Abstract
With growing interest in alternative fuels to minimize carbon and particle emissions, research continues on the production of lignocellulosic ethanol and on the development of suitable yeast strains. However, great diversities and continued technical advances in pretreatment methods for lignocellulosic biomass complicate the evaluation of developed yeast strains, and strain development often lags industrial applicability. In this review, recent studies demonstrating developed yeast strains with lignocellulosic biomass hydrolysates are compared. For the pretreatment methods, we highlight hydrothermal pretreatments (dilute acid treatment and autohydrolysis), which are the most commonly used and effective methods for lignocellulosic biomass pretreatment. Rather than pretreatment conditions, the type of biomass most strongly influences the composition of the hydrolysates. Metabolic engineering strategies for yeast strain development, the choice of xylose-metabolic pathway, adaptive evolution, and strain background are highlighted as important factors affecting ethanol yield and productivity from lignocellulosic biomass hydrolysates. A comparison of the parameters from recent studies demonstrating lignocellulosic ethanol production provides useful information for future strain development.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Albers SC, Berklund AM, Graff GD (2016) The rise and fall of innovation in biofuels. Nat Biotechnol 34:814–821. https://doi.org/10.1038/nbt.3644
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. https://doi.org/10.1016/j.biortech.2009.11.093
Basso LC, De Amorim HV, De Oliveira AJ, Lopes ML (2008) Yeast selection for fuel ethanol production in Brazil. FEMS Yeast Res 8(7):1155–1163
Costa CE, Romaní A, Cunha JT, Johansson B, Domingues L (2017) Integrated approach for selecting efficient Saccharomyces cerevisiae for industrial lignocellulosic fermentations: importance of yeast chassis linked to process conditions. Bioresour Technol 227:24–34. https://doi.org/10.1016/j.biortech.2016.12.016
Cunha JT, Romaní A, Costa CE, Sá-Correia I, Domingues L (2019a) Molecular and physiological basis of Saccharomyces cerevisiae tolerance to adverse lignocellulose-based process conditions. Appl Microbiol Biotechnol 103(1):159–175. https://doi.org/10.1007/s00253-018-9478-3
Cunha JT, Soares PO, Romaní A, Thevelein JM, Domingues L (2019b) Xylose fermentation efficiency of industrial Saccharomyces cerevisiae yeast with separate or combined xylose reductase/xylitol dehydrogenase and xylose isomerase pathways. Biotechnol Biofuels 12(1):20
Gomes D, Gama M, Domingues L (2018) Determinants on an efficient cellulase recycling process for the production of bioethanol from recycled paper sludge under high solid loadings. Biotechnol Biofuels 11:111–111. https://doi.org/10.1186/s13068-018-1103-2
Kim SR, Ha S-J, Kong II, Jin Y-S (2012) High expression of XYL2 coding for xylitol dehydrogenase is necessary for efficient xylose fermentation by engineered Saccharomyces cerevisiae. Metab Eng 14(4):336–343. https://doi.org/10.1016/j.ymben.2012.04.001
Kim SR, Park Y-C, Jin Y-S, Seo J-H (2013a) Strain engineering of Saccharomyces cerevisiae for enhanced xylose metabolism. Biotechnol Adv 31(6):851–861. https://doi.org/10.1016/j.biotechadv.2013.03.004
Kim SR, Skerker JM, Kang W, Lesmana A, Wei N, Arkin AP, Jin Y-S (2013b) Rational and evolutionary engineering approaches uncover a small set of genetic changes efficient for rapid xylose fermentation in Saccharomyces cerevisiae. PLoS One 8(2):e57048. https://doi.org/10.1371/journal.pone.0057048
Kim Y, Kreke T, Ko JK, Ladisch MR (2015) Hydrolysis-determining substrate characteristics in liquid hot water pretreated hardwood. Biotechnol Bioeng 112(4):677–687. https://doi.org/10.1002/bit.25465
Kim SR, Skerker JM, Kong II, Kim H, Maurer MJ, Zhang G-C, Peng D, Wei N, Arkin AP, Jin Y-S (2017) Metabolic engineering of a haploid strain derived from a triploid industrial yeast for producing cellulosic ethanol. Metab Eng 40:176–185. https://doi.org/10.1016/j.ymben.2017.02.006
Kim KH, Eudes A, Jeong K, Yoo CG, Kim CS, Ragauskas A (2019) Integration of renewable deep eutectic solvents with engineered biomass to achieve a closed-loop biorefinery. Proc Natl Acad Sci 116(28):13816–13824. https://doi.org/10.1073/pnas.1904636116
Ko JK, Kim Y, Ximenes E, 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. https://doi.org/10.1002/bit.25349
Ko JK, Um Y, Woo HM, Kim KH, Lee S-M (2016) Ethanol production from lignocellulosic hydrolysates using engineered Saccharomyces cerevisiae harboring xylose isomerase-based pathway. Bioresour Technol 209:290–296. https://doi.org/10.1016/j.biortech.2016.02.124
Ko JK, Enkh-Amgalan T, Gong G, Um Y, Lee S-M (2020) Improved bioconversion of lignocellulosic biomass by Saccharomyces cerevisiae engineered for tolerance to acetic acid. GCB Bioenergy 12(1):90–100. https://doi.org/10.1111/gcbb.12656
Kong II, Turner TL, Kim H, Kim SR, Jin Y-S (2018) Phenotypic evaluation and characterization of 21 industrial Saccharomyces cerevisiae yeast strains. FEMS Yeast Res 18(1). https://doi.org/10.1093/femsyr/foy001
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(8):3713–3729. https://doi.org/10.1021/ie801542g
Lane S, Xu H, Oh EJ, Kim H, Lesmana A, Jeong D, Zhang G, Tsai C-S, Jin Y-S, Kim SR (2018) Glucose repression can be alleviated by reducing glucose phosphorylation rate in Saccharomyces cerevisiae. Sci Rep 8(1):2613–2612. https://doi.org/10.1038/s41598-018-20804-4
Lee WH, Jin YS (2017) Evaluation of ethanol production activity by engineered Saccharomyces cerevisiae fermenting cellobiose through the phosphorolytic pathway in simultaneous Saccharification and fermentation of cellulose. J Microbiol Biotechnol 27(9):1649–1656. https://doi.org/10.4014/jmb.1705.05039
Lee C-R, Sung BH, Lim K-M, Kim M-J, Sohn MJ, Bae J-H, Sohn J-H (2017) Co-fermentation using recombinant Saccharomyces cerevisiae yeast strains hyper-secreting different cellulases for the production of cellulosic bioethanol. Sci Rep 7(1):4428. https://doi.org/10.1038/s41598-017-04815-1
Li Y, Shuai L, Kim H, Motagamwala AH, Mobley JK, Yue F, Tobimatsu Y, Havkin-Frenkel D, Chen F, Dixon RA, Luterbacher JS, Dumesic JA, Ralph J (2018) An “ideal lignin” facilitates full biomass utilization. Sci Adv 4(9):eaau2968. https://doi.org/10.1126/sciadv.aau2968
Liu J-J, Zhang G-C, Kwak S, Oh EJ, Yun EJ, Chomvong K, Cate JHD, Jin Y-S (2019) Overcoming the thermodynamic equilibrium of an isomerization reaction through oxidoreductive reactions for biotransformation. Nat Commun 10(1):1356. https://doi.org/10.1038/s41467-019-09288-6
Lynd LR (2017) The grand challenge of cellulosic biofuels. Nat Biotechnol 35:912–915. https://doi.org/10.1038/nbt.3976
Lynd LR, Liang X, Biddy MJ, Allee A, Cai H, Foust T, Himmel ME, Laser MS, Wang M, Wyman CE (2017) Cellulosic ethanol: status and innovation. Curr Opin Biotechnol 45:202–211. https://doi.org/10.1016/j.copbio.2017.03.008
Lyu H, Zhou J, Geng Z, Lyu C, Li Y (2018) Two-stage processing of liquid hot water pretreatment for recovering C5 and C6 sugars from cassava straw. Process Biochem 75:202–211. https://doi.org/10.1016/j.procbio.2018.10.003
Moore RH, Thornhill KL, Weinzierl B, Sauer D, D’Ascoli E, Kim J, Lichtenstern M, Scheibe M, Beaton B, Beyersdorf AJ, Barrick J, Bulzan D, Corr CA, Crosbie E, Jurkat T, Martin R, Riddick D, Shook M, Slover G, Voigt C, White R, Winstead E, Yasky R, Ziemba LD, Brown A, Schlager H, Anderson BE (2017) Biofuel blending reduces particle emissions from aircraft engines at cruise conditions. Nature 543:411–415. https://doi.org/10.1038/nature21420
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(6):673–686. https://doi.org/10.1016/j.biortech.2004.06.025
Nguyen TY, Cai CM, Kumar R, Wyman CE (2017) Overcoming factors limiting high-solids fermentation of lignocellulosic biomass to ethanol. Proc Natl Acad Sci 114(44):11673–11678. https://doi.org/10.1073/pnas.1704652114
Nitsos CK, Choli-Papadopoulou T, Matis KA, Triantafyllidis KS (2016) Optimization of hydrothermal pretreatment of hardwood and softwood lignocellulosic residues for selective hemicellulose recovery and improved cellulose enzymatic hydrolysis. ACS Sustain Chem Eng 4(9):4529–4544. https://doi.org/10.1021/acssuschemeng.6b00535
Pandiyan K, Singh A, Singh S, Saxena AK, Nain L (2019) Technological interventions for utilization of crop residues and weedy biomass for second generation bio-ethanol production. Renew Energy 132:723–741. https://doi.org/10.1016/j.renene.2018.08.049
Pereira R, Wei Y, Mohamed E, Radi M, Malina C, Herrgård MJ, Feist AM, Nielsen J, Chen Y (2019) Adaptive laboratory evolution of tolerance to dicarboxylic acids in Saccharomyces cerevisiae. Metab Eng 56:130–141. https://doi.org/10.1016/j.ymben.2019.09.008
Rahimi A, Ulbrich A, Coon JJ, Stahl SS (2014) Formic-acid-induced depolymerization of oxidized lignin to aromatics. Nature 515:249. https://doi.org/10.1038/nature13867
Sasaki K, Tsuge Y, Sasaki D, Teramura H, Inokuma K, Hasunuma T, Ogino C, Kondo A (2015) Mechanical milling and membrane separation for increased ethanol production during simultaneous saccharification and co-fermentation of rice straw by xylose-fermenting Saccharomyces cerevisiae. Bioresour Technol 185:263–268. https://doi.org/10.1016/j.biortech.2015.02.117
Searchinger TD, Wirsenius S, Beringer T, Dumas P (2018) Assessing the efficiency of changes in land use for mitigating climate change. Nature 564(7735):249–253. https://doi.org/10.1038/s41586-018-0757-z
Service RF (2014) Cellulosic ethanol at last? Science 345(6201):1111–1111. https://doi.org/10.1126/science.345.6201.1111
Shekiro Iii J, Kuhn EM, Nagle NJ, Tucker MP, Elander RT, Schell DJ (2014) Characterization of pilot-scale dilute acid pretreatment performance using deacetylated corn stover. Biotechnol Biofuels 7(1):23. https://doi.org/10.1186/1754-6834-7-23
Shin SK, Ko YJ, Hyeon JE, Han SO (2019) Studies of advanced lignin valorization based on various types of lignolytic enzymes and microbes. Bioresour Technol 289:121728. https://doi.org/10.1016/j.biortech.2019.121728
Shuai L, Amiri MT, Questell-Santiago YM, Héroguel F, Li Y, Kim H, Meilan R, Chapple C, Ralph J, Luterbacher JS (2016) Formaldehyde stabilization facilitates lignin monomer production during biomass depolymerization. Science 354(6310):329–333. https://doi.org/10.1126/science.aaf7810
Tsai C-S, Kong II, Lesmana A, Million G, Zhang G-C, Kim SR, Jin Y-S (2015) Rapid and marker-free refactoring of xylose-fermenting yeast strains with Cas9/CRISPR. Biotechnol Bioeng 112(11):2406–2411. https://doi.org/10.1002/bit.25632
Wang Z, Dien BS, Rausch KD, Tumbleson ME, Singh V (2019) Improving ethanol yields with deacetylated and two-stage pretreated corn stover and sugarcane bagasse by blending commercial xylose-fermenting and wild type Saccharomyces yeast. Bioresour Technol 282:103–109. https://doi.org/10.1016/j.biortech.2019.02.123
Wei W, Wu S, Liu L (2012) Enzymatic saccharification of dilute acid pretreated eucalyptus chips for fermentable sugar production. Bioresour Technol 110:302–307. https://doi.org/10.1016/j.biortech.2012.01.003
Weiqi W, Shubin W, Liguo L (2013) Combination of liquid hot water pretreatment and wet disk milling to improve the efficiency of the enzymatic hydrolysis of eucalyptus. Bioresour Technol 128:725–730. https://doi.org/10.1016/j.biortech.2012.08.130
Westman JO, Franzén CJ (2015) Current progress in high cell density yeast bioprocesses for bioethanol production. Biotechnol J 10(8):1185–1195
Yang J, Kim JE, Kim JK, Lee SH, Yu JH, Kim KH (2017) Evaluation of commercial cellulase preparations for the efficient hydrolysis of hydrothermally pretreated empty fruit bunches. BioResources 12:7834–7840. https://doi.org/10.15376/biores.12.4.7834-7840
Yu T, Zhou YJ, Huang M, Liu Q, Pereira R, David F, Nielsen J (2018) Reprogramming yeast metabolism from alcoholic fermentation to lipogenesis. Cell 174(6):1549–1558.e14. https://doi.org/10.1016/j.cell.2018.07.013
Zhang J, Tang M, Viikari L (2012) Xylans inhibit enzymatic hydrolysis of lignocellulosic materials by cellulases. Bioresour Technol 121:8–12. https://doi.org/10.1016/j.biortech.2012.07.010
Funding
This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. 2019R1F1A1062633). The authors also appreciate additional support provided by Korea Institute of Science and Technology (KIST) Institutional Program (2E30170).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Park, H., Jeong, D., Shin, M. et al. Xylose utilization in Saccharomyces cerevisiae during conversion of hydrothermally pretreated lignocellulosic biomass to ethanol. Appl Microbiol Biotechnol 104, 3245–3252 (2020). https://doi.org/10.1007/s00253-020-10427-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-020-10427-z