Advertisement

Expression and characterization of two glucuronoyl esterases from Thielavia terrestris and their application in enzymatic hydrolysis of corn bran

  • Jiao Tang
  • Liangkun Long
  • Yunfeng Cao
  • Shaojun DingEmail author
Biotechnologically relevant enzymes and proteins
First Online:

Abstract

The thermophilic fungus Thielavia terrestris when cultured on cellulose produces a cocktail of thermal hydrolases with potential application in saccharification of lignocellulosic biomass and other biotechnological areas. Glucuronoyl esterases are considered to play a unique role as accessory enzymes in lignocellulosic material biodegradation by cleaving the covalent ester linkage between 4-O-methyl-D-glucuronic acid (MeGlcA) and lignin in lignin-carbohydrate complexes (LCCs). Two glucuronoyl esterases from T. terrestris named TtGE1 and TtGE2 were expressed in Pichia pastoris. Both esterases displayed features of thermophilic enzymes, with the optimal temperature at 45 °C and 55 °C. TtGE1 and TtGE2 exhibited activity towards methyl (4-nitrophenyl β-D-glucopyranosid) uronate (Me-GlcA-pNP) but no catalytic activity to benzyl-D-glucuronate (BnzGlcA), indicating the difference in substrate specificity from previously studied fungal GEs. A substantial increase in the release of monomeric sugars and glucuronic acid from autohydrolysis of corn bran was observed by the supplementing TtGEs into commercial xylanase; the results clearly demonstrated that the TtGEs played a significant role in this degradation process. This research on TtGEs enriches our knowledge of this novel class of fungal GEs. These newly characterized TtGEs could be used as promising accessory enzymes to improve the hydrolysis efficiency of commercial enzymes in saccharification of lignocellulosic materials due to their thermophilic characteristics.

Keywords

Thielavia terrestris Glucuronoyl esterase Lignin-carbohydrate complexes Corn bran Substrate specificity 
This is a preview of subscription content, log in to check access.

Notes

Funding

This work was supported by a research grant (no. 31670591) from the National Natural Science Foundation of China, and a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions, and the Doctorate Fellowship Foundation of Nanjing Forestry University.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Human and animal rights

This article does not contain any studies with human participants or animals.

Supplementary material

253_2019_9662_MOESM1_ESM.pdf (378 kb)
Table S1 (PDF 378 kb)
253_2019_9662_MOESM2_ESM.xlsx (25 kb)
Table S2 (XLSX 24 kb)

References

  1. Agger JW, Busk PK, Pilgaard B, Meyer AS, Lange L (2017) A new functional classification of glucuronoyl esterases by peptide pattern recognition. Front Microbiol 8:309Google Scholar
  2. Baath JA, Giummarella N, Klaubauf S, Lawoko M, Olsson L (2016) A glucuronoyl esterase from Acremonium alcalophilum cleaves native lignin-carbohydrate ester bonds. FEBS Lett 590:2611–2618Google Scholar
  3. Baath JA, Mazurkewich S, Knudsen RM, Poulsen JCN, Olsson L, Lo Leggio L, Larsbrink J (2018) Biochemical and structural features of diverse bacterial glucuronoyl esterases facilitating recalcitrant biomass conversion. Biotechnol Biofuels 11:213Google Scholar
  4. 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 580:5815–5821Google Scholar
  5. Berka RM, Grigoriev IV, Otillar R, Salamov A, Grimwood J, Reid I, Ishmael N, John T, Darmond C, Moisan MC, Henrissat B, Coutinho PM, Lombard V, Natvig DO, Lindquist E, Schmutz J, Lucas S, Harris P, Powlowski J, Bellemare A, Taylor D, Butler G, de Vries RP, Allijn IE, van den Brink J, Ushinsky S, Storms R, Powell AJ, Paulsen IT, Elbourne LDH, Baker SE, Magnuson J, LaBoissiere S, Clutterbuck AJ, Martinez D, Wogulis M, de Leon AL, Rey MW, Tsang A (2011) Comparative genomic analysis of the thermophilic biomass-degrading fungi Myceliophthora thermophile and Thielavia terrestris. Nat Biotechnol 29:922–U222Google Scholar
  6. Biely P, Singh S, Puchart V (2016) Towards enzymatic breakdown of complex plantxylan structures: state of the art. Biotechnol Adv 34:1260–1274Google Scholar
  7. Charavgi MD, Dimarogona M, Topakas E, Christakopoulos P, Chrysina ED (2011) The structure of a novel glucuronoyl esterase from Myceliophthora thermophila gives new insights into its role as a potential biocatalyst. Acta Crystallogr D Biol Crystallogr 69:63–73Google Scholar
  8. Clark SE, Muslin EH, Henson CA (2004) Effect of adding and removing N-glycosylation recognition sites on the thermostability of barley α-glucosidase. Protein Eng Des Sel 17:245–249Google Scholar
  9. d’Errico C, Jorgensen JO, Krogh KBRM, Spodsberg N, Madsen R, Monrad RN (2015) Enzymatic degradation of lignin-carbohydrate complexes (LCCs): model studies using a fungal glucuronoyl esterase from Cerrena unicolor. Biotechnol Bioeng 112:914–922Google Scholar
  10. d’Errico C, Borjesson J, Ding HS, Krogh KBRM, Spodsberg N, Madsen R, Monrad RN (2016) Improved biomass degradation using fungal glucuronoyl-esterases hydrolysis of natural corn fiber substrate. J Biotechnol 219:117–123Google Scholar
  11. De Santi C, Willassen NP, Williamson A (2016) Biochemical characterization of a family 15 carbohydrate esterase from a bacterial marine arctic metagenome. PLoS One 11:e0159345Google Scholar
  12. Dilokpimol A, Makela MR, Cerullo G, Zhou M, Varriale S, Gidijala L, Bras JLA, Jutten P, Piechot A, Verhaert R, Faraco V, Hilden KS, de Vries RP (2018) Fungal glucuronoyl esterases: genome mining based enzyme discovery and biochemical characterization. New Biotechnol 40:282–287Google Scholar
  13. Du X, Gellerstedt G, Li J (2013) Universal fractionation of lignin-carbohydrate complexes (LCCs) from lignocellulosic biomass: an example using sprucewood. Plant J 74:328–338Google Scholar
  14. Duranova M, Spanikova S, Wosten HAB, Biely P, de Vries RP (2009) Two glucuronoyl esterases of Phanerochaete chrysosporium. Arch Microbiol 191:133–140Google Scholar
  15. Franova L, Puchart V, Biely P (2016) β-Glucuronidase-coupled assays of glucuronoyl esterases. Anal Biochem 510:114–119Google Scholar
  16. Gao J, Huang JW, Li Q, Liu WD, Ko TP, Zheng YY, Xiao XS, Kuo CJ, Chen CC, Guo RT (2017) Characterization and crystal structure of a thermostable glycoside hydrolase family 45 1,4-beta-endoglucanase from Thielavia terrestris. Enzym Microb Technol 99:32–37Google Scholar
  17. Garcia-Huante Y, Cayetano-Cruz M, Santiago-Hernandez A, Cano-Ramirez C, Marsch-Moreno R, Campos JE, Aguilar-Osorio G, Benitez-Cardoza CG, Trejo-Estrada S, Hidalgo-Lara ME (2017) The thermophilic biomass-degrading fungus Thielavia terrestris Co3Bag1 produces a hyperthermophilic and thermostable beta-1,4-xylanase with exo- and endo-activity. Extremophiles 21:175–186Google Scholar
  18. Han Y, Lei XG (1999) Role of glycosylation in the functional expression of an Aspergillus niger phytase (phyA) in Pichiapastoris. Arch Biochem Biophys 364:83–90Google Scholar
  19. Hu H, Li L, Ding S (2015) An organic solvent-tolerant phenolic acid decarboxylase from Bacillus licheniformis for the efficient bioconversion of hydroxycinnamic acids to vinyl phenol derivatives. Appl Microbiol Biotechnol 99:5071–5081Google Scholar
  20. Huang CX, He J, Li X, Min DY, Yong Q (2015) Facilitating the enzymatic saccharification of pulped bamboo residues by degrading the remained xylan and lignin-carbohydrates complexes. Bioresour Technol 192:71–477Google Scholar
  21. Huttner S, Klaubauf S, de Vries RP, Olsson L (2017) Characterization of three fungal glucuronoyl esterases on glucuronic acid ester model compounds. Appl Microbiol Biotechnol 101:5301–5311Google Scholar
  22. Huynh HH, Arioka M (2016) Functional expression and characterization of a glucuronoyl esterase from the fungus Neurospora crassa: identification of novel consensus sequences containing the catalytic triad. J Gen Appl Microbiol 62:217–224Google Scholar
  23. Huynh HH, Ishii N, Matsuo I, Arioka M (2018) A novel glucuronoyl esterase from Aspergillus fumigatus-the role of conserved Lys residue in the preference for 4-O-methyl glucuronoyl esters. Appl Microbiol Biotechnol 102:2191–2201Google Scholar
  24. Jeffries TW (1994) Biodegradation of lignin and hemicelluloses. In: Ratledge C (ed) Biochemistry of microbial degradation. Kluweracademic Publisher, Madison, pp 233–277Google Scholar
  25. Jiang KK, Li LL, Long LK, Ding SJ (2018) Comprehensive evaluation of combining hydrothermal pretreatment (autohydrolysis) with enzymatic hydrolysis for efficient release of monosaccharides and ferulic acid from corn bran. Ind Crop Prod 113:348–357Google Scholar
  26. Katsimpouras C, Benarouche A, Navarro D, Karpusas M, Dimarogona M, Berrin JG, Christakopoulos P, Topakas E (2014) Enzymatic synthesis of model substrates recognized by glucuronoyl esterases from Podospora anserina and Myceliophthora thermophila. Appl Microbiol Biotechnol 98:5507–5516Google Scholar
  27. Kim IJ, Seo N, An HJ, Kim JH, Harris PV, Kim KH (2017) Type-dependent action modes of TtAA9E and TaAA9A acting on cellulose and differently pretreated lignocellulosic substrates. Biotechnol Biofuels 10:46Google Scholar
  28. Langston JA, Shaghasi T, Abbate E, Xu F, Vlasenko E, Sweeney MD (2011) Oxidoreductive cellulose depolymerization by the enzymes cellobiose dehydrogenase and glycoside hydrolase 61. Appl Environ Microbiol 77:7007–7015Google Scholar
  29. Langston JA, Brown K, Xu F, Borch K, Garner A, Sweeney MD (2012) Cloning, expression, and characterization of a cellobiose dehydrogenase from Thielavia terrestris induced under cellulose growth conditions. Biochim Biophys Acta 1824:802–812Google Scholar
  30. Li XL, Spanikova S, de Vries RP, Biely P (2007) Identification of genes encoding microbial glucuronoyl esterases. FEBS Lett 581:4029–4035Google Scholar
  31. Lombard V, Ramulu HG, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495Google Scholar
  32. Manns D, Deutschle AL, Saake B, Meyer AS (2014) Methodology for quantitative determination of the carbohydrate composition of brown seaweeds (Laminariaceae). RSC Adv 4:25736–25746Google Scholar
  33. Menon V, Rao M (2012) Trends in bioconversion of lignocellulose: biofuels, platform chemicals and biorefinery concept. Prog Energy Combust Sci 38:522–550Google Scholar
  34. Monrad RN, Eklof J, Krogh KBRM, Biely P (2018) Glucuronoyl esterases: diversity, properties and biotechnological potential. A review. Crit Rev Biotechnol:1–16Google Scholar
  35. Mosbech C, Holck J, Meyer AS, Agger JW (2018) The natural catalytic function of CuGE glucuronoyl esterase in hydrolysis of genuine lignin–carbohydrate complexes from birch. Biotechnol Biofuels 11:71–79Google Scholar
  36. Pokkuluri PR, Duke NEC, Wood SJ, Cotta MA, Li XL, Biely P, Schiffer M (2011) Structure of the catalytic domain of glucuronoyl esterase Cip2 from Hypocrea jecorina. Proteins 79:2588–2592Google Scholar
  37. Ragauskas AJ, Williams CK, Davison BH, Britovsek G, Cairney J, Eckert CA, Frederick WJ Jr, Hallett JP, Leak DJ, Liotta CL, Mielenz JR, Murphy R, Templer R, Tschaplinski T (2006) The path forward for biofuels and biomaterials. Science 311:484–489Google Scholar
  38. Sanchez OJ, Cardona CA (2008) Trends in biotechnological production of fuel ethanol from different feedstocks. Bioresour Technol 99:5270–5295Google Scholar
  39. Shi AQ, Hu H, Zheng F, Long LK, Ding SJ (2015) Biochemical characteristics of an alkaline pectate lyase PelA from Volvariella volvacea: roles of the highly conserved N-glycosylation site in its secretion and activity. Appl Microbiol Biotechnol 99:3447–3458Google Scholar
  40. Spanikova S, Biely P (2006) Glucuronoyl esterase—novel carbohydrate esterase produced by Schizophyllum commune. FEBS Lett 580:4597–4601Google Scholar
  41. Sunner H, Charavgi M-D, Olsson L, Topakas E, Christakopoulos P (2015) Glucuronoyl esterase screening and characterization assays utilizing commercially available benzyl glucuronic acid ester. Molecules 20:17807–17817Google Scholar
  42. Takahashi N, Koshijima T (1988) Ester linkages between lignin and glucuronoxylan in a lignin-carbohydrate complex from beech (Fagus crenata) wood. Wood Sci Technol 22:231–241Google Scholar
  43. Topakas E, Moukouli M, Dimarogona M, Vafiadi C, Christakopoulos P (2010) Functional expression of a thermophilic glucuronoyl esterase from Sporotrichum thermophile: identification of the nucleophilic serine. Appl Microbiol Biotechnol 87:1765–1772Google Scholar
  44. Tsai AYL, Canam T, Gorzsas A, Mellerowicz EJ, Campbell MM, Master ER (2012) Constitutive expression of a fungal glucuronoyl esterase in Arabidopsis reveals altered cell wall composition and structure. Plant Biotechnol J 10:1077–1087Google Scholar
  45. Vafiadi C, Topakas E, Biely P, Christakopoulos P (2009) Purification, characterization and mass spectrometric sequencing of a thermophilic glucuronoyl esterase from Sporotrichum thermophile. FEMS Microbiol Lett 296:178–184Google Scholar
  46. Xu HB, Yan QJ, Duan XJ, Yang SQ, Jiang ZQ (2015) Characterization of an acidic cold-adapted cutinase from Thielavia terrestris and its application in flavor ester synthesis. Food Chem 188:439–445Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Jiao Tang
    • 1
  • Liangkun Long
    • 1
  • Yunfeng Cao
    • 1
  • Shaojun Ding
    • 1
    Email author
  1. 1.The Co-Innovation Center of Efficient Processing and Utilization of Forest Resources, Jiangsu Key Lab for the Chemistry & Utilization of Agricultural and Forest Biomass, College of Chemical EngineeringNanjing Forestry UniversityNanjingChina

Personalised recommendations

Cite article

Buy options