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Factors affecting the hydrolytic action of xylanase during pennisetum saccharification: role of lignin

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Abstract

Inhibition of cellulose hydrolysis has been reported extensively, however, there is a paucity of information describing the effect of lignin on xylan hydrolysis by endo-xylanase and β-xylosidase. In this report, the effects of two different lignins on enzymatic hydrolysis of isolated xylan and NaOH-pretreated pennisetum by endo-xylanase and β-xylosidase were assessed. Both acid insoluble lignin (AIL) and enzymatic hydrolysis lignin (EHL) were found to inhibit hydrolysis of endo-xylanase and β-xylosidase, and AIL had a stronger negative effect on enzymatic hydrolysis when compared with that of EHL. Results from inhibitory kinetics experiments showed that the inhibition of AIL and EHL on xylanase did not follow Michaelis–Menten kinetics. The higher adsorption capacity of AIL toward xylanase arose from its higher hydrophobicity and lower absolute zeta potential, and this likely explains the higher inhibitory effect of AIL than that of EHL. The results aid our understanding of the role of lignin in xylan hydrolysis by xylanolytic enzymes.

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Abbreviations

NACP:

Chinese pennisetum with NaOH pretreatment

AIL:

Acid insoluble lignin

EHL:

Enzymatic hydrolysis lignin

XYL:

Endo-xylanase from Trichoderma longibrachiatum

βX:

β-Xylosidase from Selenomonas ruminantium

XOS:

Xylo-oligosaccharides

DM:

Dry matter

References

  • Alvira P, Tomás-Pejó E, Ballesteros M, Negro MJ (2010) Pretreatment technologies for an efficient bioethanol production process based on enzymatic hydrolysis: a review. Bioresour Technol 101(13):4851–4861

    CAS  PubMed  Google Scholar 

  • Bailey MJ, Biely Poutanen (1992) Interlaboratory testing of methods for assay of xylanase activity. J Biotechnol 23(3):257–270

    CAS  Google Scholar 

  • Berlin A, Balakshin M, Gilkes N, Kadla J, Maximenko V, Kubo S, Saddler J (2006) Inhibition of cellulase, xylanase and β-glucosidase activities by softwood lignin preparations. J Biotechnol 125(2):198–209

    CAS  PubMed  Google Scholar 

  • Brigitte C, Christine T, Mickal H, Alankar V, Anouck H, Gabriel P, Lloyd D (2018) Fluorescence techniques can reveal cell wall organization and predict saccharification in pretreated wood biomass. Ind Crop Prod 123:84–92

    Google Scholar 

  • Chen G, Song W, Qi B, Lu J, Wan Y (2013) Recycling cellulase from enzymatic hydrolyzate of acid treated wheat straw by electroultrafiltration. Bioresour Technol 144(5):186–193

    CAS  PubMed  Google Scholar 

  • Chen X, Xin D, Wang R, Qin Y, Wen P, Hou X, Zhang J (2019) Factors affecting hydrolytic action of xylanase during pennisetum saccharification: role of cellulose and its derivatives. Ind Crop Prod 130:49–56

    CAS  Google Scholar 

  • Financie R, Moniruzzaman M, Uemura Y (2016) Enhanced enzymatic delignification of oil palm biomass with ionic liquid pretreatment. Biochem Eng J110:1–7

    Google Scholar 

  • García-Torreiro M, Lú-Chau T, Gullón B, Moreira M, Lema J, Eibes G (2018) Lessons learned from the treatment of organosolv pulp with ligninolytic enzymes and chemical delignification agents. Cellulose 25(1):763–776

    Google Scholar 

  • Gessner A, Waicz R, Lieske A, Paulke BR, Mäder K, Müller RH (2000) Nanoparticles with decreasing surface hydrophobicities: influence on plasma protein adsorption. Int J Pharmaceut 196(2):245–249

    CAS  Google Scholar 

  • Ghorbani F, Karimi M, Biria D, Kariminia HR, Jeihanipour A (2015) Enhancement of fungal delignification of rice straw by Trichoderma viride sp. to improve its saccharification. Biochem Eng J101:77–84

    Google Scholar 

  • Guo F, Shi W, Sun W, Li X, Wang F, Zhao J, Qu Y (2014) Differences in the adsorption of enzymes onto lignins from diverse types of lignocellulosic biomass and the underlying mechanism. Biotechnol Biofuels 7(1):38

    PubMed  PubMed Central  Google Scholar 

  • Huang C, Lin W, Lai C, Li X, Jin Y, Yong Q (2019) Coupling the post-extraction process to remove residual lignin and alter the recalcitrant structures for improving the enzymatic digestibility of acid-pretreated bamboo residues. Bioresour Technol 285:121355

    CAS  PubMed  Google Scholar 

  • Jiang B, Gu F, Wu W, Wang Z, Jin Y (2018) Comparison study of lithium chloride/dimethylsulfoxide (LiCl/DMSO) dissolution and water regeneration behavior of ball-milled wheat stem and leaf. J Forestry Eng 3(04):87–95

    Google Scholar 

  • Kellock M, Rahikainen J, Marjamaa K, Kruus K (2017) Lignin-derived inhibition of monocomponent cellulases and a xylanase in the hydrolysis of lignocellulosics. Bioresour Technol 232:183–191

    CAS  PubMed  Google Scholar 

  • Knob A, Terrasan CRF, Carmona EC (2010) Beta-Xylosidases from filamentous fungi: an overview. World J Microb Biot 26(3):389–407

    CAS  Google Scholar 

  • Ko K, Youngmi K, Eduardo X, Ladisch MR (2015) Effect of liquid hot water pretreatment severity on properties of hardwood lignin and enzymatic hydrolysis of cellulose. Biotechnol Bioeng 112(2):252–262

    CAS  PubMed  Google Scholar 

  • Lai C, Jia Y, Wang J, Wang R, Zhang Q, Chen L, Shi H, Huang C, Li X, Yong Q (2019) Co-production of xylooligosaccharides and fermentable sugars from poplar through acetic acid pretreatment followed by poly (ethylene glycol) ether assisted alkali treatment. Bioresour Technol 288:121569

    CAS  PubMed  Google Scholar 

  • Lan TQ, Lou H, Zhu JY (2013) Enzymatic saccharification of lignocelluloses should be conducted at elevated pH 5.2–6.2. Bioenerg Res 6(2):476–485

    CAS  Google Scholar 

  • Li Y, Ge X, Sun Z, Zhang J (2015) Effect of additives on adsorption and desorption behavior of xylanase on acid-insoluble lignin from corn stover and wheat straw. Bioresou Technol 186(55):316–320

    CAS  Google Scholar 

  • Li H, Xue Y, Wu J, Wu H, Qin G, Li C, Ding J, Liu J, Gan L, Long M (2016a) Enzymatic hydrolysis of hemicelluloses from Miscanthus to monosaccharides or xylo-oligosaccharides by recombinant hemicellulases. Ind Crop Prod 79:170–179

    CAS  Google Scholar 

  • Li Y, Qi B, Luo J, Wan Y (2016b) Effect of alkali lignins with different molecular weights from alkali pretreated rice straw hydrolyzate on enzymatic hydrolysis. Bioresour Technol 200:272–278

    CAS  PubMed  Google Scholar 

  • Liu J, Hu H, Gong Z, Yang G, Li R, Chen L, Huang L, Luo X (2019) Near-complete removal of non-cellulosic components from bamboo by 1-pentanol induced organosolv pretreatment under mild conditions for robust cellulose enzymatic hydrolysis. Cellulose 26(6):3801–3814

    CAS  Google Scholar 

  • Lou H, Zhu JY, Lan TQ, Lai H, Qiu X (2013) pH-Induced lignin surface modification to reduce nonspecific cellulase binding and enhance enzymatic saccharification of lignocelluloses. Chem Sus Chem 6(5):919–927

    CAS  Google Scholar 

  • Lu X, Zheng X, Li X, Zhao J (2016) Adsorption and mechanism of cellulase enzymes onto lignin isolated from corn stover pretreated with liquid hot water. Biotechnol Biofuels 9(1):118

    PubMed  PubMed Central  Google Scholar 

  • Mhlongo SI, Haan RD, Viljoen-Bloom M, Zyl WHV (2015) Lignocellulosic hydrolysate inhibitors selectively inhibit/deactivate cellulase performance. Enzym Microb Technol 81:16–22

    CAS  Google Scholar 

  • Nakagame S, Chandra R, Saddler J (2010) The effect of isolated lignins, obtained from a range of pretreated lignocellulosic substrates, on enzymatic hydrolysis. Biotechnol Bioeng 105(5):871–879

    CAS  PubMed  Google Scholar 

  • Nakagame S, Chandra RP, Kadla JF, Saddler JN (2011) The isolation, characterization and effect of lignin isolated from steam pretreated Douglas-fir on the enzymatic hydrolysis of cellulose. Bioresour Technol 102(6):4507–4517

    CAS  PubMed  Google Scholar 

  • Olivataravilla A, Tomáspejó E, Demuez M, Gonzálezfernández C, Ballesteros M (2016) Phenols and lignin: key players in reducing enzymatic hydrolysis yields of steam-pretreated biomass in presence of laccase. J Biotechnol 218:94–101

    CAS  Google Scholar 

  • Pan X (2008) Role of functional groups in lignin inhibition of enzymatic hydrolysis of cellulose to glucose. J Biobased Mater Bio 2(1):25–32

    Google Scholar 

  • Pareek N, Gillgren T, Jönsson LJ (2013) Adsorption of proteins involved in hydrolysis of lignocellulose on lignins and hemicelluloses. Bioresour Technol 148(7):70–77

    CAS  PubMed  Google Scholar 

  • Poutanen K, Puls J(1988). Characteristics of Trichoderma reesei β-xylosidase and its use in the hydrolysis of solubilized xylans. Appl Microbiol Biot28(4-5): 425-432

  • Rahikainen JL, Martin-Sampedro R, Heikkinen H, Rovio S, Marjamaa K, Tamminen T, Rojas OJ, Kruus K (2013) Inhibitory effect of lignin during cellulose bioconversion: the effect of lignin chemistry on non-productive enzyme adsorption. Bioresour Technol 133(2):270–278

    CAS  PubMed  Google Scholar 

  • Rakotoarivonina H, Hermant B, Aubry N, Rémond C (2015) Engineering the hydrophobic residues of a GH11 xylanase impacts its adsorption onto lignin and its thermostability. Enzym Microb Technol 81:47–55

    CAS  Google Scholar 

  • Ryan SE, Nolan K, Thompson RN, Gubitz GM, Savage AV, Tuohy MG (2003) Purification and characterization of a new low molecular weight endoxylanase from Penicillium capsulatum. Enzym Microb Technol 33(6):775–785

    CAS  Google Scholar 

  • Shuai L, Yang Q, Zhu JY, Lu FC, Weimer PJ, Ralph J, Pan XJ (2010) Comparative study of SPORL and dilute-acid pretreatments of spruce for cellulosic ethanol production. Bioresour Technol 101(9):3106–3114

    CAS  PubMed  Google Scholar 

  • Silveira MH, Morais AR, Da CLA, Olekszyszen DN, Bogel-Łukasik R, Andreaus J, Pereira RL (2015) Current pretreatment technologies for the development of cellulosic ethanol and biorefineries. Chem Sus Chem 8(20):3366–3390

    CAS  Google Scholar 

  • Sluiter A, Hanmes B, Ruiz R, Scarlata C, Sluiter J, Templeton D, Crocker D (2012) Determination of structural carbohydrates and lignin in biomass. Laboratory Analytical Procedure of National Renewable Energy Laboratory (NREL), Golden, Colorado

  • Tang P, Abdul P, Engliman N, Hassan O (2018) Effects of pretreatment and enzyme cocktail composition on the sugars production from oil palm empty fruit bunch fiber (OPEFBF). Cellulose 25(8):4677–4694

    CAS  Google Scholar 

  • Tenkanen M, Buchert J, Viikari L (1995) Binding of hemicellulases on isolated polysaccharide substrates. Enzym Microb Technol 17(6):499–505

    CAS  Google Scholar 

  • Tu M, Pan X, Saddler JN (2009) Adsorption of cellulase on cellulolytic enzyme lignin from Lodgepole Pine. J Agr Food Chem 57(17):7771–7778

    CAS  Google Scholar 

  • Wen JL, Xue BL, Xu F, Sun RC, Pinkert A (2013) Unmasking the structural features and property of lignin from bamboo. Ind Crop Prod 42:332–343

    CAS  Google Scholar 

  • Xin DL, Sun ZP, Viikari L, Zhang JH (2015) Role of hemicellulases in production of fermentable sugars from corn stover. Ind Crop Prod 74:209–217

    CAS  Google Scholar 

  • Xin D, Yang M, Chen X, Zhang J (2016a) The access of Trichoderma reesei 6A to cellulose is blocked by isolated hemicelluloses and their derivatives in biomass hydrolysis. RSC Adv 6(77):73859–73868

    CAS  Google Scholar 

  • Xin D, Yang M, Zhang Y, Zhang Y, Hou X, Wu J, Fan X, Wang J, Zhang J (2016b) Physicochemical characterization and enzymatic digestibility of Chinese pennisetum pretreated with 1-ethyl-3-methylimidazolium acetate at moderate temperatures. Renew Energ 91:409–416

    CAS  Google Scholar 

  • Yang M, Kuittinen S, Zhang J, Keinanen M, Pappinen A (2013) Effect of dilute acid pretreatment on the conversion of barley straw with grains to fermentable sugars. Bioresour Technol 146:444–450

    CAS  PubMed  Google Scholar 

  • Yu H, Hou J, Yu S, Liu S, Li L, Wu Q, Liu Y, Jiang J, Nie S (2019) Comprehensive understanding of the non-productive adsorption of cellulolytic enzymes onto lignins isolated from furfural residues. Cellulose 26(5):3111–3125

    CAS  Google Scholar 

  • Zhang JH, Viikari L (2012) Xylo-oligosaccharides are competitive inhibitors of cellobiohydrolase I from Thermoascus aurantiacus. Bioresour Technol 117(4):286–291

    CAS  PubMed  Google Scholar 

  • Zhang H, Wu S (2014) Dilute ammonia pretreatment of sugarcane bagasse followed by enzymatic hydrolysis to sugars. Cellulose 21(3):1341–1349

    CAS  Google Scholar 

  • Zhang HD, Wu SB (2015) Pretreatment of eucalyptus using subcritical CO2 for sugar production. J Chem Technol Biot 90(9):1640–1645

    CAS  Google Scholar 

  • Zhang JH, Moilanen U, Tang M, Viikari L (2013) The carbohydrate-binding module of xylanase from Nonomuraea flexuosa decreases its non-productive adsorption on lignin. Biotechnol Biofuels 6:18

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Wu S, Xie J (2017) Evaluation of the effects of isolated lignin on enzymatic hydrolysis of cellulose. Enzym Microb Technol 101:44–50

    CAS  Google Scholar 

  • Zhao XB, Zhang LH, Liu DH (2012) Biomass recalcitrance. Part I: the chemical compositions and physical structures affecting the enzymatic hydrolysis of lignocellulose. Biofuel Bioprod Bior 6(4):465–482

    CAS  Google Scholar 

  • Zilliox C, Debeire P (1998) Hydrolysis of wheat straw by a thermostable endoxylanase: adsorption and kinetic studies. Enzym Microb Technol 22(1):58–63

    CAS  Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China (No. 31670598 and No. 31270622) and the Science Foundation for Distinguished Young Scholars of Northwest A&F University, China (No. 2452015098).

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Authors and Affiliations

  1. College of Forestry, Northwest A&F University, No. 3 Taicheng Road, Yangling, 712100, China

    Xiang Chen, Donglin Xin & Junhua Zhang

  2. Key Laboratory of Carbohydrate Chemistry and Biotechnology Ministry of Education School of Biotechnology, Jiangnan University, Wuxi, 214122, China

    Fubao Fuelbiol Sun

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  1. Xiang Chen
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  2. Donglin Xin
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  4. Junhua Zhang
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Correspondence to Junhua Zhang.

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Chen, X., Xin, D., Sun, F.F. et al. Factors affecting the hydrolytic action of xylanase during pennisetum saccharification: role of lignin. Cellulose 27, 3143–3152 (2020). https://doi.org/10.1007/s10570-020-02996-z

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