester hydrolase from Aspergillus japonicus. Agric Biol Chem 46:1839-1848. http://dx.doi.org/10.1271/bbb1961.46.1839.
17. Barbe C, Dubourdieu D. 1998. Characterization and purification of a cinnamate esterase from Aspergillus niger industrial pectinase preparation. J Sci Food Agric 78:471-478.
18. Levasseur A, Benoit I, Asther M, Asther M, Record E. 2004. Homologous expression of the feruloyl esterase B gene from Aspergillus niger and characterization of the recombinant enzyme. Protein Expr Purif 37:126-133. http://dx.doi.org/10.1016/j.pep.2004.05.019.
19. 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 83:689-696. http://dx.doi.org/10.1007/s00253-009-1913-z.
20. Vafiadi C, Topakas E, Christakopoulos P, Faulds CB. 2006. The feruloyl esterase system of Talaromyces stipitatus: determining the hydrolytic and synthetic specificity of TsFaeC. J Biotechnol 125:210-221. http://dx.doi.org/10.1016/j.jbiotec.2006.02.009.
21. Qi M, Wang P, Selinger LB, Yanke LJ, Forster RJ, McAllister TA. 2011. Isolation and characterization of a ferulic acid esterase (Fae1A) from the rumen fungus Anaeromyces mucronatus. J Appl Microbiol 110:1341-1350. http://dx.doi.org/10.1111/j.1365-2672.2011.04990.x.
22. Couteau D, McCartney AL, Gibson GR, Williamson G, Faulds CB. 2001. Isolation and characterization of human colonic bacteria able to hydrolyse chlorogenic acid. J Appl Microbiol 90:873-881. http://dx.doi.org/10.1046/j.1365-2672.2001.01316.x.
23. Borneman WS, Hartley RD, Morrison WH, Akin DE, Ljungdahl LG. 1990. Feruloyl and p-coumaroyl esterase from anaerobic fungi in relation to plant cell wall degradation. Appl Microbiol Biotechnol 33:345-351. http://dx.doi.org/10.1007/BF00164534.
24. Allerdings E, Ralph J, Steinhart H, Bunzel M. 2006. Isolation and structural identification of complex feruloylated heteroxylan side-chains from maize bran. Phytochemistry 67:1276-1286. http://dx.doi.org/10.1016/j.phytochem.2006.04.018.
25. Linke D, Matthes R, Nimtz M, Zorn H, Bunzel M, Berger RG. 2013. An esterase from the basidiomycete Pleurotus sapidus hydrolyzes feruloylated saccharides. Appl Microbiol Biotechnol 97:7241-7251. http://dx.doi.org/10.1007/s00253-012-4598-7.
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 108:227-241. http://dx.doi.org/10.1016/j.jbiotec.2003.12.003.
27. Johnson KG, Harrison BA, Schneider H, MacKenzie CR, Fontana JD. 1988. Xylan-hydrolysing enzymes from Streptomyces spp. Enzyme Microb Technol 10:403-409.
28. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685. http://dx.doi.org/10.1038/227680a0.
29. Nieter A, Haase-Aschoff P, Linke D, Nimtz M, Berger RG. 2014. A halotolerant type A feruloyl esterase from Pleurotus eryngii. Fungal Biol 118:348-357. http://dx.doi.org/10.1016/j.funbio.2014.01.010.
30. Lin-Cereghino J, Wong WW, Xiong S, Giang W, Luong LT, Vu J, Johnson SD, Lin-Cereghino GP. 2005. Condensed protocol for competent cell preparation and transformation of the methylotrophic yeast Pichia pastoris. Biotechniques 38:44, 46, 48. http://dx.doi.org/10.2144/05381BM04.
31. Sygmund C, Gutmann A, Krondorfer I, Kujawa M, Glieder A, Pscheidt B, Haltrich D, Peterbauer C, Kittl R. 2012. Simple and efficient expression of Agaricus meleagris pyranose dehydrogenase in Pichia pastoris. Appl Microbiol Biotechnol 94:695-704. http://dx.doi.org/10.1007/s00253-011-3667-7.
32. Nicolaus RA, Piattelli M. 1965. Progress in the chemistry of natural black pigments. Acad Sci Fis Mat Napoli Rend Ser 4 32:83-97.
33. Wheeler MH. 1983. Comparison of fungal melanin biosynthesis in ascomycetous, imperfect and basidiomycetous fungi. Trans Br Mycol Soc 81: 29-36. http://dx.doi.org/10.1016/S0007-1536(83)80200-9.
34. Benoit I, Navarro D, Marnet N, Rakotomanomana N, Lesage-Meessen L, Sigoillot JC, Asther M, Asther M. 2006. Feruloyl esterases as a tool for the release of phenolic compounds from agro-industrial by-products. Carbohydr Res 341:1820-1827. http://dx.doi.org/10.1016/j.carres.2006.04.020.
35. Crepin VF, Faulds CB, Connerton IF. 2003. A non-modular type B feruloyl esterase from Neurospora crassa exhibits concentrationdependent substrate inhibition. Biochem J 370:417-427. http://dx.doi.org/10.1042/BJ20020917.
36. Koseki T, Fushinobu S, Ardiansyah Shirakawa H, Komai M. 2009. Occurrence, properties, and applications of feruloyl esterases. Appl Microbiol Biotechnol 84:803-810. http://dx.doi.org/10.1007/s00253-009-2148-8.
37. Sigoillot C, Camarero S, Vidal T, Record E, Asther M, Perez-Boada M, Martinez MJ, Sigoillot JC, Colom JF, Martinez AT. 2005. Comparison of different fungal enzymes for bleaching high-quality paper pulps. J Biotechnol 115:333-343. http://dx.doi.org/10.1016/j.jbiotec.2004.09.006.
38. Topakas E, Stamatis H, Biely P, Kekos D, Macris BJ, Christakopoulos P. 2003. Purification and characterization of a feruloyl esterase from Fusarium oxysporum catalyzing esterification of phenolic acids in ternary water-organic solvent mixtures. J Biotechnol 102:33-44. http://dx.doi.org/10.1016/S0168-1656(02)00363-2.
39. 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 63:686-690. http://dx.doi.org/10.1007/s00253-003-1481-6.
40. Vallee BL, Ulmer DD. 1972. Biochemical effects of mercury, cadmium and lead. Annu Rev Biochem 41:91-128. http://dx.doi.org/10.1146/annurev.bi.41.070172.000515.
41. Wang L, Zhang R, Ma Z, Wang H, Ng T. 2014. A feruloyl esterase (FAE) characterized by relatively high thermostability from the edible mushroom Russula virescens. Appl Biochem Biotechnol 172:993-1003. http://dx.doi.org/10.1007/s12010-013-0536-0.
42. Donaghy J, McKay AM. 1997. Purification and characterization of a feruloyl esterase from the fungus Penicillium expansum. J Appl Microbiol 83:718-726. http://dx.doi.org/10.1046/j.1365-2672.1997.00307.x.
43. Yao J, Chen QL, Shen AX, Cao W, Liu YH. 2013. A novel feruloyl esterase from a soil metagenomic library with tannase activity. J Mol Catal B Enzym 95:55-61. http://dx.doi.org/10.1016/j.molcatb.2013.05.026.
44. Gold AM, Fahrney D. 1964. Sulfonyl fluorides as inhibitors of esterases. II. Formation and reactions of phenylmethanesulfonyl alpha chymotrypsin. Biochemistry 3:783-791.
45. Anson ML. 1940. The reactions of iodine and iodoacetamide with native egg albumin. J Gen Physiol 23:321-331. http://dx.doi.org/10.1085/jgp.23.3.321.
46. Kumar L, Singh B, Adhikari DK, Mukherjee J, Ghosh D. 2012. A thermoalkaliphilic halotolerant esterase from Rhodococcus sp. LKE-028 (MTCC 5562): enzyme purification and characterization. Process Biochem 47:983-991. http://dx.doi.org/10.1016/j.procbio.2012.03.020.
47. Benoit I, Danchin EGJ, Bleichrodt R-J, de Vries RP. 2008. Biotechnological applications and potential of fungal feruloyl esterases based on prevalence, classification and biochemical diversity. Biotechnol Lett 30: 387-396. http://dx.doi.org/10.1007/s10529-007-9564-6.
48. Udatha DB, Kouskoumvekaki I, Olsson L, Panagiotou G. 2011. The interplay of descriptor-based computational analysis with pharmacophore modeling builds the basis for a novel classification scheme for feruloyl esterases. Biotechnol Adv 29:94-110. http://dx.doi.org/10.1016/j.biotechadv.2010.09.003.
49. de Vries RP, vanKuyk PA, Kester HC, 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 363:377-386. http://dx.doi.org/10.1042/0264-6021:3630377.
50. Topakas E, Christakopoulos P, Faulds CB. 2005. Comparison of mesophilic and thermophilic feruloyl esterases: characterization of their substrate specificity for methyl phenylalkanoates. J Biotechnol 115:355-366. http://dx.doi.org/10.1016/j.jbiotec.2004.10.001.
51. Kroon PA, Faulds CB, Brezillon C, Williamson G. 1997. Methyl phenylalkanoates as substrates to probe the active sites of esterases. Eur J Biochem 248:245-251. http://dx.doi.org/10.1111/j.1432-1033.1997.00245.x.
52. Faulds CB, Sancho AI, Bartolome B. 2002. Mono-and dimeric ferulic acid release from brewer's spent grain by fungal feruloyl esterases. Appl Microbiol Biotechnol 60:489-494. http://dx.doi.org/10.1007/s00253-002-1140-3.
53. Moukouli M, Topakas E, Christakopoulos P. 2008. Cloning, characterization and functional expression of an alkalitolerant type C feruloyl esterase from Fusarium oxysporum. Appl Microbiol Biotechnol 79:245-254. http://dx.doi.org/10.1007/s00253-008-1432-3.
54. 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 43:1082-1087. http://dx.doi.org/10.1007/BF00166929.
55. Benoit I, Asther M, Sulzenbacher G, Record E, Marmuse L, Parsiegla G, Gimbert I, Asther M, Bignon C. 2006. Respective importance of protein folding and glycosylation in the thermal stability of recombinant feruloyl esterase A. FEBS Lett 580:5815-5821. http://dx.doi.org/10.1016/j.febslet.2006.09.039.
56. Brenner S. 1988. The molecular evolution of genes and proteins: a tale of two serines. Nature 334:528-530. http://dx.doi.org/10.1038/334528a0.
57. Dodson G, Wlodawer A. 1998. Catalytic triads and their relatives. Trends Biochem Sci 23:347-352. http://dx.doi.org/10.1016/S0968-0004(98)01254-7.
58. Shin HD, Chen RR. 2007. A type B feruloyl esterase from Aspergillus nidulans with broad pH applicability. Appl Microbiol Biotechnol 73: 1323-1330. http://dx.doi.org/10.1007/s00253-006-0612-2.
59. Mubarak A, Hodgson JM, Considine MJ, Croft KD, Matthews VB. 2013. Supplementation of a high-fat diet with chlorogenic acid is associated with insulin resistance and hepatic lipid accumulation in mice. J Agric Food Chem 61:4371-4378. http://dx.doi.org/10.1021/jf400920x.