Skip to main content
Log in

By-products resulting from lignocellulose pretreatment and their inhibitory effect on fermentations for (bio)chemicals and fuels

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Lignocellulose might become an important feedstock for the future development of the biobased economy. Although up to 75 % of the lignocellulose dry weight consists of sugar, it is present in a polymerized state and cannot be used directly in most fermentation processes for the production of chemicals and fuels. Several methods have been developed to depolymerize the sugars present in lignocellulose, making the sugars available for fermentation. In this review, we describe five different pretreatment methods and their effect on the sugar and non-sugar fraction of lignocellulose. For several pretreatment methods and different types of lignocellulosic biomass, an overview is given of by-products formed. Most unwanted by-products present after pretreatment are dehydrated sugar monomers (furans), degraded lignin polymers (phenols) and small organic acids. Qualitative and quantitative effects of these by-products on fermentation processes have been studied. We conclude this review by giving an overview of techniques and methods to decrease inhibitory effects of unwanted by-products.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

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

    PubMed Central  PubMed  Google Scholar 

  • Almario MP, Reyes LH, Kao KC (2013) Evolutionary engineering of Saccharomyces cerevisiae for enhanced tolerance to hydrolysates of lignocellulosic biomass. Biotechnol Bioeng 110:2616–2623. doi:10.1002/bit.24938

    CAS  PubMed  Google Scholar 

  • Ando S, Arai I, Kiyoto K, Hanai S (1986) Identification of aromatic monomers in steam-exploded poplar and their influences on ethanol fermentation by Saccharomyces cerevisiae. J Ferment Technol 64:567–570

    CAS  Google Scholar 

  • Axe DD, Bailey JE (1995) Transport of lactate and acetate through the energized cytoplasmic membrane of Escherichia coli. Biotechnol Bioeng 47:8–19. doi:10.1002/bit.260470103

    CAS  PubMed  Google Scholar 

  • Balan V, Sousa LC, Chundawat SPS, Marshall D, Sharma LN, Chambliss CK, Dale BE (2009) Enzymatic digestibility and pretreatment degradation products of AFEX-treated hardwoods (Populus nigra). Biotechnol Prog 25:365–375. doi:10.1002/btpr.160

    CAS  PubMed  Google Scholar 

  • Banerjee N, Bhatnagar R, Viswanathan L (1981) Inhibition of glycolysis by furfural in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 11:226–228. doi:10.1007/bf00505872

    CAS  Google Scholar 

  • Bellido C, Bolado S, Coca M, Lucas S, González-Benito G, García-Cubero MT (2011) Effect of inhibitors formed during wheat straw pretreatment on ethanol fermentation by Pichia stipitis. Bioresour Technol 102:10868–10874. doi:10.1016/j.biortech.2011.08.128

    CAS  PubMed  Google Scholar 

  • Bjerre AB, Olesen AB, Fernqvist T, Plöger A, Schmidt AS (1996) Pretreatment of wheat straw using combined wet oxidation and alkaline hydrolysis resulting in convertible cellulose and hemicellulose. Biotechnol Bioeng 49:568–577. doi:10.1002/(SICI)1097-0290(19960305)49:5%3C568::AID-BIT10%3E3.0.CO;2-6

  • Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546. doi:10.1146/annurev.arplant.54.031902.134938

    CAS  PubMed  Google Scholar 

  • Boopathy R, Bokang H, Daniels L (1993) Biotransformation of furfural and 5-hydroxymethyl furfural by enteric bacteria. J Ind Microbiol 11:147–150. doi:10.1007/bf01583715

    CAS  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. doi:10.1021/bp0257978

    CAS  PubMed  Google Scholar 

  • Carter B, Gilcrease PC, Menkhaus TJ (2011) Removal and recovery of furfural, 5-hydroxymethylfurfural, and acetic acid from aqueous solutions using a soluble polyelectrolyte. Biotechnol Bioeng 108:2046–2052. doi:10.1002/bit.23153

    CAS  PubMed  Google Scholar 

  • Chandel AK, Kapoor RK, Singh A, Kuhad RC (2007) Detoxification of sugarcane bagasse hydrolysate improves ethanol production by Candida shehatae NCIM 3501. Bioresour Technol 98:1947–1950

    CAS  PubMed  Google Scholar 

  • Chang V, Holtzapple M (2000) Fundamental factors affecting biomass enzymatic reactivity. Appl Biochem Biotechnol 84–86:5–37. doi:10.1385/abab:84-86:1-9:5

    PubMed  Google Scholar 

  • Chen S-F, Mowery RA, Castleberry VA, Walsum GP, Chambliss CK (2006) High-performance liquid chromatography method for simultaneous determination of aliphatic acid, aromatic acid and neutral degradation products in biomass pretreatment hydrolysates. J Chromatogr A 1104:54–61

    CAS  PubMed  Google Scholar 

  • Chundawat SPS, Vismeh R, Sharma LN, Humpala JF, da Costa Sousa L, Jones AD, Balan V, Dale BE (2010) Multifaceted characterization of cell wall decomposition products formed during ammonia fiber expansion (AFEX) and dilute acid based pretreatments. Bioresour Technol 101:8429–8438

    CAS  PubMed  Google Scholar 

  • Claassen PAM, van Lier JB, Lopez Contreras AM, van Niel EWJ, Sijtsma L, Stams AJM, de Vries SS, Weusthuis RA (1999) Utilisation of biomass for the supply of energy carriers. Appl Microbiol Biotechnol 52:741–755. doi:10.1007/s002530051586

    CAS  Google Scholar 

  • Converti A, Perego P, Domínguez J (1999) Xylitol production from hardwood hemicellulose hydrolysates by Pachysolen tannophilus, Debaryomyces hansenii, and Candida guilliermondii. Appl Biochem Biotechnol 82:141–151. doi:10.1385/abab:82:2:141

    CAS  Google Scholar 

  • Dale BE, Leong CK, Pham TK, Esquivel VM, Rios I, Latimer VM (1996) Hydrolysis of lignocellulosics at low enzyme levels: application of the AFEX process. Bioresour Technol 56:111–116

    CAS  Google Scholar 

  • de Vrije T, de Haas GG, Tan GB, Keijsers ERP, Claassen PAM (2002) Pretreatment of Miscanthus for hydrogen production by Thermotoga elfii. Int J Hydrog Energy 27:1381–1390. doi:10.1016/S0360-3199(02)00124-6

    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. doi:10.1016/0141-0229(95)00237-5

    CAS  Google Scholar 

  • Dong H-W, Fan L-Q, Luo Z, Zhong J-J, Ryu DDY, Bao J (2013) Improvement of ethanol productivity and energy efficiency by degradation of inhibitors using recombinant Zymomonas mobilis (pHW20a-fdh). Biotechnol Bioeng 110:2395–2404. doi:10.1002/bit.24897

    CAS  PubMed  Google Scholar 

  • Du B, Sharma LN, Becker C, Chen S-F, Mowery RA, van Walsum GP, Chambliss CK (2010) Effect of varying feedstock–pretreatment chemistry combinations on the formation and accumulation of potentially inhibitory degradation products in biomass hydrolysates. Biotechnol Bioeng 107:430–440. doi:10.1002/bit.22829

    CAS  PubMed  Google Scholar 

  • Eggeman T, Elander RT (2005) Process and economic analysis of pretreatment technologies. Bioresour Technol 96:2019–2025. doi:10.1016/j.biortech.2005.01.017

    CAS  PubMed  Google Scholar 

  • Endo A, Nakamura T, Ando A, Tokuyasu K, Shima J (2008) Genome-wide screening of the genes required for tolerance to vanillin, which is a potential inhibitor of bioethanol fermentation, in Saccharomyces cerevisiae. Biotechnol Biofuels 1:3. doi:10.1186/1754-6834-1-3

    PubMed Central  PubMed  Google Scholar 

  • Fengel D, Wegener G (1983) Wood: chemistry, ultrastructure, reactions. De Gruyter, Berlin

    Google Scholar 

  • Feron VJ, Til HP, de Vrijer F, Woutersen RA, Cassee FR, van Bladeren PJ (1991) Aldehydes: occurrence, carcinogenic potential, mechanism of action and risk assessment. Mutat Res Genet Toxicol 259:363–385. doi:10.1016/0165-1218(91)90128-9

    CAS  Google Scholar 

  • Fitzgerald DJ, Stratford M, Gasson MJ, Ueckert J, Bos A, Narbad A (2004) Mode of antimicrobial action of vanillin against Escherichia coli, Lactobacillus plantarum and Listeria innocua. J Appl Microbiol 97:104–113. doi:10.1111/j.1365-2672.2004.02275.x

    CAS  PubMed  Google Scholar 

  • Foody P (1984) Method for increasing the accessibility of cellulose in lignocellulosic materials, particularly hardwoods agricultural residues and the like Google Patents http://www.google.nl/patents?hl=nl&lr=&vid=USPAT4461648&id=pJx1AAAAEBAJ&oi=fnd&dq=steam+AND+lignocellulose+AND+explosive+AND+decompression+AND+novel&printsec=abstract#v=onepage&q&f=false. Accessed 28 Oct 2013

  • Franden MA, Pienkos PT, Zhang M (2009) Development of a high-throughput method to evaluate the impact of inhibitory compounds from lignocellulosic hydrolysates on the growth of Zymomonas mobilis. J Biotechnol 144:259–267. doi:10.1016/j.jbiotec.2009.08.006

    CAS  PubMed  Google Scholar 

  • Franden MA, Pilath H, Mohagheghi A, Pienkos P, Zhang M (2013) Inhibition of growth of Zymomonas mobilis by model compounds found in lignocellulosic hydrolysates. Biotechnol Biofuels 6:99. doi:10.1186/1754-6834-6-99

    CAS  PubMed Central  PubMed  Google Scholar 

  • Frazer FR, McCaskey TA (1989) Wood hydrolyzate treatments for improved fermentation of wood sugars to 2,3-butanediol. Biomass 18:31–42. doi:10.1016/0144-4565(89)90079-6

    CAS  Google Scholar 

  • García-Aparicio MAP, Ballesteros I, González A, Oliva JM, Ballesteros M, Negro MAJ (2006) Effect of inhibitors released during steam-explosion pretreatment of barley straw on enzymatic hydrolysis. Appl Biochem Biotechnol 129:278–288. doi:10.1385/ABAB:129:1:278

    PubMed  Google Scholar 

  • Garlotta D (2001) A literature review of poly(lactic acid). J Polym Environ 9:63–84. doi:10.1023/a:1020200822435

    CAS  Google Scholar 

  • Gorsich SW, Dien BS, Nichols NN, Slininger PJ, Liu ZL, Skory CD (2006) Tolerance to furfural-induced stress is associated with pentose phosphate pathway genes ZWF1, GND1, RPE1, and TKL1 in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 71:339–349. doi:10.1007/s00253-005-0142-3

    CAS  PubMed  Google Scholar 

  • Gray KA, Zhao L, Emptage M (2006) Bioethanol Curr Opin Chem Biol 10:141–146

    CAS  Google Scholar 

  • Gutiérrez T, Buszko M, Ingram L, Preston J (2002) Reduction of furfural to furfuryl alcohol by ethanologenic strains of bacteria and its effect on ethanol production from xylose. Appl Biochem Biotechnol 98–100:327–340. doi:10.1007/978-1-4612-0119-9_27

    PubMed  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 Fact 10:2

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hatfield RD, Ralph J, Grabber JH (1999) Cell wall cross-linking by ferulates and diferulates in grasses. J Sci Food Agric 79:403–407

    CAS  Google Scholar 

  • Heaton EA, Dohleman FG, Long SP (2008) Meeting US biofuel goals with less land: the potential of Miscanthus. Glob Chang Biol 14:2000–2014. doi:10.1111/j.1365-2486.2008.01662.x

    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. doi:10.1128/AEM. 01649-09

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hendriks ATWM, Zeeman G (2009) Pretreatments to enhance the digestibility of lignocellulosic biomass. Bioresour Technol 100:10–18. doi:10.1016/j.biortech.2008.05.027

    CAS  PubMed  Google Scholar 

  • Herbert D, Elsworth R, Telling RC (1956) The continuous culture of bacteria; a theoretical and experimental study. J Gen Microbiol 14:601–622. doi:10.1099/00221287-14-3-601

    CAS  PubMed  Google Scholar 

  • Holtzapple M, Jun J-H, Ashok G, Patibandla S, Dale B (1991) The ammonia freeze explosion (AFEX) process. Appl Biochem Biotechnol 28–29:59–74. doi:10.1007/bf02922589

    Google Scholar 

  • Horváth IS, Taherzadeh MJ, Niklasson C, Lidén G (2001) Effects of furfural on anaerobic continuous cultivation of Saccharomyces cerevisiae. Biotechnol Bioeng 75:540–549. doi:10.1002/bit.10090

    PubMed  Google Scholar 

  • Hoskinson RL, Karlen DL, Birrell SJ, Radtke CW, Wilhelm WW (2007) Engineering, nutrient removal, and feedstock conversion evaluations of four corn stover harvest scenarios. Biomass Bioenergy 31:126–136. doi:10.1016/j.biombioe.2006.07.006

    CAS  Google Scholar 

  • Hu C, Zhao X, Zhao J, Wu S, Zhao ZK (2009) Effects of biomass hydrolysis by-products on oleaginous yeast Rhodosporidium toruloides. Bioresour Technol 100:4843–4847

    CAS  PubMed  Google Scholar 

  • Huang C, Wu H, Smith T, Z-j L, Lou W-Y, Zong M-h (2012) In vivo detoxification of furfural during lipid production by the oleaginous yeast Trichosporon fermentans. Biotechnol Lett 34:1637–1642. doi:10.1007/s10529-012-0948-x

    CAS  PubMed  Google Scholar 

  • Humbird D, Davis R, Tao L, Kinchin C, Hsu D, Aden A, Schoen P, Lukas J, Olthof B, Worley M, Sexton D, Dudgeon D (2011) Process design and economics for biochemical conversion of lignocellulosic biomass to ethanol NREL http://www.researchgate.net/publication/229843699_Process_Design_and_Economics_for_Biochemical_Conversion_of_Lignocellulosic_Biomass_to_Ethanol_Dilute-Acid_Pretreatment_and_Enzymatic_Hydrolysis_of_Corn_Stover/file/9fcfd5011638d5a2af.pdf. Accessed 27 May 2013

  • Iwaki A, Ohnuki S, Suga Y, Izawa S, Ohya Y (2013) Vanillin inhibits translation and induces messenger ribonucleoprotein (mRNP) granule formation in Saccharomyces cerevisiae: application and validation of high-content, image-based profiling. PLoS One 8:e61748

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jackson MG (1977) Review article: the alkali treatment of straws. Anim Feed Sci Technol 2:105–130. doi:10.1016/0377-8401(77)90013-X

    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. doi:10.1007/s002530051233

    Google Scholar 

  • Kaar WE, Gutierrez CV, Kinoshita CM (1998) Steam explosion of sugarcane bagasse as a pretreatment for conversion to ethanol. Biomass Bioenergy 14:277–287

    CAS  Google Scholar 

  • Kabel MA, Bos G, Zeevalking J, Voragen AGJ, Schols HA (2007) Effect of pretreatment severity on xylan solubility and enzymatic breakdown of the remaining cellulose from wheat straw. Bioresour Technol 98:2034–2042

    CAS  PubMed  Google Scholar 

  • Karimi K, Kheradmandinia S, Taherzadeh MJ (2006) Conversion of rice straw to sugars by dilute-acid hydrolysis. Biomass Bioenergy 30:247–253

    CAS  Google Scholar 

  • Keweloh H, Diefenbach R, Rehm H-J (1991) Increase of phenol tolerance of Escherichia coli by alterations of the fatty acid composition of the membrane lipids. Arch Microbiol 157:49–53. doi:10.1007/bf00245334

    CAS  PubMed  Google Scholar 

  • Klemm D, Heublein B, Fink HP, Bohn A (2005) Cellulose: fascinating biopolymer and sustainable raw material. Angew Chem Int Ed 44:3358–3393. doi:10.1002/anie.200460587

    CAS  Google Scholar 

  • Klinke HB, Ahring BK, Schmidt AS, Thomsen AB (2002) Characterization of degradation products from alkaline wet oxidation of wheat straw. Bioresour Technol 82:15–26. doi:10.1016/S0960-8524(01)00152-3

    CAS  PubMed  Google Scholar 

  • Klinke HB, Olsson L, Thomsen AB, Ahring BK (2003) Potential inhibitors from wet oxidation of wheat straw and their effect on ethanol production of Saccharomyces cerevisiae: wet oxidation and fermentation by yeast. Biotechnol Bioeng 81:738–747. doi:10.1002/bit.10523

    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. doi:10.1007/s00253-004-1642-2

  • Kolb M, Sieber V, Amann M, Faulstich M, Schieder D (2012) Removal of monomer delignification products by laccase from Trametes versicolor. Bioresour Technol 104:298–304

    CAS  PubMed  Google Scholar 

  • Koopman F, Wierckx N, De Winde JH, Ruijssenaars HJ (2010) Identification and characterization of the furfural and 5-(hydroxymethyl) furfural degradation pathways of Cupriavidus basilensis HMF14. Proc Natl Acad Sci 107:4919

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kootstra AM, Beeftink H, Scott E, Sanders J (2009) Optimization of the dilute maleic acid pretreatment of wheat straw. Biotechnol Biofuels 2:31. doi:10.1186/1754-6834-2-31

    PubMed Central  PubMed  Google Scholar 

  • Kwon Y-J, Ma A-Z, Li Q, Wang F, Zhuang G-Q, Liu C-Z (2011) Effect of lignocellulosic inhibitory compounds on growth and ethanol fermentation of newly-isolated thermotolerant Issatchenkia orientalis. Bioresour Technol 102:8099–8104. doi:10.1016/j.biortech.2011.06.035

    CAS  PubMed  Google Scholar 

  • Laadan B, Almeida JRM, Rådström P, Hahn-Hägerdal B, Gorwa-Grauslund M (2008) Identification of an NADH-dependent 5-hydroxymethylfurfural-reducing alcohol dehydrogenase in Saccharomyces cerevisiae. Yeast 25:191–198. doi:10.1002/yea.1578

    CAS  PubMed  Google Scholar 

  • Larsson S, Palmqvist E, Hahn-Hägerdal B, Tengborg C, Stenberg K, Zacchi G, Nilvebrant N-O (1999a) The generation of fermentation inhibitors during dilute acid hydrolysis of softwood. Enzyme Microb Technol 24:151–159

    CAS  Google Scholar 

  • Larsson S, Reimann A, Nilvebrant N-O, Jönsson L (1999b) Comparison of different methods for the detoxification of lignocellulose hydrolyzates of spruce. Appl Biochem Biotechnol 77:91–103. doi:10.1385/abab:77:1-3:91

    Google Scholar 

  • Larsson S, Quintana-Sáinz A, Reimann A, Nilvebrant N-O, Jönsson L (2000) Influence of lignocellulose-derived aromatic compounds on oxygen-limited growth and ethanolic fermentation by Saccharomyces cerevisiae. Appl Biochem Biotechnol 84–86:617–632. doi:10.1385/abab:84-86:1-9:617

    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. doi:10.1128/AEM. 67.3.1163-1170.2001

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lashof DA, Ahuja DR (1990) Relative contributions of greenhouse gas emissions to global warming. Nature 344:529–531. doi:10.1038/344529a0

    CAS  Google Scholar 

  • Lee H-J, Lim W-S, Lee J-W (2013) Improvement of ethanol fermentation from lignocellulosic hydrolysates by the removal of inhibitors. J Ind Eng Chem 19:2010–2015. doi:10.1016/j.jiec.2013.03.014

    CAS  Google Scholar 

  • Lewis Liu Z, Blaschek HP (2010) Biomass conversion inhibitors and in situ detoxification biomass to biofuels: strategies for global industries. John Wiley& sons Ltd, United Kingdom

    Google Scholar 

  • Lewis Liu Z, Ma M, Song M (2009) Evolutionarily engineered ethanologenic yeast detoxifies lignocellulosic biomass conversion inhibitors by reprogrammed pathways. Mol Genet Genomics 282:233–244. doi:10.1007/s00438-009-0461-7

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ma M, Liu ZL (2010) Comparative transcriptome profiling analyses during the lag phase uncover YAP1, PDR1, PDR3, RPN4, and HSF1 as key regulatory genes in genomic adaptation to the lignocellulose derived inhibitor HMF for Saccharomyces cerevisiae. BMC Genomics 11:660

    CAS  PubMed Central  PubMed  Google Scholar 

  • Martín C, Klinke HB, Thomsen AB (2007) Wet oxidation as a pretreatment method for enhancing the enzymatic convertibility of sugarcane bagasse. Enzyme Microb Technol 40:426–432. doi:10.1016/j.enzmictec.2006.07.015

    Google Scholar 

  • McIntosh S, Vancov T (2010) Enhanced enzyme saccharification of Sorghum bicolor straw using dilute alkali pretreatment. Bioresour Technol 101:6718–6727

  • McMillan J, Adney WS, Mielenz JR, Klasson KT, Thomsen MH, Thygesen A, Jørgensen H, Larsen J, Christensen BH, Thomsen AB (2006) Preliminary results on optimization of pilot scale pretreatment of wheat straw used in coproduction of bioethanol and electricity. Appl Biochem Biotechnol 130:448–460. doi:10.1385/ABAB:130:1:448

    Google Scholar 

  • Miller EN, Jarboe LR, Turner PC, Pharkya P, Yomano LP, York SW, Nunn D, Shanmugam KT, Ingram LO (2009) Furfural inhibits growth by limiting sulfur assimilation in ethanologenic Escherichia coli strain LY180. Appl Environ Microbiol 75:6132–6141. doi:10.1128/AEM. 01187-09

    CAS  PubMed Central  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Moon J, Liu ZL (2012) Engineered NADH-dependent GRE2 from Saccharomyces cerevisiae by directed enzyme evolution enhances HMF reduction using additional cofactor NADPH. Enzyme Microb Technol 50:115–120. doi:10.1016/j.enzmictec.2011.10.007

    CAS  PubMed  Google Scholar 

  • Morsomme P, de Kerchove d’Exaerde A, De Meester S, Thines D, Goffeau A, Boutry M (1996) Single point mutations in various domains of a plant plasma membrane H(+)-ATPase expressed in Saccharomyces cerevisiae increase H(+)-pumping and permit yeast growth at low pH. EMBO J 15:5513–5526

    CAS  PubMed Central  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. doi:10.1016/j.biortech.2004.06.025

    CAS  PubMed  Google Scholar 

  • Muñoz C, Guillén F, Martínez AT, Martínez MJ (1997) Induction and characterization of laccase in the ligninolytic fungus Pleurotus eryngii. Curr Microbiol 34:1–5. doi:10.1007/s002849900134

    PubMed  Google Scholar 

  • Nichols NN, Dien BS, Guisado GM, López MJ, Davison BH, Evans BR, Finkelstein M, McMillan JD (2005) Bioabatement to remove inhibitors from biomass-derived sugar hydrolysates. Appl Biochem Biotechnol 121:379–390. doi:10.1385/ABAB:121:1-3:0379

    PubMed  Google Scholar 

  • 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. Enzyme Microb Technol 42:624–630

    CAS  Google Scholar 

  • Nilvebrant N-O, Reimann A, Larsson S, Jönsson L (2001) Detoxification of lignocellulose hydrolysates with ion-exchange resins. Appl Biochem Biotechnol 91–93:35–49. doi:10.1385/abab:91-93:1-9:35

    PubMed  Google Scholar 

  • Nilvebrant N-O, Persson P, Reimann A, de Sousa F, Gorton L, Jönsson L (2003) Limits for alkaline detoxification of dilute-acid lignocellulose hydrolysates. Appl Biochem Biotechnol 107:615–628. doi:10.1385/abab:107:1-3:615

    Google Scholar 

  • Nishikawa NK, Sutcliffe R, Saddler JN (1988) The influence of lignin degradation products on xylose fermentation by Klebsiella pneumoniae. Appl Microbiol Biotechnol 27:549–552. doi:10.1007/bf00451630

    CAS  Google Scholar 

  • Öhgren K, Bura R, Saddler J, Zacchi G (2007) Effect of hemicellulose and lignin removal on enzymatic hydrolysis of steam pretreated corn stover. Bioresour Technol 98:2503–2510

    PubMed  Google Scholar 

  • Oliva JM, Ballesteros I, Negro MJ, Manzanares P, Cabañas A, Ballesteros M (2004) Effect of Binary Combinations of Selected Toxic Compounds on Growth and Fermentation of Kluyveromyces marxianus. Biotechnol Prog 20:715–720. doi:10.1021/bp034317p

  • Oliva J, Sáez F, Ballesteros I, González A, Negro M, 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 105:141–153. doi:10.1385/abab:105:1-3:141

    PubMed  Google Scholar 

  • Orij R, Brul S, Smits GJ (2011) Intracellular pH is a tightly controlled signal in yeast BBA-Gen. Subjects 1810:933–944

    CAS  Google Scholar 

  • Palmqvist E, Hahn-Hägerdal B (2000) Fermentation of lignocellulosic hydrolysates. II: inhibitors and mechanisms of inhibition. Bioresour Technol 74:25–33. doi:10.1016/S0960-8524(99)00161-3

    CAS  Google Scholar 

  • Palmqvist E, Grage H, Meinander NQ, Hahn-Hägerdal B (1999) Main and interaction effects of acetic acid, furfural, and p-hydroxybenzoic acid on growth and ethanol productivity of yeasts. Biotechnol Bioeng 63:46–55. doi:10.1002/(SICI)1097-0290(19990405)63:1%3C46::AID-BIT5%3E3.0.CO;2-J

  • 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. doi:10.1007/bf00270792

    CAS  Google Scholar 

  • Park SE, Koo HM, Park YP, Park SM, Park JC, Lee OH, Park YC, Seo JH (2011) Expression of aldehyde dehydrogenase 6 reduces inhibitory effect of furan derivatives on cell growth and ethanol production in Saccharomyces cerevisiae. Bioresour Technol 102:6033–6038

    CAS  PubMed  Google Scholar 

  • Persson P, Andersson J, Gorton L, Larsson S, Nilvebrant NO, Jönsson LJ (2002) Effect of different forms of alkali treatment on specific fermentation inhibitors and on the fermentability of lignocellulose hydrolysates for production of fuel ethanol. J Agric Food Chem 50:5318–5325. doi:10.1021/jf025565o

    CAS  PubMed  Google Scholar 

  • Pirt SJ (1965) The maintenance energy of bacteria in growing cultures. Proc R Soc B 163:224–231

    CAS  Google Scholar 

  • Roberto IC, Mussatto SI, Rodrigues RCLB (2003) Dilute-acid hydrolysis for optimization of xylose recovery from rice straw in a semi-pilot reactor. Ind Crop Prod 17:171–176. doi:10.1016/S0926-6690(02)00095-X

    CAS  Google Scholar 

  • Saha BC (2003) Hemicellulose bioconversion. J Ind Microbiol Biotechnol 30:279–291. doi:10.1007/s10295-003-0049-x

    CAS  PubMed  Google Scholar 

  • Sanchez G, Pilcher L, Roslander C, Modig T, Galbe M, Liden G (2004) Dilute-acid hydrolysis for fermentation of the Bolivian straw material Paja Brava. Bioresour Technol 93:249–256

  • Sárvári Horváth I, Franzén CJ, Taherzadeh MJ, Niklasson C, Lidén G (2003) Effects of furfural on the respiratory metabolism of Saccharomyces cerevisiae in glucose-limited chemostats. Appl Environ Microbiol 69:4076–4086. doi:10.1128/aem. 69.7.4076-4086.2003

    PubMed Central  PubMed  Google Scholar 

  • Sendich E, Laser M, Kim S, Alizadeh H, Laureano-Perez L, Dale B, Lynd L (2008) Recent process improvements for the ammonia fiber expansion (AFEX) process and resulting reductions in minimum ethanol selling price. Bioresour Technol 99:8429–8435. doi:10.1016/j.biortech.2008.02.059

    CAS  PubMed  Google Scholar 

  • Shafiei M, Karimi K, Taherzadeh MJ (2010) Pretreatment of spruce and oak by N-methylmorpholine-N-oxide (NMMO) for efficient conversion of their cellulose to ethanol. Bioresour Technol 101:4914–4918. doi:10.1016/j.biortech.2009.08.100

    CAS  PubMed  Google Scholar 

  • Srinivasan S (2009) The food v. fuel debate: a nuanced view of incentive structures. Renew Energy 34:950–954. doi:10.1016/j.renene.2008.08.015

    Google Scholar 

  • Sun Y, Cheng J (2002) Hydrolysis of lignocellulosic materials for ethanol production: a review. Bioresour Technol 83:1–11. doi:10.1016/S0960-8524(01)00212-7

    CAS  PubMed  Google Scholar 

  • Sun JX, Sun XF, Sun RC, Su YQ (2004) Fractional extraction and structural characterization of sugarcane bagasse hemicelluloses. Carbohydr Polym 56:195–204. doi:10.1016/j.carbpol.2004.02.002

    CAS  Google Scholar 

  • Sundström L, Larsson S, Jönsson L (2010) Identification of Saccharomyces cerevisiae genes involved in the resistance to phenolic fermentation inhibitors. Appl Biochem Biotechnol 161:106–115. doi:10.1007/s12010-009-8811-9

    PubMed  Google Scholar 

  • Taherzadeh MJ, Niklasson C, Lidén G (1997) Acetic acid—friend or foe in anaerobic batch conversion of glucose to ethanol by Saccharomyces cerevisiae? Chem Eng Sci 52:2653–2659

    CAS  Google Scholar 

  • Taherzadeh MJ, Gustafsson L, Niklasson C, Lidén G (1999) Conversion of furfural in aerobic and anaerobic batch fermentation of glucose by Saccharomyces cerevisiae. J Biosci Bioeng 87:169–174

    CAS  PubMed  Google Scholar 

  • Taherzadeh MJ, Gustafsson L, Niklasson C, Lidén G (2000) Physiological effects of 5-hydroxymethylfurfural on Saccharomyces cerevisiae. Appl Microbiol Biotechnol 53:701–708. doi:10.1007/s002530000328

    CAS  PubMed  Google Scholar 

  • Teeri TT (1997) Crystalline cellulose degradation: new insight into the function of cellobiohydrolases. Trends Biotechnol 15:160–167

    Google Scholar 

  • Toledano A, García A, Mondragon I, Labidi J (2010) Lignin separation and fractionation by ultrafiltration. Sep Purif Technol 71:38–43. doi:10.1016/j.seppur.2009.10.024

    CAS  Google Scholar 

  • Tucker M, Kim K, Newman M, Nguyen Q (2003) Effects of temperature and moisture on dilute-acid steam explosion pretreatment of corn stover and cellulase enzyme digestibility. Appl Biochem Biotechnol 105:165–177. doi:10.1385/abab:105:1-3:165

    PubMed  Google Scholar 

  • Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiol 153:895–905. doi:10.1104/pp. 110.155119

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vennestrøm PNR, Osmundsen CM, Christensen CH, Taarning E (2011) Beyond petrochemicals: the renewable chemicals industry. Angew Chem Int Ed 50:10502–10509. doi:10.1002/anie.201102117

    Google Scholar 

  • Verduyn C, Postma E, Scheffers WA, Van Dijken JP (1992) Effect of benzoic acid on metabolic fluxes in yeasts: a continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 8:501–517. doi:10.1002/yea.320080703

    CAS  PubMed  Google Scholar 

  • Wang X, Miller EM, Yomano L, Zhang X, Shanmugam KT, Ingram LO (2011) Overexpression of NADH-dependent oxidoreductase fucO increases furfural tolerance in Escherichia coli strains engineered for the production of ethanol and lactate. Appl Environ Microbiol 77:5132–5140. doi:10.1128/AEM. 05008-11

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang X, Miller EM, Yomano LP, Zhang X, Shanmugam KT, Ingram LO (2013) Engineering furfural tolerance in Escherichia coli improves the fermentation of lignocellulosic sugars into renewable chemicals. Proc Natl Acad Sci 110:4021–4026. doi:10.1073/pnas.1217958110

    CAS  PubMed Central  PubMed  Google Scholar 

  • Whetten R, Sederoff R (1995) Lignin biosynthesis. Plant Physiol 7:1001–1013

    CAS  Google Scholar 

  • Zaldivar J, Ingram LO (1999) Effect of organic acids on the growth and fermentation of ethanologenic Escherichia coli LY01. Biotechnol Bioeng 66:203–210. doi:10.1002/(sici)1097-0290(1999)66:4<203::aid-bit1>3.0.co;2-#

  • Zhang YHP, Ding SY, Mielenz JR, Cui JB, Elander RT, Laser M, Himmel ME, McMilland JR, Lynd LR (2007) Fractionating recalcitrant lignocellulose at modest reaction conditions. Biotechnol Bioeng 97:214–223. doi:10.1002/bit.21386

    CAS  PubMed  Google Scholar 

  • Zhang J, Geng A, Yao C, Lu Y, Li Q (2012) Effects of lignin-derived phenolic compounds on xylitol production and key enzyme activities by a xylose utilizing yeast Candida athensensis SB18. Bioresour Technol 121:369–378

    CAS  PubMed  Google Scholar 

  • Zhong C, Lau M, Balan V, Dale B, Yuan Y-J (2009) Optimization of enzymatic hydrolysis and ethanol fermentation from AFEX-treated rice straw. Appl Microbiol Biotechnol 84:667–676. doi:10.1007/s00253-009-2001-0

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The writers of this article would like to thank the BE-Basic consortium, Corbion and DSM for funding this research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Edwin C. van der Pol.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

van der Pol, E.C., Bakker, R.R., Baets, P. et al. By-products resulting from lignocellulose pretreatment and their inhibitory effect on fermentations for (bio)chemicals and fuels. Appl Microbiol Biotechnol 98, 9579–9593 (2014). https://doi.org/10.1007/s00253-014-6158-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-014-6158-9

Keywords

Navigation