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Compounds inhibiting the bioconversion of hydrothermally pretreated lignocellulose

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Abstract

Hydrothermal pretreatment using liquid hot water, steam explosion, or dilute acids enhances the enzymatic digestibility of cellulose by altering the chemical and/or physical structures of lignocellulosic biomass. However, compounds that inhibit both enzymes and microbial activity, including lignin-derived phenolics, soluble sugars, furan aldehydes, and weak acids, are also generated during pretreatment. Insoluble lignin, which predominantly remains within the pretreated solids, also acts as a significant inhibitor of cellulases during hydrolysis of cellulose. Exposed lignin, which is modified to be more recalcitrant to enzymes during pretreatment, adsorbs cellulase nonproductively and reduces the availability of active cellulase for hydrolysis of cellulose. Similarly, lignin-derived phenolics inhibit or deactivate cellulase and β-glucosidase via irreversible binding or precipitation. Meanwhile, the performance of fermenting microorganisms is negatively affected by phenolics, sugar degradation products, and weak acids. This review describes the current knowledge regarding the contributions of inhibitors present in whole pretreatment slurries to the enzymatic hydrolysis of cellulose and fermentation. Furthermore, we discuss various biological strategies to mitigate the effects of these inhibitors on enzymatic and microbial activity to improve the lignocellulose-to-biofuel process robustness. While the inhibitory effect of lignin on enzymes can be relieved through the use of lignin blockers and by genetically engineering the structure of lignin or of cellulase itself, soluble inhibitors, including phenolics, furan aldehydes, and weak acids, can be detoxified by microorganisms or laccase.

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References

  • Adeboye PT, Bettiga M, Olsson L (2014) The chemical nature of phenolic compounds determines their toxicity and induces distinct physiological responses in Saccharomyces cerevisiae in lignocellulose hydrolysates. AMB Express 4:46

    PubMed Central  PubMed  Google Scholar 

  • Allen SA, Clark W, McCaffery JM, Cai Z, Lanctot A, Slininger PJ, Liu ZL, Gorsich SW (2010) Furfural induces reactive oxygen species accumulation and cellular damage in Saccharomyces cerevisiae. Biotechnol Biofuels 3:2

    PubMed Central  PubMed  Google Scholar 

  • Almeida JRM, Modig T, Petersson A, Hahn-Hägerdal B, Lidén G, Gorwa-Grauslund MF (2007) Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae. J Chem Technol Biotechnol 82:340–349

    CAS  Google Scholar 

  • 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 101:4851–4861

    CAS  PubMed  Google Scholar 

  • Ask M, Bettiga M, Mapelli V, Olsson L (2013) The influence of HMF and furfural on redox-balance and energy-state of xylose-utilizing Saccharomyces cerevisiae. Biotechnol Biofuels 6:22

    PubMed Central  CAS  PubMed  Google Scholar 

  • Avellar BK, Glasser WG (1998) Steam-assisted biomass fractionation. I. Process considerations and economic evaluation. Biomass Bioenergy 14:205–218

    CAS  Google Scholar 

  • Banerjee N, Bhatnagar R, Viswanathan L (1981) Inhibition of glycolysis by furfural in Saccharomyces cerevisiae. Eur J Appl Microbiol Biotechnol 11:226–228

    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 125:198–209

    CAS  PubMed  Google Scholar 

  • Bernardez TD, Lyford K, Hogsett DA, Lynd LR (1993) Adsorption of Clostridium thermocellum cellulases onto pretreated mixed hardwood, avicel, and lignin. Biotechnol Bioeng 42:899–907

    CAS  PubMed  Google Scholar 

  • Bonawitz ND, Kim JI, Tobimatsu Y, Ciesielski PN, Anderson NA, Ximenes E, Maeda J, Ralph J, Donohoe BS, Ladisch M, Chapple C (2014) Disruption of mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant. Nature 509:376–380

    CAS  PubMed  Google Scholar 

  • Brownell HH, Yu EKC, Saddler JN (1986) Steam explosion pretreatment of wood: effect of chip size, acid, moisture content, and pressure drop. Biotechnol Bioeng 28:792–801

    CAS  PubMed  Google Scholar 

  • Cantarella M, Cantarella L, Gallifuoco A, Spera A, Alfani F (2004) Effect of inhibitors released during steam-explosion treatment of poplar wood on subsequent enzymatic hydrolysis and SSF. Biotechnol Prog 20:200–206

    CAS  PubMed  Google Scholar 

  • Cao G, Ximenes E, Nichols NN, Zhang L, Ladisch M (2013) Biological abatement of cellulase inhibitors. Bioresour Technol 146:604–610

    CAS  PubMed  Google Scholar 

  • Carvalheiro F, Silva-Fernandes T, Duarte LC, Gírio FM (2009) Wheat straw autohydrolysis: process optimization and products characterization. Appl Biochem Biotechnol 153:84–93

    CAS  PubMed  Google Scholar 

  • Casey E, Sedlak M, Ho MW, Mosier NS (2010) Effect of acetic acid and pH on the cofermentation of glucose and xylose to ethanol by a genetically engineered strain of Saccharomyces cerevisiae. FEMS Yeast Res 10:385–393

    CAS  PubMed  Google Scholar 

  • Chang VS, Holtzapple MT (2000) Fundamental factors affecting biomass enzymatic reactivity. Appl Biochem Biotechnol 84–86:5–37

    PubMed  Google Scholar 

  • Chapple C, Ladisch M, Melilan R (2007) Loosening lignin’s grip on biofuel production. Nat Biotechnol 25:746–748

    CAS  PubMed  Google Scholar 

  • Chen F, Dixon RA (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol 25:759–761

    CAS  PubMed  Google Scholar 

  • Chua MGS, Wayman M (1979a) Characterization of autohydrolysis aspen (P. tremuloides) lignins. Part 1. Composition and molecular weight distribution of extracted autohydrolysis lignin. Can J Chem 57:1141–1149

    CAS  Google Scholar 

  • Chua MGS, Wayman M (1979b) Characterization of autohydrolysis aspen (P. tremuloides) lignins. Part 3. Infrared and ultraviolet studies of extracted autohydrolysis lignin. Can J Chem 57:2603–2611

    CAS  Google Scholar 

  • Ciesielski PN, Resch MG, Hewetson B, Killgore JP, Curtin A, Anderson N, Chiaramonti AN, Hurley DC, Sanders A, Himmel ME, Chapple C, Mosier N, Donohoe BS (2014) Engineering plant cell walls: tuning lignin monomer composition for deconstructable biofuel feedstocks or resilient biomaterials. Green Chem 16:2627–2635

    CAS  Google Scholar 

  • Clark TA, Mackie KL (1984) Fermentation inhibitors in wood hydrolysates derived from the softwood Pinus radiata. J Chem Technol Biotechnol 34:101–110

    Google Scholar 

  • Converti A, Domínguez JM, Perego P, da Silva SS, Zilli M (2000) Wood hydrolysis and hydrolyzate detoxification for subsequent xylitol production. Chem Eng Technol 23:1013–1020

    CAS  Google Scholar 

  • Dekker RFH (1988) Inhibitors of Trichoderma reesei β-glucosidase activity derived from auto-hydrolysis-exploded Eucalyptous regnans. Appl Microbiol Biotechnol 29:593–598

    Google Scholar 

  • Delgenes JP, Moletta R, Navarro JM (1996) Effects of lignocellulose degradation products on ethanol fermentations of glucose and xylose by Saccharomyces cerevisiae, Zymomonas mobilis, Pichia stipitis, and Candida shehatae. Enzym Microb Technol 19:220–225

    CAS  Google Scholar 

  • Dunlop A (1948) Furfural formation and behavior. Ind Eng Chem 40:204–209

    CAS  Google Scholar 

  • Eriksson T, Börjesson J, Tjerneld F (2002) Mechanism of surfactant effect in enzymatic hydrolysis of lignocelluloses. Enzym Microb Technol 31:353–364

    CAS  Google Scholar 

  • Excoffier G, Toussaint B, Vignon MR (1991) Saccharification of steam-exploded poplar wood. Biotechnol Bioeng 38:1308–1317

    CAS  PubMed  Google Scholar 

  • Fu C, Mielenz JR, Xiao X, Ge Y, Hamilton CY, Rodriguez M, Chen F, Foston M, Ragauskas A, Bouton J, Dixon RA, Wang Z-Y (2011) Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass. Proc Natl Acad Sci U S A 108:3803–3808

    PubMed Central  CAS  PubMed  Google Scholar 

  • García-Aparicio MP, Ballesteros I, González A, Oliva JM, Ballesteros M, Negro MJ (2006) Effect of inhibitors released during steam-explosion pretreatment of barley straw on enzymatic hydrolysis. Appl Biochem Biotechnol 129–132:278–288

    PubMed  Google Scholar 

  • Gellerstedt G, Henriksson G (2008) Lignins: major sources, structure and properties. In: Belgacem M, Gandini A (eds) Monomers, polymers and composites from renewable resources. Wiley, Amsterdam, pp 201–224

    Google Scholar 

  • Gong CS, Ladisch MR, Tsao GT (1977) Cellobiase from Trichoderma viride: purification properties, kinetics, and mechanism. Biotechnol Bioeng 19:958–981

    Google Scholar 

  • Grant TM, King CJ (1990) Mechanism of irreversible adsorption of phenolic compounds by activated carbons. Ind Eng Chem Res 29:264–271

    CAS  Google Scholar 

  • Gurram RN, Datta S, Lin YJ, Snyder SW, Menkhaus TJ (2011) Removal of enzymatic and fermentation inhibitory compounds from biomass slurries for enhanced biorefinery process efficiencies. Bioresour Technol 102:7850–7859

    CAS  PubMed  Google Scholar 

  • Gusakov AV, Sinitsyn AP (1992) A theoretical analysis of cellulase product inhibition: effect of cellulase binding constant, enzyme/substrate ratio, and beta-glucosidase activity on the inhibition pattern. Biotechnol Bioeng 40:663–671

    CAS  PubMed  Google Scholar 

  • Han Y, Chen H (2010) Synergism between hydrophobic proteins of corn stover and cellulase in lignocellulose hydrolysis. Biochem Eng J 48:218–224

    CAS  Google Scholar 

  • Hasunuma T, Sanda T, Yamada R, Yoshimura K, Ishii J, Kondo A (2011) Metabolic pathway engineering based on metabolomics confers acetic and formic acid tolerance to a recombinant xylose-fermenting strain of Saccharomyces cerevisiae. Microb Cell Factories 10:2

    CAS  Google Scholar 

  • Heer D, Heine D, Sauer U (2009) Resistance of Saccharomyces cerevisiae to high concentrations of furfural is based on NADPH-dependent reduction by at least two oxireductases. Appl Environ Microbiol 75:7631–7638

    PubMed Central  CAS  PubMed  Google Scholar 

  • Heipieper HJ, Weber FJ, Sikkema J, Keweloh H, De Bont JAM (1994) Mechanisms of resistance of whole cells to toxic organic solvents. Trends Biotechnol 12:409–415

    CAS  Google Scholar 

  • Holtzapple M, Cognata M, Shu Y, Hendrickson C (1990) Inhibition of Trichoderma reesei cellulase by sugars and solvents. Biotechnol Bioeng 36:275–287

    CAS  PubMed  Google Scholar 

  • Hong J, Ladisch MR, Gong CS, Wankat PC, Tsao GT (1981) Combined product and substrate inhibition equation for cellobiase. Biotechnol Bioeng 23:2779–2788

    CAS  Google Scholar 

  • Hu F, Jung S, Ragauskas A (2012) Pseudo-lignin formation and its impact on enzymatic hydrolysis. Bioresour Technol 117:7–12

    CAS  PubMed  Google Scholar 

  • Imai T, Ohno T (1995) The relationship between viability and intracellular pH in the yeast Saccharomyces cerevisiae. Appl Environ Microbiol 61:3604–3608

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jönsson LJ, Palmqvist E, Nilvebrant NO, Hahn-Hägerdal B (1998) Detoxification of wood hydrolysates with laccase and peroxidase from the white-rot fungus Trametes versicolor. Appl Microbiol Biotechnol 49:691–697

    Google Scholar 

  • Jönsson LJ, Alriksson B, Nilvebrant NO (2013) Bioconversion of lignocellulose: inhibitors and detoxification. Biotechnol Biofuels 6:16

    PubMed Central  PubMed  Google Scholar 

  • Jung YH, Kim IJ, Kim HK, Kim KH (2013) Dilute acid pretreatment of lignocellulose for whole slurry ethanol fermentation. Bioresour Technol 132:109–114

    CAS  PubMed  Google Scholar 

  • Jung YH, Kim IJ, Kim HK, Kim KH (2014) Whole slurry fermentation of maleic acid-pretreated oil palm empty fruit bunches for ethanol production not necessitating a detoxification process. Bioprocess Biosyst Eng 37:659–665

    CAS  PubMed  Google Scholar 

  • Keller FA, Bates D, Ruiz R, Nguyen Q (1998) Yeast adaptation on softwood prehydrolysate. Appl Biochem Biotechnol 70–72:137–148

    PubMed  Google Scholar 

  • Kim ES, Lee HJ, Bang WG, Choi IG, Kim KH (2009a) Functional characterization of a bacterial expansin from Bacillus subtilis for enhanced enzymatic hydrolysis of cellulose. Biotechnol Bioeng 102:1342–1353

    CAS  PubMed  Google Scholar 

  • Kim Y, Mosier NS, Ladisch MR (2009b) Enzymatic digestion of liquid hot water pretreated hybrid poplar. Biotechnol Prog 25:340–348

    CAS  PubMed  Google Scholar 

  • Kim Y, Ximenes E, Mosier NS, Ladisch MR (2011) Soluble inhibitors/deactivators of cellulase enzymes from lignocellulosic biomass. Enzym Microb Technol 48:408–415

    CAS  Google Scholar 

  • Kim IJ, Ko HJ, Kim TW, Nam KH, Choi IG, Kim KH (2013a) Binding characteristics of a bacterial expansin (BsEXLX1) for various types of pretreated lignocellulose. Appl Microbiol Biotechnol 97:5381–5388

    CAS  PubMed  Google Scholar 

  • Kim Y, Kreke T, Mosier NS, Ladisch MR (2013b) Severity factor coefficients for subcritical liquid hot water pretreatment of hardwood chips. Biotechnol Bioeng 111:254–263

    PubMed  Google Scholar 

  • Kim Y, Kreke T, Hendrickson R, Parenti J, Ladisch MR (2013c) Fractionation of cellulase and fermentation inhibitors from steam pretreated mixed hardwood. Bioresour Technol 135:30–38

    CAS  PubMed  Google Scholar 

  • Kim Y, Kreke T, Ko JK, Ladisch MR (2015) Hydrolysis-determining substrate characteristics in liquid hot water pretreated hardwood. Biotechnol Bioeng 112:677–687

    CAS  PubMed  Google Scholar 

  • Klein-Marcuschamer D, Oleskowicz-Popiel P, Simmons BA, Blanch HW (2012) The challenge of enzyme cost in the production of lignocellulosic biofuels. Biotechnol Bioeng 109:1083–1087

    CAS  PubMed  Google Scholar 

  • Klinke HB, Thomsen AB, Ahring BK (2004) Inhibition of ethanol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass. Appl Microbiol Biotechnol 66:10–26

    CAS  PubMed  Google Scholar 

  • Ko JK, Kim Y, Ximenes E, Ladisch MR (2015a) Effect of liquid hot water pretreatment severity on properties of hardwood lignin and enzymatic hydrolysis of cellulose. Biotechnol Bioeng 112:252–262

    CAS  PubMed  Google Scholar 

  • Ko JK, Ximenes E, Kim Y, Ladisch MR (2015b) Adsorption of enzyme onto lignins of liquid hot water pretreated hardwoods. Biotechnol Bioeng 112:447–456

    CAS  PubMed  Google Scholar 

  • Kumar R, Wyman CE (2009) Effect of xylanase supplementation of cellulase on digestion of corn stover solids prepared by leading pretreatment technologies. Bioresour Technol 100:4203–4213

  • Kumar P, Barrett DM, Delwiche MJ, Stroeve P (2009) Methods for pretreatment of lignocellulosic biomass for efficient hydrolysis and biofuel production. Ind Eng Chem Res 48:3713–3729

    CAS  Google Scholar 

  • Kumar L, Arantes V, Chandra R, Saddler J (2012) The lignin present in steam pretreated softwood binds enzymes and limits cellulose accessibility. Bioresour Technol 103:201–208

    CAS  PubMed  Google Scholar 

  • Langmuir I (1918) The adsorption of gases on plane surfaces of glass, mica and platinum. J Am Chem Soc 40:1361–1403

    CAS  Google Scholar 

  • Larsson S, Palmqvist E, Hahn-Hägerdal B, Tengborg C, Stenberg K, Zacchi G, Nilvebrant NO (1999a) The generation of fermentation inhibitors during dilute acid hydrolysis of softwood. Enzym Microb Technol 24:151–159

    CAS  Google Scholar 

  • Larsson S, Reimann A, Nilvebrant N, Jönsson LJ (1999b) Comparison of different methods for the detoxification of lignocellulose hydrolyzates of spruce. Appl Biochem Biotechnol 77–79:91–103

    Google Scholar 

  • Larsson S, Quintana-Sáinz A, Reimann A, Nilvebrant NO, Jönsson LJ (2000) Influence of lignocellulose-derived aromatic compounds on oxygen-limited growth and ethanolic fermentation by Saccharomyces cerevisiae. Appl Biochem Biotechnol 84–86:617–632

    PubMed  Google Scholar 

  • Larsson S, Cassland P, Jönsson LJ (2001) Development of a Saccharomyces cerevisiae strain with enhanced resistance to phenolic fermentation inhibitors in lignocellulose hydrolysates by heterologous expression of laccase. Appl Environ Microbiol 67:1163–1170

    PubMed Central  CAS  PubMed  Google Scholar 

  • Li J, Henriksson G, Gellerstedt G (2007) Lignin depolymerization/repolymerization and its critical role for delignification of aspen wood by steam explosion. Bioresour Technol 98:3061–3068

    CAS  PubMed  Google Scholar 

  • Li X, Ximenes E, Kim Y, Slininger M, Meilan R, Ladisch MR, Chapple C (2010) Lignin monomer composition affects Arabidopsis cell-wall degradability after liquid hot water pretreatment. Biotechnol Biofuels 3:27

    PubMed Central  CAS  PubMed  Google Scholar 

  • Liu ZL, Slininger PJ, Gorsich SW (2005) Enhanced biotransformation of furfural and hydroxymethylfurfural by newly developed ethanologenic yeast strains. Appl Biochem Biotechnol 121–124:451–460

    PubMed  Google Scholar 

  • Liu ZL, Moon J, Andersh BJ, Slininger PJ, Weber S (2008) Multiple gene-mediated NAD(P)H-dependent aldehyde reduction is a mechanism of in situ detoxification of furfural and 5-hydroxy methylfurfural by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 81:743–753

    CAS  PubMed  Google Scholar 

  • López MJ, Nichols NN, Dien BS, Moreno J, Bothast RJ (2004) Isolation of microorganisms for biological detoxification of lignocellulosic hydrolysates. Appl Microbiol Biotechnol 64:125–131

    PubMed  Google Scholar 

  • Lu Y, Warner R, Sedlak M, Ho N, Mosier NS (2009) Comparison of glucose/xylose cofermentation of poplar hydrolysates processed by different pretreatment technologies. Biotechnol Prog 25:349–356

    CAS  PubMed  Google Scholar 

  • Lück E, Jager M (1997) Antimicrobial food additives: characteristics, uses, effects. Springer, New York

    Google Scholar 

  • Mandels M, Reese ET (1965) Inhibition of cellulases. Annu Rev Phytopathol 3:85–102

    CAS  Google Scholar 

  • Mansfield SD, Kang KY, Chapple C (2012) Designed for deconstruction–poplar trees altered in cell wall lignification improve the efficacy of bioethanol production. New Phytol 194:91–101

    CAS  PubMed  Google Scholar 

  • Modig T, Lidén G, Taherzadeh MJ (2002) Inhibition effects of furfural on alcohol dehydrogenase, aldehyde dehydrogenase and pyruvate dehydrogenase. Biochem J 363:769–776

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mosier N, Wyman C, Dale B, Elander R, Lee YY, Holtzapple M, Ladisch M (2005) Features of promising technologies for pretreatment of lignocellulosic biomass. Bioresour Technol 96:673–686

    CAS  PubMed  Google Scholar 

  • Mussatto SI, Roberto IC (2004) Alternatives for detoxification of diluted-acid lignocellulosic hydrolyzates for use in fermentative processes: a review. Bioresour Technol 93:1–10

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Nakagame S, Chandra RP, Saddler JN (2011b) The influence of lignin on the enzymatic hydrolysis of pretreated biomass substrates. In: Zhu JY, Zhang X, Pan XJ (eds) Sustainable production of fuels, chemicals, and fibers from forest biomass. American Chemical Society, Washington DC, pp 145–167

    Google Scholar 

  • Nevoigt E (2008) Progress in metabolic engineering of Saccharomyces cerevisiae. Microbiol Mol Biol Rev 72:379–412

  • Nichols NN, Sharma LN, Mowery RA, Chambliss CK, van Walsum GP, Dien BS, Iten LB (2008) Fungal metabolism of fermentation inhibitors present in corn stover dilute acid hydrolysate. Enzym Microb Technol 42:624–630

    CAS  Google Scholar 

  • Nordwald EM, Brunecky R, Himmel ME, Beckham GT, Kaar JL (2014) Charge engineering of cellulases improves ionic liquid tolerance and reduces lignin inhibition. Biotechnol Bioeng 111:1541–1549

    CAS  PubMed  Google Scholar 

  • Obst JR (1982) Guaiacyl and syringyl lignin composition in hardwood cell components. Holzforschung 36:143–152

    CAS  Google Scholar 

  • Oliva JM, Sáez F, Ballesteros I, González A, Negro MJ, Manzanares P, Ballesteros M (2003) Effect of lignocellulosic degradation compounds from steam explosion pretreatment on ethanol fermentation by thermotolerant yeast Kluyveromyces marxianus. Appl Biochem Biotechnol 105–108:141–153

    PubMed  Google Scholar 

  • Olsson L, Hahn-Hägerdal B (1996) Fermentation of lignocellulosic hydrolysates for ethanol production. Enzym Microb Technol 18:312–331

    CAS  Google Scholar 

  • Palmqvist E, Hahn-Hägerdal B (2000) Fermentation of lignocellulosic hydrolysates. II: inhibitors and mechanisms of inhibition. Bioresour Technol 74:25–33

    CAS  Google Scholar 

  • Palmqvist E, Hahn-Hägerdal B, Szengyel Z, Zacchi G, Rèczey K (1997) Simultaneous detoxification and enzyme production of hemicellulose hydrolysates obtained after steam pretreatment. Enzym Microb Technol 20:286–293

    CAS  Google Scholar 

  • Palmqvist E, Almeida JS, Hahn-Hägerdal B (1999) Influence of furfural on anaerobic glycolytic kinetics of Saccharomyces cerevisiae in batch culture. Biotechnol Bioeng 62:447–454

    CAS  PubMed  Google Scholar 

  • Pampulha ME, Loureiro-Dias MC (1989) Combined effect of acetic acid, pH and ethanol on intracellular pH of fermenting yeast. Appl Microbiol Biotechnol 31:547–550

    CAS  Google Scholar 

  • Parawira W, Tekere M (2011) Biotechnological strategies to overcome inhibitors in lignocellulose hydrolysates for ethanol production: review. Crit Rev Biotechnol 31:20–31

    CAS  PubMed  Google Scholar 

  • Pereira S, Ivanuša Š, Evtuguin DV, Serafim LS, Xavier AMRB (2012) Biological treatment of eucalypt spent sulphite liquors: a way to boost the production of second generation bioethanol. Bioresour Technol 103:131–135

    CAS  PubMed  Google Scholar 

  • Philippidis GP, Smith TK, Wyman CE (1993) Study of the enzymatic hydrolysis of cellulose for production of fuel ethanol by the simultaneous saccharification and fermentation process. Biotechnol Bioeng 41:846–853

    CAS  PubMed  Google Scholar 

  • Pu Y, Hu F, Huang F, Davison BH, Ragauskas AJ (2013) Assessing the molecular structure basis for biomass recalcitrance during dilute acid and hydrothermal pretreatments. Biotechnol Biofuels 6:15

    PubMed Central  CAS  PubMed  Google Scholar 

  • Qing Q, Wyman CE (2011) Supplementation with xylanase and β-xylosidase to reduce xylo-oligomer and xylan inhibition of enzymatic hydrolysis of cellulose and pretreated corn stover. Biotechnol Biofuels 4:1

    Google Scholar 

  • Qing Q, Yang B, Wyman CE (2010) Xylooligomers are strong inhibitors of cellulose hydrolysis by enzymes. Bioresour Technol 101:9624–9630

    CAS  PubMed  Google Scholar 

  • Rahikainen J, Mikander S, Marjamaa K, Tamminen T, Lappas A, Viikari L, Kruus K (2011) Inhibition of enzymatic hydrolysis by residual lignins from softwood–study of enzyme binding and inactivation on lignin-rich surface. Biotechnol Bioeng 108:2823–2834

    CAS  PubMed  Google Scholar 

  • Sanchez B, Bautista J (1988) Effects of furfural and 5-hydroxymethylfurfural on the fermentation of Saccharomyces cerevisiae and biomass production from Candida guilliermondii. Enzym Microb Technol 10:315–318

    CAS  Google Scholar 

  • Sannigrahi P, Ragauskus AJ, Miller SJ (2008) Effects of two-stage dilute acid pretreatment on the structure and composition of lignin and cellulose in loblolly pine. Bioenerg Res 1:205–214

    Google Scholar 

  • Sipos B, Dienes D, Schleicher Á, Perazzini R, Crestini C, Siika-aho M, Réczey K (2010) Hydrolysis efficiency and enzyme adsorption on steam-pretreated spruce in the presence of poly(ethylene glycol). Enzym Microb Technol 47:84–90

    CAS  Google Scholar 

  • Tejirian A, Xu F (2011) Inhibition of enzymatic cellulolysis by phenolic compounds. Enzym Microb Technol 48:239–247

    CAS  Google Scholar 

  • Tengborg C, Stenberg K, Galbe M, Zacchi G, Larsson S, Palmqvist E, Hahn-Hägerdal B (1998) Comparison of SO2 and H2SO4 impregnation of softwood prior to steam pretreatment on ethanol production. Appl Biochem Biotechnol 70–72:3–15

    Google Scholar 

  • Tengborg C, Galbe M, Zacchi G (2001) Reduced inhibition of enzymatic hydrolysis of steam-pretreated softwood. Enzym Microb Technol 28:835–844

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ulbricht RJ, Sharon J, Thomas JA (1984) A review of 5-hydroxymethylfurfural (HMF) in parental solutions. Fundam Appl Toxicol 4:843–853

    CAS  PubMed  Google Scholar 

  • Verduyn C, Postma E, Scheffers WA, van Dijken JP (1990) Energetics of Saccharomyces cerevisiae in anaerobic glucose-limited chemostat cultures. J Gen Microbiol 136:405–412

    CAS  PubMed  Google Scholar 

  • Wei N, Quarterman J, Kim SR, Cate JH, Jin YS (2013) Enhanced biofuel production through coupled acetic acid and xylose consumption by engineered yeast. Nat Commun 4:2580

    PubMed  Google Scholar 

  • Wyman CE, Dale BE, Elander RT, Holtzapple M, Ladisch MR, Lee YY, Mitchinson C, Saddler JN (2009) Comparative sugar recovery and fermentation data following pretreatment of poplar wood by leading technologies. Biotechnol Prog 25:333–339

    CAS  PubMed  Google Scholar 

  • Ximenes E, Kim Y, Mosier N, Dien B, Ladisch M (2010) Inhibition of cellulases by phenols. Enzym Microb Technol 46:170–176

    CAS  Google Scholar 

  • Ximenes E, Kim Y, Mosier N, Dien B, Ladisch M (2011) Deactivation of cellulases by phenols. Enzym Microb Technol 48:54–60

    CAS  Google Scholar 

  • Yang B, Wyman CE (2006) BSA treatment to enhance enzymatic hydrolysis of cellulose in lignin containing substrates. Biotechnol Bioeng 94:611–617

    CAS  PubMed  Google Scholar 

  • Yang B, Wyman CE (2013) Lignin blockers and uses thereof. US Patent 8,580,541

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Acknowledgments

This work was supported by grants from the National Research Foundation of Korea (2013M1A2A2072597), funded through the Korean Government (MSIP). Experiments were performed at the Korea University Food Safety Hall for the Institute of Biomedical Science and Food Safety.

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Authors and Affiliations

  1. Clean Energy Research Center, Korea Institute of Science and Technology, Seoul, 136-791, Republic of Korea

    Ja Kyong Ko & Youngsoon Um

  2. Department of Bio and Fermentation Convergence Technology, Kookmin University, Seoul, 136-702, Republic of Korea

    Yong-Cheol Park

  3. Department of Agricultural Biotechnology and Center for Food and Bioconvergence, Seoul National University, Seoul, 151-921, Republic of Korea

    Jin-Ho Seo

  4. Department of Biotechnology, Korea University Graduate School, Seoul, 136-713, Republic of Korea

    Kyoung Heon Kim

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  5. Kyoung Heon Kim
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Correspondence to Kyoung Heon Kim.

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Ko, J.K., Um, Y., Park, YC. et al. Compounds inhibiting the bioconversion of hydrothermally pretreated lignocellulose. Appl Microbiol Biotechnol 99, 4201–4212 (2015). https://doi.org/10.1007/s00253-015-6595-0

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  • DOI: https://doi.org/10.1007/s00253-015-6595-0

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