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Title: Engineering and Two-Stage Evolution of a Lignocellulosic Hydrolysate-Tolerant Saccharomyces cerevisiae Strain for Anaerobic Fermentation of Xylose from AFEX Pretreated Corn Stover

Abstract

The inability of the yeast Saccharomyces cerevisiae to ferment xylose effectively under anaerobic conditions is a major barrier to economical production of lignocellulosic biofuels. Although genetic approaches have enabled engineering of S. cerevisiae to convert xylose efficiently into ethanol in defined lab medium, few strains are able to ferment xylose from lignocellulosic hydrolysates in the absence of oxygen. This limited xylose conversion is believed to result from small molecules generated during biomass pretreatment and hydrolysis, which induce cellular stress and impair metabolism. Here, we describe the development of a xylose-fermenting S. cerevisiae strain with tolerance to a range of pretreated and hydrolyzed lignocellulose, including Ammonia Fiber Expansion (AFEX)-pretreated corn stover hydrolysate (ACSH). We genetically engineered a hydrolysate-resistant yeast strain with bacterial xylose isomerase and then applied two separate stages of aerobic and anaerobic directed evolution. The emergent S. cerevisiae strain rapidly converted xylose from lab medium and ACSH to ethanol under strict anaerobic conditions. Metabolomic, genetic and biochemical analyses suggested that a missense mutation in GRE3, which was acquired during the anaerobic evolution, contributed toward improved xylose conversion by reducing intracellular production of xylitol, an inhibitor of xylose isomerase. These results validate our combinatorial approach, which utilized phenotypic strain selection,more » rational engineering and directed evolution for the generation of a robust S. cerevisiae strain with the ability to ferment xylose anaerobically from ACSH.« less

Authors:
 [1];  [1];  [1];  [2];  [1];  [1];  [1];  [3];  [1];  [4];  [4];  [4];  [5];  [6];  [7];  [7];  [1];  [1];  [1];  [1] more »;  [1];  [8];  [9];  [4];  [4];  [10];  [10];  [1];  [1];  [11];  [12];  [1] « less
+ Show Author Affiliations
  1. Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center
  2. Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center; Univ. of Wisconsin, Madison, WI (United States). Dept. of Chemistry
  3. Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
  4. Univ. of Wisconsin, Madison, WI (United States). Dept. of Chemistry
  5. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Great Bioenergy Research Center; Michigan State Univ., East Lansing, MI (United States). Dept. of Chemical Engineering and Materials Science. Biomass Conversion Research Lab.
  6. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Great Bioenergy Research Center; Qilu Univ. of Technology, Jinan (China). School of Food and Bioengineering
  7. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Advanced Biofuels Process Demonstration Unit
  8. Joint BioEnergy Institute (JBEI), Emeryville, CA (United States)
  9. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Great Bioenergy Research Center; Michigan State Univ., East Lansing, MI (United States). Dept. of Chemical Engineering and Materials Science; Michigan State Univ., East Lansing, MI (United States). Dept. of Biosystems and Agricultural Engineering; Lulea Univ. of Technology (Sweden). Division of Sustainable Process Engineering
  10. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Great Bioenergy Research Center; Michigan State Univ., East Lansing, MI (United States). Dept. of Chemical Engineering and Materials Science. Biomass Conversion Research Lab.
  11. Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center; Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology; Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry
  12. Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center; Univ. of Wisconsin, Madison, WI (United States). Lab. of Genetics
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division
OSTI Identifier:
1627733
Grant/Contract Number:  
AC02-05CH11231; FC02-07ER64494
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 9; Journal Issue: 9; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES; Science & Technology - Other Topics

Citation Formats

Parreiras, Lucas S., Breuer, Rebecca J., Avanasi Narasimhan, Ragothaman, Higbee, Alan J., La Reau, Alex, Tremaine, Mary, Qin, Li, Willis, Laura B., Bice, Benjamin D., Bonfert, Brandi L., Pinhancos, Rebeca C., Balloon, Allison J., Uppugundla, Nirmal, Liu, Tongjun, Li, Chenlin, Tanjore, Deepti, Ong, Irene M., Li, Haibo, Pohlmann, Edward L., Serate, Jose, Withers, Sydnor T., Simmons, Blake A., Hodge, David B., Westphall, Michael S., Coon, Joshua J., Dale, Bruce E., Balan, Venkatesh, Keating, David H., Zhang, Yaoping, Landick, Robert, Gasch, Audrey P., and Sato, Trey K. Engineering and Two-Stage Evolution of a Lignocellulosic Hydrolysate-Tolerant Saccharomyces cerevisiae Strain for Anaerobic Fermentation of Xylose from AFEX Pretreated Corn Stover. United States: N. p., 2014. Web. doi:10.1371/journal.pone.0107499.
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Parreiras, Lucas S., Breuer, Rebecca J., Avanasi Narasimhan, Ragothaman, Higbee, Alan J., La Reau, Alex, Tremaine, Mary, Qin, Li, Willis, Laura B., Bice, Benjamin D., Bonfert, Brandi L., Pinhancos, Rebeca C., Balloon, Allison J., Uppugundla, Nirmal, Liu, Tongjun, Li, Chenlin, Tanjore, Deepti, Ong, Irene M., Li, Haibo, Pohlmann, Edward L., Serate, Jose, Withers, Sydnor T., Simmons, Blake A., Hodge, David B., Westphall, Michael S., Coon, Joshua J., Dale, Bruce E., Balan, Venkatesh, Keating, David H., Zhang, Yaoping, Landick, Robert, Gasch, Audrey P., & Sato, Trey K. Engineering and Two-Stage Evolution of a Lignocellulosic Hydrolysate-Tolerant Saccharomyces cerevisiae Strain for Anaerobic Fermentation of Xylose from AFEX Pretreated Corn Stover. United States. https://doi.org/10.1371/journal.pone.0107499
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Parreiras, Lucas S., Breuer, Rebecca J., Avanasi Narasimhan, Ragothaman, Higbee, Alan J., La Reau, Alex, Tremaine, Mary, Qin, Li, Willis, Laura B., Bice, Benjamin D., Bonfert, Brandi L., Pinhancos, Rebeca C., Balloon, Allison J., Uppugundla, Nirmal, Liu, Tongjun, Li, Chenlin, Tanjore, Deepti, Ong, Irene M., Li, Haibo, Pohlmann, Edward L., Serate, Jose, Withers, Sydnor T., Simmons, Blake A., Hodge, David B., Westphall, Michael S., Coon, Joshua J., Dale, Bruce E., Balan, Venkatesh, Keating, David H., Zhang, Yaoping, Landick, Robert, Gasch, Audrey P., and Sato, Trey K. Mon . "Engineering and Two-Stage Evolution of a Lignocellulosic Hydrolysate-Tolerant Saccharomyces cerevisiae Strain for Anaerobic Fermentation of Xylose from AFEX Pretreated Corn Stover". United States. https://doi.org/10.1371/journal.pone.0107499. https://www.osti.gov/servlets/purl/1627733.
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@article{osti_1627733,
title = {Engineering and Two-Stage Evolution of a Lignocellulosic Hydrolysate-Tolerant Saccharomyces cerevisiae Strain for Anaerobic Fermentation of Xylose from AFEX Pretreated Corn Stover},
author = {Parreiras, Lucas S. and Breuer, Rebecca J. and Avanasi Narasimhan, Ragothaman and Higbee, Alan J. and La Reau, Alex and Tremaine, Mary and Qin, Li and Willis, Laura B. and Bice, Benjamin D. and Bonfert, Brandi L. and Pinhancos, Rebeca C. and Balloon, Allison J. and Uppugundla, Nirmal and Liu, Tongjun and Li, Chenlin and Tanjore, Deepti and Ong, Irene M. and Li, Haibo and Pohlmann, Edward L. and Serate, Jose and Withers, Sydnor T. and Simmons, Blake A. and Hodge, David B. and Westphall, Michael S. and Coon, Joshua J. and Dale, Bruce E. and Balan, Venkatesh and Keating, David H. and Zhang, Yaoping and Landick, Robert and Gasch, Audrey P. and Sato, Trey K.},
abstractNote = {The inability of the yeast Saccharomyces cerevisiae to ferment xylose effectively under anaerobic conditions is a major barrier to economical production of lignocellulosic biofuels. Although genetic approaches have enabled engineering of S. cerevisiae to convert xylose efficiently into ethanol in defined lab medium, few strains are able to ferment xylose from lignocellulosic hydrolysates in the absence of oxygen. This limited xylose conversion is believed to result from small molecules generated during biomass pretreatment and hydrolysis, which induce cellular stress and impair metabolism. Here, we describe the development of a xylose-fermenting S. cerevisiae strain with tolerance to a range of pretreated and hydrolyzed lignocellulose, including Ammonia Fiber Expansion (AFEX)-pretreated corn stover hydrolysate (ACSH). We genetically engineered a hydrolysate-resistant yeast strain with bacterial xylose isomerase and then applied two separate stages of aerobic and anaerobic directed evolution. The emergent S. cerevisiae strain rapidly converted xylose from lab medium and ACSH to ethanol under strict anaerobic conditions. Metabolomic, genetic and biochemical analyses suggested that a missense mutation in GRE3, which was acquired during the anaerobic evolution, contributed toward improved xylose conversion by reducing intracellular production of xylitol, an inhibitor of xylose isomerase. These results validate our combinatorial approach, which utilized phenotypic strain selection, rational engineering and directed evolution for the generation of a robust S. cerevisiae strain with the ability to ferment xylose anaerobically from ACSH.},
doi = {10.1371/journal.pone.0107499},
journal = {PLoS ONE},
number = 9,
volume = 9,
place = {United States},
year = {Mon Sep 15 00:00:00 EDT 2014},
month = {Mon Sep 15 00:00:00 EDT 2014}
}
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    Natural Variation in the Multidrug Efflux Pump SGE1 Underlies Ionic Liquid Tolerance in Yeast
    journal, July 2018

    Mechanism of imidazolium ionic liquids toxicity in Saccharomyces cerevisiae and rational engineering of a tolerant, xylose-fermenting strain
    journal, January 2016

    Systematic improvement of isobutanol production from d-xylose in engineered Saccharomyces cerevisiae
    journal, October 2019

    Increasing the economic value of lignocellulosic stillage through medium-chain fatty acid production
    journal, July 2018

    • Scarborough, Matthew J.; Lynch, Griffin; Dickson, Mitch
    • Biotechnology for Biofuels, Vol. 11, Issue 1
    • DOI: 10.1186/s13068-018-1193-x

    Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production
    journal, March 2017

    • Peris, David; Moriarty, Ryan V.; Alexander, William G.
    • Biotechnology for Biofuels, Vol. 10, Issue 1
    • DOI: 10.1186/s13068-017-0763-7

    Genome Assembly of a Highly Aldehyde-Resistant Saccharomyces cerevisiae SA1-Derived Industrial Strain
    journal, March 2019

    • Nagamatsu, Sheila Tiemi; Teixeira, Gleidson Silva; de Mello, Fellipe da Silveira Bezerra
    • Microbiology Resource Announcements, Vol. 8, Issue 13
    • DOI: 10.1128/mra.00071-19

    Chromosomal mutations in Escherichia coli that improve tolerance to nonvolatile side‐products from dilute acid treatment of sugarcane bagasse
    journal, November 2019

    • Shi, Aiqin; Yomano, Lorraine P.; York, Sean W.
    • Biotechnology and Bioengineering, Vol. 117, Issue 1
    • DOI: 10.1002/bit.27189

    Mechanism of imidazolium ionic liquids toxicity in Saccharomyces cerevisiae and rational engineering of a tolerant, xylose-fermenting strain
    journal, January 2016

    Construction of advanced producers of first- and second-generation ethanol in Saccharomyces cerevisiae and selected species of non-conventional yeasts (Scheffersomyces stipitis, Ogataea polymorpha)
    journal, October 2019

    • Ruchala, Justyna; Kurylenko, Olena O.; Dmytruk, Kostyantyn V.
    • Journal of Industrial Microbiology & Biotechnology, Vol. 47, Issue 1
    • DOI: 10.1007/s10295-019-02242-x

    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
    • DOI: 10.1101/540534

    Inhibition of microbial biofuel production in drought-stressed switchgrass hydrolysate
    journal, November 2016

    • Ong, Rebecca Garlock; Higbee, Alan; Bottoms, Scott
    • Biotechnology for Biofuels, Vol. 9, Issue 1
    • DOI: 10.1186/s13068-016-0657-0

    Improved simultaneous co-fermentation of glucose and xylose by Saccharomyces cerevisiae for efficient lignocellulosic biorefinery
    journal, January 2020

    • Hoang Nguyen Tran, Phuong; Ko, Ja Kyong; Gong, Gyeongtaek
    • Biotechnology for Biofuels, Vol. 13, Issue 1
    • DOI: 10.1186/s13068-019-1641-2

    Chemical genomic guided engineering of gamma-valerolactone tolerant yeast
    journal, January 2018

    Systems Metabolic Engineering of Escherichia coli Improves Coconversion of Lignocellulose‐Derived Sugars
    journal, July 2019

    • Kim, Joonhoon; Tremaine, Mary; Grass, Jeffrey A.
    • Biotechnology Journal, Vol. 14, Issue 9
    • DOI: 10.1002/biot.201800441

    PKA and HOG signaling contribute separable roles to anaerobic xylose fermentation in yeast engineered for biofuel production
    journal, May 2019

    Construction of advanced producers of first- and second-generation ethanol in Saccharomyces cerevisiae and selected species of non-conventional yeasts (Scheffersomyces stipitis, Ogataea polymorpha)
    journal, October 2019

    • Ruchala, Justyna; Kurylenko, Olena O.; Dmytruk, Kostyantyn V.
    • Journal of Industrial Microbiology & Biotechnology, Vol. 47, Issue 1
    • DOI: 10.1007/s10295-019-02242-x

    Natural Variation in the Multidrug Efflux Pump SGE1 Underlies Ionic Liquid Tolerance in Yeast
    journal, July 2018

    Systematic improvement of isobutanol production from d-xylose in engineered Saccharomyces cerevisiae
    journal, October 2019

    Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production
    journal, March 2017

    • Peris, David; Moriarty, Ryan V.; Alexander, William G.
    • Biotechnology for Biofuels, Vol. 10, Issue 1
    • DOI: 10.1186/s13068-017-0763-7

    Enhanced scale and scope of genome engineering and regulation using CRISPR/Cas in Saccharomyces cerevisiae
    journal, October 2019

    Modeling Microbial Growth Curves with GCAT
    journal, February 2015

    Genome Sequence and Analysis of a Stress-Tolerant, Wild-Derived Strain of Saccharomyces cerevisiae Used in Biofuels Research
    journal, April 2016

    • McIlwain, Sean J.; Peris, David; Sardi, Maria
    • G3: Genes|Genomes|Genetics, Vol. 6, Issue 6
    • DOI: 10.1534/g3.116.029389

    Emerging Technologies for the Production of Renewable Liquid Transport Fuels from Biomass Sources Enriched in Plant Cell Walls
    journal, December 2016

    • Tan, Hwei-Ting; Corbin, Kendall R.; Fincher, Geoffrey B.
    • Frontiers in Plant Science, Vol. 7
    • DOI: 10.3389/fpls.2016.01854

    Enabling technologies for utilization of maize as a bioenergy feedstock
    journal, November 2019

    • Choudhary, Mukesh; Singh, Alla; Gupta, Mamta
    • Biofuels, Bioproducts and Biorefining, Vol. 14, Issue 2
    • DOI: 10.1002/bbb.2060

    EasyClone 2.0: expanded toolkit of integrative vectors for stable gene expression in industrial Saccharomyces cerevisiae strains
    journal, November 2015

    • Stovicek, Vratislav; Borja, Gheorghe M.; Forster, Jochen
    • Journal of Industrial Microbiology and Biotechnology, Vol. 42, Issue 11
    • DOI: 10.1007/s10295-015-1684-8

    Metabolic engineering of Saccharomyces cerevisiae to produce a reduced viscosity oil from lignocellulose
    journal, March 2017

    • Tran, Tam N. T.; Breuer, Rebecca J.; Avanasi Narasimhan, Ragothaman
    • Biotechnology for Biofuels, Vol. 10, Issue 1
    • DOI: 10.1186/s13068-017-0751-y

    Metabolic engineering of Saccharomyces cerevisiae to produce a reduced viscosity oil from lignocellulose
    journal, March 2017

    • Tran, Tam N. T.; Breuer, Rebecca J.; Avanasi Narasimhan, Ragothaman
    • Biotechnology for Biofuels, Vol. 10, Issue 1
    • DOI: 10.1186/s13068-017-0751-y
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