Abstract
Efficient deconstruction of lignocellulose is achieved by the synergistic action of various hydrolytic and oxidative enzymes. However, the aldonolactones generated by oxidative enzymes have inhibitory effects on some cellulolytic enzymes. In this work, d-glucono-1,5-lactone was shown to have a much stronger inhibitory effect than d-glucose and d-gluconate on β-glucosidase, a vital enzyme during cellulose degradation. AltA, a secreted enzyme from Penicillium oxalicum, was identified as an aldonolactonase which can catalyze the hydrolysis of d-glucono-1,5-lactone to d-gluconic acid. In the course of lignocellulose saccharification conducted by cellulases from P. oxalicum or Trichoderma reesei, supplementation of AltA was able to relieve the decrease of β-glucosidase activity obviously with a stimulation of glucose yield. This boosting effect disappeared when sodium azide and ethylenediaminetetraacetic acid (EDTA) were added to the saccharification system to inhibit the activities of oxidative enzymes. In summary, we describe the first heterologous expression of a fungal secreted aldonolactonase and its application as an efficient supplement of cellulolytic enzyme system for lignocellulose biodegradation.
Similar content being viewed by others
References
Andric P, Meyer AS, Jensen PA, Dam-Johansen K (2010) Reactor design for minimizing product inhibition during enzymatic lignocellulose hydrolysis: I. Significance and mechanism of cellobiose and glucose inhibition on cellulolytic enzymes. Biotechnol Adv 28(3):308–324. doi:10.1016/j.biotechadv.2010.01.003
Bankar SB, Bule MV, Singhal RS, Ananthanarayan L (2009) Glucose oxidase—an overview. Biotechnol Adv 27(4):489–501. doi:10.1016/j.biotechadv.2009.04.003
Beeson WT, Iavarone AT, Hausmann CD, Cate JHD, Marletta MA (2011) Extracellular aldonolactonase from Myceliophthora thermophila. Appl Environ Microbiol 77(2):650–656. doi:10.1128/Aem.01922-10
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3
Brodie AF, Lipmann F (1955) Identification of a gluconolactonase. J Biol Chem 212(2):677–686
Bruchmann E, Schach H, Graf H (1987) Role and properties of lactonase in a cellulase system. Biotechnol Appl Biochem 9(2):146–159
Cannella D, Hsieh CW, Felby C, Jorgensen H (2012) Production and effect of aldonic acids during enzymatic hydrolysis of lignocellulose at high dry matter content. Biotechnol Biofuels 5(1):26. doi:10.1186/1754-6834-5-26
Cannella D, Jorgensen H (2014) Do new cellulolytic enzyme preparations affect the industrial strategies for high solids lignocellulosic ethanol production? Biotechnol Bioeng 111:59–68. doi:10.1002/bit.25098
Chen M, Qin Y, Liu Z, Liu K, Wang F, Qu Y (2010) Isolation and characterization of a β-glucosidase from Penicillium decumbens and improving hydrolysis of corncob residue by using it as cellulase supplementation. Enzym Microb Technol 46(6):444–449. doi:10.1016/j.enzmictec.2010.01.008
Conchie J, Gelman AL, Levvy GA (1967) Inhibition of glycosidases by aldonolactones of corresponding configuration. The C-4- and C-6-specificity of β-glucosidase and β-galactosidase. Biochem J 103(3):609–615
Coradetti ST, Xiong Y, Glass NL (2013) Analysis of a conserved cellulase transcriptional regulator reveals inducer-independent production of cellulolytic enzymes in Neurospora crassa. MicrobiologyOpen 2(4):595–609. doi:10.1002/mbo3.94
Fang X, Shen Y, Zhao J, Bao X, Qu Y (2010) Status and prospect of lignocellulosic bioethanol production in China. Bioresour Technol 101(13):4814–4819. doi:10.1016/j.biortech.2009.11.050
Ferrari AR, Rozeboom HJ, Dobruchowska JM, Van Leeuwen SS, Vugts ASC, Koetsier MJ, Visser J, Fraaije MW (2016) Discovery of a xylooligosaccharide oxidase from Myceliophthora thermophila C1. J Biol Chem 291(45):23709–23718. doi:10.1074/jbc.M116.741173
Gupta VK, Kubicek CP, Berrin JG, Wilson DW, Couturier M, Berlin A, Filho EXF, Ezeji T (2016) Fungal enzymes for bio-products from sustainable and waste biomass. Trends Biochem Sci 41(7):633–645. doi:10.1016/j.tibs.2016.04.006
Harris PV, Welner D, McFarland KC, Re E, Navarro Poulsen JC, Brown K, Salbo R, Ding H, Vlasenko E, Merino S, Xu F, Cherry J, Larsen S, Lo Leggio L (2010) Stimulation of lignocellulosic biomass hydrolysis by proteins of glycoside hydrolase family 61: structure and function of a large, enigmatic family. Biochemistry 49(15):3305–3316. doi:10.1021/bi100009p
Hemsworth GR, Johnston EM, Davies GJ, Walton PH (2015) Lytic polysaccharide monooxygenases in biomass conversion. Trends Biotechnol 33(12):747–761. doi:10.1016/j.tibtech.2015.09.006
Henriksson G, Johansson G, Pettersson G (2000) A critical review of cellobiose dehydrogenases. J Biotechnol 78(2):93–113. doi:10.1016/S0168-1656(00)00206-6
Hildebrand A, Addison JB, Kasuga T, Fan ZL (2016) Cellobionic acid inhibition of cellobiohydrolase I and cellobiose dehydrogenase. Biochem Eng J 109:236–242. doi:10.1016/j.bej.2016.01.024
Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315(5813):804–807. doi:10.1126/science.1137016
Igarashi K, Samejima M, Eriksson KEL (1998) Cellobiose dehydrogenase enhances Phanerochaete chrysosporium cellobiohydrolase I activity by relieving product inhibition. Eur J Biochem 253(1):101–106. doi:10.1046/j.1432-1327.1998.2530101.x
Kracher D, Scheiblbrandner S, Felice AKG, Breslmayr E, Preims M, Ludwicka K, Haltrich D, Eijsink VGH, Ludwig R (2016) Extracellular electron transfer systems fuel cellulose oxidative degradation. Science 352(6289):1098–1101. doi:10.1126/science.aaf3165
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(19):7007–7015. doi:10.1128/aem.05815-11
Li X, Chomvong K, Yu VY, Liang JM, Lin Y, Cate JHD (2015a) Cellobionic acid utilization: from Neurospora crassa to Saccharomyces cerevisiae. Biotechnol Biofuels 8:120. doi:10.1186/s13068-015-0303-2
Li Z, Yao G, Wu R, Gao L, Kan Q, Liu M, Yang P, Liu G, Qin Y, Song X, Zhong Y, Fang X, Qu Y (2015b) Synergistic and dose-controlled regulation of cellulase gene expression in Penicillium oxalicum. PLoS Genet 11(9):e1005509. doi:10.1371/journal.pgen.1005509
Liu G, Zhang L, Qin Y, Zou G, Li Z, Yan X, Wei X, Chen M, Chen L, Zheng K, Zhang J, Ma L, Li J, Liu R, Xu H, Bao X, Fang X, Wang L, Zhong Y, Liu W, Zheng H, Wang S, Wang C, Xun L, Zhao GP, Wang T, Zhou Z, Qu Y (2013a) Long-term strain improvements accumulate mutations in regulatory elements responsible for hyper-production of cellulolytic enzymes. Sci Rep 3:1569. doi:10.1038/srep01569
Liu G, Qin Y, Li Z, Qu Y (2013b) Development of highly efficient, low-cost lignocellulolytic enzyme systems in the post-genomic era. Biotechnol Adv 31(6):962–975. doi:10.1016/j.biotechadv.2013.03.001
Liu K, Lin X, Yue J, Li X, Fang X, Zhu M, Lin J, Qu Y, Xiao L (2010) High concentration ethanol production from corncob residues by fed-batch strategy. Bioresour Technol 101(13):4952–4958. doi:10.1016/j.biortech.2009.11.013
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31(3):426. doi:10.1021/ac60147a030
Qian Y, Zhong L, Hou Y, Qu Y, Zhong Y (2016) Characterization and strain improvement of a hypercellulytic variant, Trichoderma reesei SN1, by genetic engineering for optimized cellulase production in biomass conversion improvement. Front Microbiol 7:1349. doi:10.3389/fmicb.2016.01349
Scott BR, Huang HZ, Frickman J, Halvorsen R, Johansen KS (2016) Catalase improves saccharification of lignocellulose by reducing lytic polysaccharide monooxygenase-associated enzyme inactivation. Biotechnol Lett 38(3):425–434. doi:10.1007/s10529-015-1989-8
Song W, Han X, Qian Y, Liu G, Yao G, Zhong Y, Qu Y (2016) Proteomic analysis of the biomass hydrolytic potentials of Penicillium oxalicum lignocellulolytic enzyme system. Biotechnol Biofuels 9:68. doi:10.1186/s13068-016-0477-2
Sørensen A, Lübeck PS, Lübeck M, Teller PJ, Ahring BK (2011) β-glucosidases from a new Aspergillus species can substitute commercial β-glucosidases for saccharification of lignocellulosic biomass. Can J Microbiol 57(8):638–650. doi:10.1139/w11-052
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. doi:10.1093/molbev/msr121
Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics Chapter 2: Unit 2.3 doi:10.1002/0471250953.bi0203s00
Van Dyk JS, Pletschke BI (2012) A review of lignocellulose bioconversion using enzymatic hydrolysis and synergistic cooperation between enzymes—factors affecting enzymes, conversion and synergy. Biotechnol Adv 30(6):1458–1480. doi:10.1016/j.biotechadv.2012.03.002
Vuong TV, Vesterinen AH, Foumani M, Juvonen M, Seppala J, Tenkanen M, Master ER (2013) Xylo- and cello-oligosaccharide oxidation by gluco-oligosaccharide oxidase from Sarocladium strictum and variants with reduced substrate inhibition. Biotechnol Biofuels 6(1):148. doi:10.1186/1754-6834-6-148
Wei X, Zheng K, Chen M, Liu G, Li J, Lei Y, Qin Y, Qu Y (2011) Transcription analysis of lignocellulolytic enzymes of Penicillium decumbens 114-2 and its catabolite-repression-resistant mutant. C R Biol 334(11):806–811. doi:10.1016/j.crvi.2011.06.002
Witteveen FB, van de Vondervoort PJ, van den Broeck HC, van Engelenburg AC, de Graaff LH, Hillebrand MH, Schaap PJ, Visser J (1993) Induction of glucose oxidase, catalase, and lactonase in Aspergillus niger. Curr Genet 24(5):408–416. doi:10.1007/BF00351849
Zhang Z, Gibson P, Clark SB, Tian G, Zanonato PL, Rao L (2007) Lactonization and protonation of gluconic acid: a thermodynamic and kinetic study by potentiometry, NMR and ESI-MS. J Solut Chem 36(10):1187–1200. doi:10.1007/s10953-007-9182-x
Acknowledgements
This work was supported by grants from the National Basic Research Program of China (grant no. 2011CB707403), the Key Research and Development Project of Shandong Province (grant no. 2016GSF121026), and the National Natural Sciences Foundation of China (grant no. 21376141).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
This article does not contain any studies with human participants or animals performed by any of the author.
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
ESM 1
(PDF 629 kb)
Rights and permissions
About this article
Cite this article
Peng, S., Cao, Q., Qin, Y. et al. An aldonolactonase AltA from Penicillium oxalicum mitigates the inhibition of β-glucosidase during lignocellulose biodegradation. Appl Microbiol Biotechnol 101, 3627–3636 (2017). https://doi.org/10.1007/s00253-017-8134-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-017-8134-7