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Title: Evolved hexose transporter enhances xylose uptake and glucose/xylose co-utilization in Saccharomyces cerevisiae

Abstract

Enhancing xylose utilization has been a major focus in Saccharomyces cerevisiae strain-engineering efforts. The incentive for these studies arises from the need to use all sugars in the typical carbon mixtures that comprise standard renewable plant-biomass-based carbon sources. While major advances have been made in developing utilization pathways, the efficient import of five carbon sugars into the cell remains an important bottleneck in this endeavor. Here we use an engineered S. cerevisiae BY4742 strain, containing an established heterologous xylose utilization pathway, and imposed a laboratory evolution regime with xylose as the sole carbon source. We obtained several evolved strains with improved growth phenotypes and evaluated the best candidate using genome resequencing. We observed remarkably few single nucleotide polymorphisms in the evolved strain, among which we confirmed a single amino acid change in the hexose transporter HXT7 coding sequence to be responsible for the evolved phenotype. The mutant HXT7(F79S) shows improved xylose uptake rates (Vmax = 186.4 ± 20.1 nmol·min -1 ·mg -1 ) that allows the S. cerevisiae strain to show significant growth with xylose as the sole carbon source, as well as partial co-utilization of glucose and xylose in a mixed sugar cultivation.

Authors:
 [1];  [1];  [2];  [3];  [1]
+ Show Author Affiliations
  1. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States)
  3. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (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)
OSTI Identifier:
1256065
Alternate Identifier(s):
OSTI ID: 1379040
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Reider Apel, Amanda, Ouellet, Mario, Szmidt-Middleton, Heather, Keasling, Jay D., and Mukhopadhyay, Aindrila. Evolved hexose transporter enhances xylose uptake and glucose/xylose co-utilization in Saccharomyces cerevisiae. United States: N. p., 2016. Web. doi:10.1038/srep19512.
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Reider Apel, Amanda, Ouellet, Mario, Szmidt-Middleton, Heather, Keasling, Jay D., & Mukhopadhyay, Aindrila. Evolved hexose transporter enhances xylose uptake and glucose/xylose co-utilization in Saccharomyces cerevisiae. United States. https://doi.org/10.1038/srep19512
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Reider Apel, Amanda, Ouellet, Mario, Szmidt-Middleton, Heather, Keasling, Jay D., and Mukhopadhyay, Aindrila. Tue . "Evolved hexose transporter enhances xylose uptake and glucose/xylose co-utilization in Saccharomyces cerevisiae". United States. https://doi.org/10.1038/srep19512. https://www.osti.gov/servlets/purl/1256065.
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@article{osti_1256065,
title = {Evolved hexose transporter enhances xylose uptake and glucose/xylose co-utilization in Saccharomyces cerevisiae},
author = {Reider Apel, Amanda and Ouellet, Mario and Szmidt-Middleton, Heather and Keasling, Jay D. and Mukhopadhyay, Aindrila},
abstractNote = {Enhancing xylose utilization has been a major focus in Saccharomyces cerevisiae strain-engineering efforts. The incentive for these studies arises from the need to use all sugars in the typical carbon mixtures that comprise standard renewable plant-biomass-based carbon sources. While major advances have been made in developing utilization pathways, the efficient import of five carbon sugars into the cell remains an important bottleneck in this endeavor. Here we use an engineered S. cerevisiae BY4742 strain, containing an established heterologous xylose utilization pathway, and imposed a laboratory evolution regime with xylose as the sole carbon source. We obtained several evolved strains with improved growth phenotypes and evaluated the best candidate using genome resequencing. We observed remarkably few single nucleotide polymorphisms in the evolved strain, among which we confirmed a single amino acid change in the hexose transporter HXT7 coding sequence to be responsible for the evolved phenotype. The mutant HXT7(F79S) shows improved xylose uptake rates (Vmax = 186.4 ± 20.1 nmol·min -1 ·mg -1 ) that allows the S. cerevisiae strain to show significant growth with xylose as the sole carbon source, as well as partial co-utilization of glucose and xylose in a mixed sugar cultivation.},
doi = {10.1038/srep19512},
journal = {Scientific Reports},
number = ,
volume = 6,
place = {United States},
year = {Tue Jan 19 00:00:00 EST 2016},
month = {Tue Jan 19 00:00:00 EST 2016}
}
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https://doi.org/10.1038/srep19512
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Comparison of heterologous xylose transporters in recombinant Saccharomyces cerevisiae
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  • Runquist, David; Hahn-Hagerdal, Barbel; Radstrom, Peter
  • Biotechnology for Biofuels, Vol. 3, Issue 1
  • DOI: 10.1186/1754-6834-3-5

Discovery and characterization of novel d-xylose-specific transporters from Neurospora crassa and Pichia stipitis
journal, January 2010

  • Du, Jing; Li, Sijin; Zhao, Huimin
  • Molecular BioSystems, Vol. 6, Issue 11
  • DOI: 10.1039/c0mb00007h

Employing a combinatorial expression approach to characterize xylose utilization in Saccharomyces cerevisiae
journal, September 2014

Expression of a heterologous xylose transporter in a Saccharomyces cerevisiae strain engineered to utilize xylose improves aerobic xylose consumption
journal, July 2008

  • Hector, Ronald E.; Qureshi, Nasib; Hughes, Stephen R.
  • Applied Microbiology and Biotechnology, Vol. 80, Issue 4
  • DOI: 10.1007/s00253-008-1583-2

Employing a combinatorial expression approach to characterize xylose utilization in Saccharomyces cerevisiae
journal, September 2014

The genome sequence of the popular hexose-transport-deficient Saccharomyces cerevisiae strain EBY.VW4000 reveals LoxP/Cre-induced translocations and gene loss
journal, February 2015

  • Solis-Escalante, Daniel; van den Broek, Marcel; Kuijpers, Niels G. A.
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A history of research on yeasts 9: regulation of sugar metabolism
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Isolation of xylose isomerases by sequence- and function-based screening from a soil metagenomic library
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Effects of xylulokinase activity on ethanol production from d-xylulose by recombinant Saccharomyces cerevisiae
journal, October 2003

Cloning and characterization of three genes (SUT1-3 ) encoding glucose transporters of the yeast Pichia stipitis
journal, February 1999

Competition between pentoses and glucose during uptake and catabolism in recombinant Saccharomyces cerevisiae
journal, January 2012

Design, implementation and practice of JBEI-ICE: an open source biological part registry platform and tools
journal, June 2012

  • Ham, T. S.; Dmytriv, Z.; Plahar, H.
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Xylose transport studies with xylose-utilizing Saccharomyces cerevisiae strains expressing heterologous and homologous permeases
journal, December 2006

  • Saloheimo, Anu; Rauta, Jenita; Stasyk, Oleh V.
  • Applied Microbiology and Biotechnology, Vol. 74, Issue 5, p. 1041-1052
  • DOI: 10.1007/s00253-006-0747-1

Hexose and pentose transport in ascomycetous yeasts: an overview
journal, June 2009

A molecular transporter engineering approach to improving xylose catabolism in Saccharomyces cerevisiae
journal, July 2012

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    Engineering xylose metabolism for production of polyhydroxybutyrate in the non-model bacterium Burkholderia sacchari
    journal, May 2018

    • Guamán, Linda P.; Barba-Ostria, Carlos; Zhang, Fuzhong
    • Microbial Cell Factories, Vol. 17, Issue 1
    • DOI: 10.1186/s12934-018-0924-9

    Production of fuels and chemicals from xylose by engineered Saccharomyces cerevisiae: a review and perspective
    journal, May 2017

    Engineering yeast with bifunctional minicellulosome and cellodextrin pathway for co-utilization of cellulose-mixed sugars
    journal, July 2016

    Restoration of biofuel production levels and increased tolerance under ionic liquid stress is enabled by a mutation in the essential Escherichia coli gene cydC
    journal, October 2018

    A toolset of constitutive promoters for metabolic engineering of Rhodosporidium toruloides
    journal, June 2019

    • Nora, Luísa Czamanski; Wehrs, Maren; Kim, Joonhoon
    • Microbial Cell Factories, Vol. 18, Issue 1
    • DOI: 10.1186/s12934-019-1167-0

    Engineering of Pentose Transport in Saccharomyces cerevisiae for Biotechnological Applications
    journal, January 2020

    • Nijland, Jeroen G.; Driessen, Arnold J. M.
    • Frontiers in Bioengineering and Biotechnology, Vol. 7
    • DOI: 10.3389/fbioe.2019.00464

    Production of fuels and chemicals from xylose by engineered Saccharomyces cerevisiae: a review and perspective
    journal, May 2017

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