Expression of Gre2p improves tolerance of engineered xylose-fermenting Saccharomyces cerevisiae to glycolaldehyde under xylose metabolism
Abstract
Engineered S. cerevisiae employing the xylose reductase pathway enables efficient xylose valorization to fuels and chemicals. However, toxicity of thermochemically pretreated biomass hydrolysate on S. cerevisiae is one of the key technical challenges to upgrade biomass-derived sugars including xylose and glucose into high-value products. We investigated the effect of glycolaldehyde, one of the biomass-derived highly toxic aldehyde compounds, and its combinatorial inhibitory effect with other major fermentation inhibitors commonly found in plant hydrolysate such as methylglyoxal, 5-HMF, furfural, vanillin, and acetic acid on engineered xylose-fermenting S. cerevisiae in xylose and/or glucose media. We elucidated that glycolaldehyde and methylglyoxal are the key inhibitory short-aliphatic aldehydes on engineered xylose-fermenting S. cerevisiae in xylose-containing medium. Indeed, the degree of toxicity of these tested fermentation inhibitors varies with the sole carbon source of the medium. We demonstrate that genome integration of an extra copy of autologous GRE2 with its native promotor substantially improved the toxic tolerance of engineered xylose-fermenting S. cerevisiae to major inhibitory compounds including glycolaldehyde in the xylose-containing medium, and xylose-rich, lignocellulosic hydrolysate derived from Miscanthus giganteus, and concurrently improved the ethanol fermentation profile. In conclusion, outcomes of this study will aid the development of next-generation robust S. cerevisiae strains for efficientmore »
- Authors:
-
- National Renewable Energy Lab. (NREL), Golden, CO (United States); Univ. of Illinois, Urbana-Champaign, IL (United States)
- Univ. of Illinois, Urbana-Champaign, IL (United States); Northwestern Univ. Feinberg School of Medicine, Chicago, IL (United States)
- Univ. of Illinois, Urbana-Champaign, IL (United States)
- Publication Date:
- Research Org.:
- National Renewable Energy Laboratory (NREL), Golden, CO (United States)
- Sponsoring Org.:
- USDOE Office of Energy Efficiency and Renewable Energy (EERE)
- OSTI Identifier:
- 1462470
- Report Number(s):
- NREL/JA-5100-72078
Journal ID: ISSN 0175-7598
- Grant/Contract Number:
- AC36-08GO28308
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Applied Microbiology and Biotechnology
- Additional Journal Information:
- Journal Volume: 102; Journal Issue: 18; Journal ID: ISSN 0175-7598
- Publisher:
- Springer
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 09 BIOMASS FUELS; S. cerevisiae; xylose; glycolaldehyde; aldehydes toxicity; Gre2p
Citation Formats
Jayakody, Lahiru N., Turner, Timothy Lee, Yun, Eun Ju, Kong, In Iok, Liu, Jing -Jing, and Jin, Yong -Su. Expression of Gre2p improves tolerance of engineered xylose-fermenting Saccharomyces cerevisiae to glycolaldehyde under xylose metabolism. United States: N. p., 2018.
Web. doi:10.1007/s00253-018-9216-x.
Jayakody, Lahiru N., Turner, Timothy Lee, Yun, Eun Ju, Kong, In Iok, Liu, Jing -Jing, & Jin, Yong -Su. Expression of Gre2p improves tolerance of engineered xylose-fermenting Saccharomyces cerevisiae to glycolaldehyde under xylose metabolism. United States. https://doi.org/10.1007/s00253-018-9216-x
Jayakody, Lahiru N., Turner, Timothy Lee, Yun, Eun Ju, Kong, In Iok, Liu, Jing -Jing, and Jin, Yong -Su. Thu .
"Expression of Gre2p improves tolerance of engineered xylose-fermenting Saccharomyces cerevisiae to glycolaldehyde under xylose metabolism". United States. https://doi.org/10.1007/s00253-018-9216-x. https://www.osti.gov/servlets/purl/1462470.
@article{osti_1462470,
title = {Expression of Gre2p improves tolerance of engineered xylose-fermenting Saccharomyces cerevisiae to glycolaldehyde under xylose metabolism},
author = {Jayakody, Lahiru N. and Turner, Timothy Lee and Yun, Eun Ju and Kong, In Iok and Liu, Jing -Jing and Jin, Yong -Su},
abstractNote = {Engineered S. cerevisiae employing the xylose reductase pathway enables efficient xylose valorization to fuels and chemicals. However, toxicity of thermochemically pretreated biomass hydrolysate on S. cerevisiae is one of the key technical challenges to upgrade biomass-derived sugars including xylose and glucose into high-value products. We investigated the effect of glycolaldehyde, one of the biomass-derived highly toxic aldehyde compounds, and its combinatorial inhibitory effect with other major fermentation inhibitors commonly found in plant hydrolysate such as methylglyoxal, 5-HMF, furfural, vanillin, and acetic acid on engineered xylose-fermenting S. cerevisiae in xylose and/or glucose media. We elucidated that glycolaldehyde and methylglyoxal are the key inhibitory short-aliphatic aldehydes on engineered xylose-fermenting S. cerevisiae in xylose-containing medium. Indeed, the degree of toxicity of these tested fermentation inhibitors varies with the sole carbon source of the medium. We demonstrate that genome integration of an extra copy of autologous GRE2 with its native promotor substantially improved the toxic tolerance of engineered xylose-fermenting S. cerevisiae to major inhibitory compounds including glycolaldehyde in the xylose-containing medium, and xylose-rich, lignocellulosic hydrolysate derived from Miscanthus giganteus, and concurrently improved the ethanol fermentation profile. In conclusion, outcomes of this study will aid the development of next-generation robust S. cerevisiae strains for efficient fermentation of hexose and pentose sugars found in biomass hydrolysate.},
doi = {10.1007/s00253-018-9216-x},
journal = {Applied Microbiology and Biotechnology},
number = 18,
volume = 102,
place = {United States},
year = {Thu Jul 19 00:00:00 EDT 2018},
month = {Thu Jul 19 00:00:00 EDT 2018}
}
Web of Science
Figures / Tables:
Works referenced in this record:
Metabolic pathway engineering based on metabolomics confers acetic and formic acid tolerance to a recombinant xylose-fermenting strain of Saccharomyces cerevisiae
journal, January 2011
- Hasunuma, Tomohisa; Sanda, Tomoya; Yamada, Ryosuke
- Microbial Cell Factories, Vol. 10, Issue 1
Optimization of an acetate reduction pathway for producing cellulosic ethanol by engineered yeast: Optimization of the Acetate Reduction Pathway in Yeast
journal, September 2016
- Zhang, Guo-Chang; Kong, In Iok; Wei, Na
- Biotechnology and Bioengineering, Vol. 113, Issue 12
Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae
journal, January 2007
- Almeida, Joao; Modig, Tobias; Petersson, Anneli
- Journal of Chemical Technology & Biotechnology, Vol. 82, Issue 4, p. 340-349
Pulsed addition of HMF and furfural to batch-grown xylose-utilizing Saccharomyces cerevisiae results in different physiological responses in glucose and xylose consumption phase
journal, January 2013
- Ask, Magnus; Bettiga, Maurizio; Duraiswamy, Varuni
- Biotechnology for Biofuels, Vol. 6, Issue 1
SUMO expression shortens the lag phase of Saccharomyces cerevisiae yeast growth caused by complex interactive effects of major mixed fermentation inhibitors found in hot-compressed water-treated lignocellulosic hydrolysate
journal, October 2014
- Jayakody, Lahiru N.; Kadowaki, Masafumi; Tsuge, Keisuke
- Applied Microbiology and Biotechnology, Vol. 99, Issue 1
Rational and Evolutionary Engineering Approaches Uncover a Small Set of Genetic Changes Efficient for Rapid Xylose Fermentation in Saccharomyces cerevisiae
journal, February 2013
- Kim, Soo Rin; Skerker, Jeffrey M.; Kang, Wei
- PLoS ONE, Vol. 8, Issue 2
Glyoxalase I in micro-organisms: Molecular characteristics, genetics and biochemical regulation
journal, May 1993
- Kimura, Akira; Inoue, Yoshiharu
- Biochemical Society Transactions, Vol. 21, Issue 2
Application of the Hard and Soft, Acids and Bases (HSAB) Theory to Toxicant–Target Interactions
journal, November 2011
- LoPachin, Richard M.; Gavin, Terrence; DeCaprio, Anthony
- Chemical Research in Toxicology, Vol. 25, Issue 2
Lignocellulosic Biomass: A Review of Conversion Technologies and Fuel Products
journal, November 2015
- Nanda, Sonil; A. Kozinski, Janusz; K. Dalai, Ajay
- Current Biochemical Engineering, Vol. 3, Issue 1
The biorefinery concept: Using biomass instead of oil for producing energy and chemicals
journal, July 2010
- Cherubini, Francesco
- Energy Conversion and Management, Vol. 51, Issue 7
Mechanism of Protein Modification by Glyoxal and Glycolaldehyde, Reactive Intermediates of the Maillard Reaction
journal, April 1995
- Glomb, Marcus A.; Monnier, Vincent M.
- Journal of Biological Chemistry, Vol. 270, Issue 17
Structural insights into the cofactor-assisted substrate recognition of yeast methylglyoxal/isovaleraldehyde reductase Gre2
journal, September 2014
- Guo, Peng-Chao; Bao, Zhang-Zhi; Ma, Xiao-Xiao
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1844, Issue 9
Three genes whose expression is induced by stress inSaccharomyces cerevisiae
journal, July 1999
- Garay-Arroyo, Adriana; Covarrubias, Alejandra A.
- Yeast, Vol. 15, Issue 10A
Protein Misfolding and Inclusion Body Formation in Recombinant Escherichia coli Cells Overexpressing Heat-shock Proteins
journal, May 1996
- Thomas, Jeffrey G.; Baneyx, François
- Journal of Biological Chemistry, Vol. 271, Issue 19
Involvement of yeastYOL151W/GRE2 in ergosterol metabolism
journal, January 2006
- Warringer, Jonas; Blomberg, Anders
- Yeast, Vol. 23, Issue 5
Glycolaldehyde Monomer and Oligomer Equilibria in Aqueous Solution: Comparing Computational Chemistry and NMR Data
journal, March 2013
- Kua, Jeremy; Galloway, Melissa M.; Millage, Katherine D.
- The Journal of Physical Chemistry A, Vol. 117, Issue 14
Comparative metabolic profiling revealed limitations in xylose-fermenting yeast during co-fermentation of glucose and xylose in the presence of inhibitors: Metabolic Profiling Revealed Limitations in Xylose-Fermenting Yeast
journal, August 2013
- Wang, Xin; Jin, Mingjie; Balan, Venkatesh
- Biotechnology and Bioengineering, Vol. 111, Issue 1
Engineering redox cofactor utilization for detoxification of glycolaldehyde, a key inhibitor of bioethanol production, in yeast Saccharomyces cerevisiae
journal, June 2013
- Jayakody, Lahiru N.; Horie, Kenta; Hayashi, Nobuyuki
- Applied Microbiology and Biotechnology, Vol. 97, Issue 14
Molecular Mechanisms of Aldehyde Toxicity: A Chemical Perspective
journal, June 2014
- LoPachin, Richard M.; Gavin, Terrence
- Chemical Research in Toxicology, Vol. 27, Issue 7
Regulation of xylose metabolism in recombinant Saccharomyces cerevisiae
journal, January 2008
- Salusjärvi, Laura; Kankainen, Matti; Soliymani, Rabah
- Microbial Cell Factories, Vol. 7, Issue 1
Dissecting a complex chemical stress: chemogenomic profiling of plant hydrolysates
journal, January 2013
- Skerker, Jeffrey M.; Leon, Dacia; Price, Morgan N.
- Molecular Systems Biology, Vol. 9, Issue 1
GRE2 from Scheffersomyces stipitis as an aldehyde reductase contributes tolerance to aldehyde inhibitors derived from lignocellulosic biomass
journal, March 2016
- Wang, Xu; Ma, Menggen; Liu, Z. Lewis
- Applied Microbiology and Biotechnology, Vol. 100, Issue 15
The glucose metabolite methylglyoxal inhibits expression of the glucose transporter genes by inactivating the cell surface glucose sensors Rgt2 and Snf3 in yeast
journal, March 2016
- Roy, Adhiraj; Hashmi, Salman; Li, Zerui
- Molecular Biology of the Cell, Vol. 27, Issue 5
Improvement of tolerance of Saccharomyces cerevisiae to hot-compressed water-treated cellulose by expression of ADH1
journal, February 2012
- Jayakody, Lahiru N.; Horie, Kenta; Hayashi, Nobuyuki
- Applied Microbiology and Biotechnology, Vol. 94, Issue 1
Two-step hydrolysis of Japanese beech as treated by semi-flow hot-compressed water
journal, October 2009
- Lu, Xin; Yamauchi, Kazuchika; Phaiboonsilpa, Natthanon
- Journal of Wood Science, Vol. 55, Issue 5
Partial flow of compressed-hot water through corn stover to enhance hemicellulose sugar recovery and enzymatic digestibility of cellulose
journal, December 2005
- Liu, Chaogang; Wyman, Charles E.
- Bioresource Technology, Vol. 96, Issue 18, p. 1978-1985
A constraint-based model analysis of the metabolic consequences of increased NADPH oxidation in Saccharomyces cerevisiae
journal, July 2012
- Celton, Magalie; Goelzer, Anne; Camarasa, Carole
- Metabolic Engineering, Vol. 14, Issue 4
Identification and detoxification of glycolaldehyde, an unattended bioethanol fermentation inhibitor
journal, December 2015
- Jayakody, Lahiru N.; Ferdouse, Jannatul; Hayashi, Nobuyuki
- Critical Reviews in Biotechnology, Vol. 37, Issue 2
The VFH1 ( YLL056C ) promoter is vanillin-inducible and enables mRNA translation despite pronounced translation repression caused by severe vanillin stress in Saccharomyces cerevisiae
journal, May 2018
- Nguyen, Trinh Thi My; Ishida, Yoko; Kato, Sae
- Yeast, Vol. 35, Issue 7
Identification of Small Aliphatic Aldehydes in Pretreated Lignocellulosic Feedstocks and Evaluation of Their Inhibitory Effects on Yeast
journal, November 2015
- Cavka, Adnan; Stagge, Stefan; Jönsson, Leif J.
- Journal of Agricultural and Food Chemistry, Vol. 63, Issue 44
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
journal, January 2010
- Ma, Menggen; Liu, Z. Lewis
- BMC Genomics, Vol. 11, Issue 1
Effects of lignocellulose degradation products on ethanol fermentations of glucose and xylose by Saccharomyces cerevisiae, Zymomonas mobilis, Pichia stipitis, and Candida shehatae
journal, August 1996
- Delgenes, J. P.; Moletta, R.; Navarro, J. M.
- Enzyme and Microbial Technology, Vol. 19, Issue 3
The influence of HMF and furfural on redox-balance and energy-state of xylose-utilizing Saccharomyces cerevisiae
journal, January 2013
- Ask, Magnus; Bettiga, Maurizio; Mapelli, Valeria
- Biotechnology for Biofuels, Vol. 6, Issue 1
Deciphering Dynamic Dose Responses of Natural Promoters and Single cis Elements upon Osmotic and Oxidative Stress in Yeast
journal, March 2013
- Dolz-Edo, L.; Rienzo, A.; Poveda-Huertes, D.
- Molecular and Cellular Biology, Vol. 33, Issue 11
Inhibitor tolerance of a recombinant flocculating industrial Saccharomyces cerevisiae strain during glucose and xylose co-fermentation
journal, October 2017
- Li, Yun-Cheng; Gou, Zi-Xi; Zhang, Ying
- Brazilian Journal of Microbiology, Vol. 48, Issue 4
Review of pretreatment processes for lignocellulosic ethanol production, and development of an innovative method
journal, November 2012
- Chiaramonti, David; Prussi, Matteo; Ferrero, Simone
- Biomass and Bioenergy, Vol. 46
Molecular mechanisms of yeast tolerance and in situ detoxification of lignocellulose hydrolysates
journal, March 2011
- Liu, Z. Lewis
- Applied Microbiology and Biotechnology, Vol. 90, Issue 3
Engineered NADH-dependent GRE2 from Saccharomyces cerevisiae by directed enzyme evolution enhances HMF reduction using additional cofactor NADPH
journal, February 2012
- Moon, Jaewoong; Liu, Z. Lewis
- Enzyme and Microbial Technology, Vol. 50, Issue 2
Thermochemical wastewater valorization via enhanced microbial toxicity tolerance
journal, January 2018
- Jayakody, Lahiru N.; Johnson, Christopher W.; Whitham, Jason M.
- Energy & Environmental Science, Vol. 11, Issue 6
Feasibility of xylose fermentation by engineered Saccharomyces cerevisiae overexpressing endogenous aldose reductase ( GRE3 ), xylitol dehydrogenase ( XYL2 ), and xylulokinase ( XYL3 ) from Scheffersomyces stipitis
journal, March 2013
- Kim, Soo Rin; Kwee, Nathania R.; Kim, Heejin
- FEMS Yeast Research, Vol. 13, Issue 3
Integrated control of transporter endocytosis and recycling by the arrestin-related protein Rod1 and the ubiquitin ligase Rsp5
journal, November 2014
- Becuwe, Michel; Léon, Sébastien
- eLife, Vol. 3
Some Recent Advances in Hydrolysis of Biomass in Hot-Compressed Water and Its Comparisons with Other Hydrolysis Methods †
journal, January 2008
- Yu, Yun; Lou, Xia; Wu, Hongwei
- Energy & Fuels, Vol. 22, Issue 1
Single and combined effects of acetic acid, furfural, and sugars on the growth of the pentose-fermenting yeast Meyerozyma guilliermondii
journal, February 2018
- Perna, Michelle dos Santos Cordeiro; Bastos, Reinaldo Gaspar; Ceccato-Antonini, Sandra Regina
- 3 Biotech, Vol. 8, Issue 2
Construction of a Quadruple Auxotrophic Mutant of an Industrial Polyploid Saccharomyces cerevisiae Strain by Using RNA-Guided Cas9 Nuclease
journal, October 2014
- Zhang, Guo-Chang; Kong, In Iok; Kim, Heejin
- Applied and Environmental Microbiology, Vol. 80, Issue 24
Works referencing / citing this record:
Molecular and physiological basis of Saccharomyces cerevisiae tolerance to adverse lignocellulose-based process conditions
journal, November 2018
- Cunha, Joana T.; Romaní, Aloia; Costa, Carlos E.
- Applied Microbiology and Biotechnology, Vol. 103, Issue 1
PKA and HOG signaling contribute separable roles to anaerobic xylose fermentation in yeast engineered for biofuel production
journal, May 2019
- Wagner, Ellen R.; Myers, Kevin S.; Riley, Nicholas M.
- PLOS ONE, Vol. 14, Issue 5
High Gravity Fermentation of Sugarcane Bagasse Hydrolysate by Saccharomyces pastorianus to Produce Economically Distillable Ethanol Concentrations: Necessity of Medium Components Examined
journal, January 2020
- Harcum, Sarah W.; Caldwell, Thomas P.
- Fermentation, Vol. 6, Issue 1
PKA and HOG signaling contribute separable roles to anaerobic xylose fermentation in yeast engineered for biofuel production
posted_content, February 2019
- Wagner, Ellen R.; Myers, Kevin S.; Riley, Nicholas M.
- PLOS ONE
Molecular and physiological basis of Saccharomyces cerevisiae tolerance to adverse lignocellulose-based process conditions
journal, November 2018
- Cunha, Joana T.; Romaní, Aloia; Costa, Carlos E.
- Applied Microbiology and Biotechnology, Vol. 103, Issue 1
Engineered Saccharomyces cerevisiae for lignocellulosic valorization: a review and perspectives on bioethanol production
journal, January 2020
- Cunha, Joana T.; Soares, Pedro O.; Baptista, Sara L.
- Bioengineered, Vol. 11, Issue 1
Sodium Acetate Responses in Saccharomyces cerevisiae and the Ubiquitin Ligase Rsp5
journal, October 2018
- Watcharawipas, Akaraphol; Watanabe, Daisuke; Takagi, Hiroshi
- Frontiers in Microbiology, Vol. 9
Figures / Tables found in this record: