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Title: Rational and Evolutionary Engineering Approaches Uncover a Small Set of Genetic Changes Efficient for Rapid Xylose Fermentation in Saccharomyces cerevisiae

Abstract

Economic bioconversion of plant cell wall hydrolysates into fuels and chemicals has been hampered mainly due to the inability of microorganisms to efficiently co-ferment pentose and hexose sugars, especially glucose and xylose, which are the most abundant sugars in cellulosic hydrolysates. Saccharomyces cerevisiae cannot metabolize xylose due to a lack of xylose-metabolizing enzymes. We developed a rapid and efficient xylose-fermenting S. cerevisiae through rational and inverse metabolic engineering strategies, comprising the optimization of a heterologous xylose-assimilating pathway and evolutionary engineering. Strong and balanced expression levels of the XYL1, XYL2, and XYL3 genes constituting the xyloseassimilating pathway increased ethanol yields and the xylose consumption rates from a mixture of glucose and xylose with little xylitol accumulation. The engineered strain, however, still exhibited a long lag time when metabolizing xylose above 10 g/l as a sole carbon source, defined here as xylose toxicity. Through serial-subcultures on xylose, we isolated evolved strains which exhibited a shorter lag time and improved xylose-fermenting capabilities than the parental strain. Genome sequencing of the evolved strains revealed that mutations in PHO13 causing loss of the Pho13p function are associated with the improved phenotypes of the evolved strains. Crude extracts of a PHO13-overexpressing strain showed a higher phosphatasemore » activity on xylulose-5-phosphate (X-5-P), suggesting that the dephosphorylation of X-5-P by Pho13p might generate a futile cycle with xylulokinase overexpression. While xylose consumption rates by the evolved strains improved substantially as compared to the parental strain, xylose metabolism was interrupted by accumulated acetate. Deletion of ALD6 coding for acetaldehyde dehydrogenase not only prevented acetate accumulation, but also enabled complete and efficient fermentation of xylose as well as a mixture of glucose and xylose by the evolved strain. These findings provide direct guidance for developing industrial strains to produce cellulosic fuels and chemicals« less

Authors:
 [1];  [2];  [1];  [3];  [1];  [2];  [1]
+ Show Author Affiliations
  1. University of Illinois at Urbana-Champaign, IL (United States)
  2. University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
  3. University of Illinois at Urbana-Champaign, IL (United States)=
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Energy Biosciences Institute
OSTI Identifier:
1627587
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 8; Journal Issue: 2; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; xylose; saccharomyces cerevisiae; fermentation; ethanol; genetic engineering; glucose; genomics; single nucleotide polymorphisms

Citation Formats

Kim, Soo Rin, Skerker, Jeffrey M., Kang, Wei, Lesmana, Anastashia, Wei, Na, Arkin, Adam P., and Jin, Yong-Su. Rational and Evolutionary Engineering Approaches Uncover a Small Set of Genetic Changes Efficient for Rapid Xylose Fermentation in Saccharomyces cerevisiae. United States: N. p., 2013. Web. doi:10.1371/journal.pone.0057048.
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Kim, Soo Rin, Skerker, Jeffrey M., Kang, Wei, Lesmana, Anastashia, Wei, Na, Arkin, Adam P., & Jin, Yong-Su. Rational and Evolutionary Engineering Approaches Uncover a Small Set of Genetic Changes Efficient for Rapid Xylose Fermentation in Saccharomyces cerevisiae. United States. https://doi.org/10.1371/journal.pone.0057048
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Kim, Soo Rin, Skerker, Jeffrey M., Kang, Wei, Lesmana, Anastashia, Wei, Na, Arkin, Adam P., and Jin, Yong-Su. Tue . "Rational and Evolutionary Engineering Approaches Uncover a Small Set of Genetic Changes Efficient for Rapid Xylose Fermentation in Saccharomyces cerevisiae". United States. https://doi.org/10.1371/journal.pone.0057048. https://www.osti.gov/servlets/purl/1627587.
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@article{osti_1627587,
title = {Rational and Evolutionary Engineering Approaches Uncover a Small Set of Genetic Changes Efficient for Rapid Xylose Fermentation in Saccharomyces cerevisiae},
author = {Kim, Soo Rin and Skerker, Jeffrey M. and Kang, Wei and Lesmana, Anastashia and Wei, Na and Arkin, Adam P. and Jin, Yong-Su},
abstractNote = {Economic bioconversion of plant cell wall hydrolysates into fuels and chemicals has been hampered mainly due to the inability of microorganisms to efficiently co-ferment pentose and hexose sugars, especially glucose and xylose, which are the most abundant sugars in cellulosic hydrolysates. Saccharomyces cerevisiae cannot metabolize xylose due to a lack of xylose-metabolizing enzymes. We developed a rapid and efficient xylose-fermenting S. cerevisiae through rational and inverse metabolic engineering strategies, comprising the optimization of a heterologous xylose-assimilating pathway and evolutionary engineering. Strong and balanced expression levels of the XYL1, XYL2, and XYL3 genes constituting the xyloseassimilating pathway increased ethanol yields and the xylose consumption rates from a mixture of glucose and xylose with little xylitol accumulation. The engineered strain, however, still exhibited a long lag time when metabolizing xylose above 10 g/l as a sole carbon source, defined here as xylose toxicity. Through serial-subcultures on xylose, we isolated evolved strains which exhibited a shorter lag time and improved xylose-fermenting capabilities than the parental strain. Genome sequencing of the evolved strains revealed that mutations in PHO13 causing loss of the Pho13p function are associated with the improved phenotypes of the evolved strains. Crude extracts of a PHO13-overexpressing strain showed a higher phosphatase activity on xylulose-5-phosphate (X-5-P), suggesting that the dephosphorylation of X-5-P by Pho13p might generate a futile cycle with xylulokinase overexpression. While xylose consumption rates by the evolved strains improved substantially as compared to the parental strain, xylose metabolism was interrupted by accumulated acetate. Deletion of ALD6 coding for acetaldehyde dehydrogenase not only prevented acetate accumulation, but also enabled complete and efficient fermentation of xylose as well as a mixture of glucose and xylose by the evolved strain. These findings provide direct guidance for developing industrial strains to produce cellulosic fuels and chemicals},
doi = {10.1371/journal.pone.0057048},
journal = {PLoS ONE},
number = 2,
volume = 8,
place = {United States},
year = {Tue Feb 26 00:00:00 EST 2013},
month = {Tue Feb 26 00:00:00 EST 2013}
}
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    • DOI: 10.1101/540534

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    • DOI: 10.1074/jbc.m115.657916

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    • DOI: 10.1186/s13068-014-0126-6

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    • DOI: 10.1002/bit.26569

    Sustainable conversion of coffee and other crop wastes to biofuels and bioproducts using coupled biochemical and thermochemical processes in a multi-stage biorefinery concept
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    • Hughes, Stephen R.; López-Núñez, Juan Carlos; Jones, Marjorie A.
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    • DOI: 10.1007/s00253-014-5991-1

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    Absence of Rtt109p, a fungal-specific histone acetyltransferase, results in improved acetic acid tolerance of Saccharomyces cerevisiae
    journal, February 2016

    • Cheng, Cheng; Zhao, Xinqing; Zhang, Mingming
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    Saccharomyces cerevisiae strains for second-generation ethanol production: from academic exploration to industrial implementation
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    • Jansen, Mickel L. A.; Bracher, Jasmine M.; Papapetridis, Ioannis
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    Systematic improvement of isobutanol production from d-xylose in engineered Saccharomyces cerevisiae
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    Advancing Metabolic Engineering of Saccharomyces cerevisiae Using the CRISPR/Cas System
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    • DOI: 10.1007/s00253-019-09829-5

    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)
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    • Ruchala, Justyna; Kurylenko, Olena O.; Dmytruk, Kostyantyn V.
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    • DOI: 10.1007/s10295-019-02242-x

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    • Tsai, Ching-Sung; Kong, In Iok; Lesmana, Anastashia
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    Production of fuels and chemicals from xylose by engineered Saccharomyces cerevisiae: a review and perspective
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    Gene Amplification on Demand Accelerates Cellobiose Utilization in Engineered Saccharomyces cerevisiae
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    • Oh, Eun Joong; Skerker, Jeffrey M.; Kim, Soo Rin
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    • DOI: 10.1128/AEM.00410-16

    Systematic and evolutionary engineering of a xylose isomerase-based pathway in Saccharomyces cerevisiae for efficient conversion yields
    journal, August 2014

    Xylose utilization stimulates mitochondrial production of isobutanol and 2-methyl-1-butanol in Saccharomyces cerevisiae
    journal, September 2019

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