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

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.

doi:10.1371/journal.pone.0107499

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

Journal Article · Mon Sep 15 04:00:00 EDT 2014 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0107499· OSTI ID:1627733

Parreiras, Lucas S. ^[1]; Breuer, Rebecca J. ^[2]; Avanasi Narasimhan, Ragothaman ^[2]; Higbee, Alan J. ^[3]; La Reau, Alex ^[2]; Tremaine, Mary ^[2]; Qin, Li ^[2]; Willis, Laura B. ^[4]; Bice, Benjamin D. ^[2]; Bonfert, Brandi L. ^[5]; Pinhancos, Rebeca C. ^[5]; Balloon, Allison J. ^[5]; Uppugundla, Nirmal ^[6]; Liu, Tongjun ^[7]; Li, Chenlin ^[8]; Tanjore, Deepti ^[8]; Ong, Irene M. ^[2]; Li, Haibo ^[2]; Pohlmann, Edward L. ^[2]; Serate, Jose ^[2] more »

Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center; DOE/OSTI
Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center
Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center; Univ. of Wisconsin, Madison, WI (United States). Dept. of Chemistry
Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
Univ. of Wisconsin, Madison, WI (United States). Dept. of Chemistry
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.
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
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Advanced Biofuels Process Demonstration Unit
Joint BioEnergy Institute (JBEI), Emeryville, CA (United States)
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
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.
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
Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center; Univ. of Wisconsin, Madison, WI (United States). Lab. of Genetics

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.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: AC02-05CH11231; FC02-07ER64494

OSTI ID:: 1627733

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 9 Vol. 9; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Natural Variation in the Multidrug Efflux Pump SGE1 Underlies Ionic Liquid Tolerance in Yeast Higgins, Douglas A.; Young, Megan K. M.; Tremaine, Mary Genetics, Vol. 210, Issue 1 https://doi.org/10.1534/genetics.118.301161	journal	July 2018
Multiomic Fermentation Using Chemically Defined Synthetic Hydrolyzates Revealed Multiple Effects of Lignocellulose-Derived Inhibitors on Cell Physiology and Xylose Utilization in Zymomonas mobilis Zhang, Yaoping; Vera, Jessica M.; Xie, Dan Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02596	journal	November 2019
Emerging Technologies for the Production of Renewable Liquid Transport Fuels from Biomass Sources Enriched in Plant Cell Walls Tan, Hwei-Ting; Corbin, Kendall R.; Fincher, Geoffrey B. Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01854	journal	December 2016
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Systems Metabolic Engineering of Escherichia coli Improves Coconversion of Lignocellulose‐Derived Sugars Kim, Joonhoon; Tremaine, Mary; Grass, Jeffrey A. Biotechnology Journal, Vol. 14, Issue 9 https://doi.org/10.1002/biot.201800441	journal	July 2019
Chromosomal mutations in Escherichia coli that improve tolerance to nonvolatile side‐products from dilute acid treatment of sugarcane bagasse Shi, Aiqin; Yomano, Lorraine P.; York, Sean W. Biotechnology and Bioengineering, Vol. 117, Issue 1 https://doi.org/10.1002/bit.27189	journal	November 2019
Engineering and Evolution of Saccharomyces cerevisiae to Produce Biofuels and Chemicals Turner, Timothy L.; Kim, Heejin; Kong, In Iok Synthetic Biology – Metabolic Engineering https://doi.org/10.1007/10_2016_22	book	January 2016
Modeling Microbial Growth Curves with GCAT Bukhman, Yury V.; DiPiazza, Nathan W.; Piotrowski, Jeff BioEnergy Research, Vol. 8, Issue 3 https://doi.org/10.1007/s12155-015-9584-3	journal	February 2015
Optimization of low-temperature energy-efficient pretreatment for enhanced saccharification and fermentation of Conocarpus erectus leaves to produce ethanol using Saccharomyces cerevisiae Rehman, Omama; Shahid, Ayesha; Liu, Chen-Guang Biomass Conversion and Biorefinery https://doi.org/10.1007/s13399-019-00529-8	journal	November 2019
Toward lower cost cellulosic biofuel production using ammonia based pretreatment technologies Jin, Mingjie; da Costa Sousa, Leonardo; Schwartz, Christopher Green Chemistry, Vol. 18, Issue 4 https://doi.org/10.1039/c5gc02433a	journal	January 2016
Enhanced scale and scope of genome engineering and regulation using CRISPR/Cas in Saccharomyces cerevisiae Deaner, Matthew; Alper, Hal S. FEMS Yeast Research, Vol. 19, Issue 7 https://doi.org/10.1093/femsyr/foz076	journal	October 2019
PKA and HOG signaling contribute separable roles to anaerobic xylose fermentation in yeast engineered for biofuel production Wagner, Ellen R.; Myers, Kevin S.; Riley, Nicholas M. PLOS ONE https://doi.org/10.1101/540534	posted_content	February 2019
Diverse lignocellulosic feedstocks can achieve high field-scale ethanol yields while providing flexibility for the biorefinery and landscape-level environmental benefits Zhang, Yaoping; Oates, Lawrence G.; Serate, Jose GCB Bioenergy, Vol. 10, Issue 11 https://doi.org/10.1111/gcbb.12533	journal	July 2018
Chemical genomic guided engineering of gamma-valerolactone tolerant yeast Bottoms, Scott; Dickinson, Quinn; McGee, Mick Microbial Cell Factories, Vol. 17, Issue 1 https://doi.org/10.1186/s12934-017-0848-9	journal	January 2018
Inhibition of microbial biofuel production in drought-stressed switchgrass hydrolysate Ong, Rebecca Garlock; Higbee, Alan; Bottoms, Scott Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0657-0	journal	November 2016
Disruption of the transcription factors Thi2p and Nrm1p alleviates the post-glucose effect on xylose utilization in Saccharomyces cerevisiae Wei, Shan; Liu, Yanan; Wu, Meiling Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1112-1	journal	April 2018
Improved simultaneous co-fermentation of glucose and xylose by Saccharomyces cerevisiae for efficient lignocellulosic biorefinery Hoang Nguyen Tran, Phuong; Ko, Ja Kyong; Gong, Gyeongtaek Biotechnology for Biofuels, Vol. 13, Issue 1 https://doi.org/10.1186/s13068-019-1641-2	journal	January 2020
Directed Evolution Reveals Unexpected Epistatic Interactions That Alter Metabolic Regulation and Enable Anaerobic Xylose Use by Saccharomyces cerevisiae Sato, Trey K.; Tremaine, Mary; Parreiras, Lucas S. PLOS Genetics, Vol. 12, Issue 10 https://doi.org/10.1371/journal.pgen.1006372	journal	October 2016
Water-soluble phenolic compounds produced from extractive ammonia pretreatment exerted binary inhibitory effects on yeast fermentation using synthetic hydrolysate Xue, Saisi; Jones, A. Daniel; Sousa, Leonardo PLOS ONE, Vol. 13, Issue 3 https://doi.org/10.1371/journal.pone.0194012	journal	March 2018
PKA and HOG signaling contribute separable roles to anaerobic xylose fermentation in yeast engineered for biofuel production Wagner, Ellen R.; Myers, Kevin S.; Riley, Nicholas M. PLOS ONE, Vol. 14, Issue 5 https://doi.org/10.1371/journal.pone.0212389	journal	May 2019

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