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Title: Natural Variation in the Multidrug Efflux Pump SGE1 Underlies Ionic Liquid Tolerance in Yeast

Abstract

Imidazolium ionic liquids (IILs) have a range of biotechnological applications, including as pretreatment solvents that extract cellulose from plant biomass for microbial fermentation into sustainable bioenergy. However, residual levels of IILs, such as 1-ethyl-3-methylimidazolium chloride ([C 2C 1im]Cl), are toxic to biofuel-producing microbes, including the yeast Saccharomyces cerevisiae. S. cerevisiae strains isolated from diverse ecological niches differ in genomic sequence and in phenotypes potentially beneficial for industrial applications, including tolerance to inhibitory compounds present in hydrolyzed plant feedstocks. We evaluated >100 genome-sequenced S. cerevisiae strains for tolerance to [C 2C 1im]Cl and identified one strain with exceptional tolerance. By screening a library of genomic DNA fragments from the [C 2C 1im]Cl-tolerant strain for improved IIL tolerance, we identified SGE1, which encodes a plasma membrane multidrug efflux pump, and a previously uncharacterized gene that we named ionic liquid tolerance 1 (ILT1), which encodes a predicted membrane protein. Analyses of SGE1 sequences from our panel of S. cerevisiae strains together with growth phenotypes implicated two single nucleotide polymorphisms (SNPs) that associated with IIL tolerance and sensitivity. We confirmed these phenotypic effects by transferring the SGE1 SNPs into a [C 2C 1im]Cl-sensitive yeast strain using CRISPR/Cas9 genome editing. Further studies indicated that thesemore » SNPs affect Sge1 protein stability and cell surface localization, influencing the amount of toxic IILs that cells can pump out of the cytoplasm. Our results highlight the general potential for discovering useful biotechnological functions from untapped natural sequence variation and provide functional insight into emergent SGE1 alleles with reduced capacities to protect against IIL toxicity.« less

Authors:
 [1];  [2];  [2];  [2];  [2];  [2];  [2];  [2]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2];  [2];  [3]; ORCiD logo [1];  [2]; ORCiD logo [1]; ORCiD logo [2]
  1. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  2. Univ. of Wisconsin, Madison, WI (United States)
  3. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); UC Laboratory Fees Research Program (LFRP) (UCRI)
OSTI Identifier:
1477368
Alternate Identifier(s):
OSTI ID: 1506442
Grant/Contract Number:  
[AC02-05CH11231; SC0018409; FC02-07ER64494]
Resource Type:
Accepted Manuscript
Journal Name:
Genetics
Additional Journal Information:
[ Journal Volume: 210; Journal Issue: 1]; Journal ID: ISSN 0016-6731
Publisher:
Genetics Society of America
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 09 BIOMASS FUELS; SACCHAROMYCES CEREVISIAE; YEASTIONIC LIQUID; NATURAL VARIATION; MAJOR FACILITATOR SUPERFAMILY; BIOFUELS; TOXIN TOLERANCE

Citation Formats

Higgins, Douglas A., Young, Megan K. M., Tremaine, Mary, Sardi, Maria, Fletcher, Jenna M., Agnew, Margaret, Liu, Lisa, Dickinson, Quinn, Peris, David, Wrobel, Russell L., Hittinger, Chris Todd, Gasch, Audrey P., Singer, Steven W., Simmons, Blake A., Landick, Robert, Thelen, Michael P., and Sato, Trey K. Natural Variation in the Multidrug Efflux Pump SGE1 Underlies Ionic Liquid Tolerance in Yeast. United States: N. p., 2018. Web. doi:10.1534/genetics.118.301161.
Higgins, Douglas A., Young, Megan K. M., Tremaine, Mary, Sardi, Maria, Fletcher, Jenna M., Agnew, Margaret, Liu, Lisa, Dickinson, Quinn, Peris, David, Wrobel, Russell L., Hittinger, Chris Todd, Gasch, Audrey P., Singer, Steven W., Simmons, Blake A., Landick, Robert, Thelen, Michael P., & Sato, Trey K. Natural Variation in the Multidrug Efflux Pump SGE1 Underlies Ionic Liquid Tolerance in Yeast. United States. doi:10.1534/genetics.118.301161.
Higgins, Douglas A., Young, Megan K. M., Tremaine, Mary, Sardi, Maria, Fletcher, Jenna M., Agnew, Margaret, Liu, Lisa, Dickinson, Quinn, Peris, David, Wrobel, Russell L., Hittinger, Chris Todd, Gasch, Audrey P., Singer, Steven W., Simmons, Blake A., Landick, Robert, Thelen, Michael P., and Sato, Trey K. Wed . "Natural Variation in the Multidrug Efflux Pump SGE1 Underlies Ionic Liquid Tolerance in Yeast". United States. doi:10.1534/genetics.118.301161. https://www.osti.gov/servlets/purl/1477368.
@article{osti_1477368,
title = {Natural Variation in the Multidrug Efflux Pump SGE1 Underlies Ionic Liquid Tolerance in Yeast},
author = {Higgins, Douglas A. and Young, Megan K. M. and Tremaine, Mary and Sardi, Maria and Fletcher, Jenna M. and Agnew, Margaret and Liu, Lisa and Dickinson, Quinn and Peris, David and Wrobel, Russell L. and Hittinger, Chris Todd and Gasch, Audrey P. and Singer, Steven W. and Simmons, Blake A. and Landick, Robert and Thelen, Michael P. and Sato, Trey K.},
abstractNote = {Imidazolium ionic liquids (IILs) have a range of biotechnological applications, including as pretreatment solvents that extract cellulose from plant biomass for microbial fermentation into sustainable bioenergy. However, residual levels of IILs, such as 1-ethyl-3-methylimidazolium chloride ([C2C1im]Cl), are toxic to biofuel-producing microbes, including the yeast Saccharomyces cerevisiae. S. cerevisiae strains isolated from diverse ecological niches differ in genomic sequence and in phenotypes potentially beneficial for industrial applications, including tolerance to inhibitory compounds present in hydrolyzed plant feedstocks. We evaluated >100 genome-sequenced S. cerevisiae strains for tolerance to [C2C1im]Cl and identified one strain with exceptional tolerance. By screening a library of genomic DNA fragments from the [C2C1im]Cl-tolerant strain for improved IIL tolerance, we identified SGE1, which encodes a plasma membrane multidrug efflux pump, and a previously uncharacterized gene that we named ionic liquid tolerance 1 (ILT1), which encodes a predicted membrane protein. Analyses of SGE1 sequences from our panel of S. cerevisiae strains together with growth phenotypes implicated two single nucleotide polymorphisms (SNPs) that associated with IIL tolerance and sensitivity. We confirmed these phenotypic effects by transferring the SGE1 SNPs into a [C2C1im]Cl-sensitive yeast strain using CRISPR/Cas9 genome editing. Further studies indicated that these SNPs affect Sge1 protein stability and cell surface localization, influencing the amount of toxic IILs that cells can pump out of the cytoplasm. Our results highlight the general potential for discovering useful biotechnological functions from untapped natural sequence variation and provide functional insight into emergent SGE1 alleles with reduced capacities to protect against IIL toxicity.},
doi = {10.1534/genetics.118.301161},
journal = {Genetics},
number = [1],
volume = [210],
place = {United States},
year = {2018},
month = {7}
}

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    • Kuang, Meihua Christina; Kominek, Jacek; Alexander, William G.
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    • Li, Haibo; Schmitz, Olivia; Alper, Hal S.
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    • Ruegg, Thomas L.; Kim, Eun-Mi; Simmons, Blake A.
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    • DOI: 10.1038/ncomms4490

    Ionic liquid tolerant hyperthermophilic cellulases for biomass pretreatment and hydrolysis
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    • Green Chemistry, Vol. 12, Issue 2, p. 338-345
    • DOI: 10.1039/b916564a

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    Yeast protein kinase Ptk2 localizes at the plasma membrane and phosphorylates in vitro the C-terminal peptide of the H+-ATPase
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    • Dias, Ana Rita; Costa-Rodrigues, João; Fernandes, Maria Helena
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    • DOI: 10.1002/cmdc.201600480

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    journal, April 2016

    • Alexander, William G.; Peris, David; Pfannenstiel, Brandon T.
    • Fungal Genetics and Biology, Vol. 89
    • DOI: 10.1016/j.fgb.2015.11.002

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    journal, March 2014

    • Farwick, A.; Bruder, S.; Schadeweg, V.
    • Proceedings of the National Academy of Sciences, Vol. 111, Issue 14
    • DOI: 10.1073/pnas.1323464111

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    • Jezegou, A.; Llinares, E.; Anne, C.
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    Phenotypic evaluation and characterization of 21 industrial Saccharomyces cerevisiae yeast strains
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    • Kong, In Iok; Turner, Timothy Lee; Kim, Heejin
    • FEMS Yeast Research, Vol. 18, Issue 1
    • DOI: 10.1093/femsyr/foy001

    High quality de novo sequencing and assembly of the Saccharomyces arboricolus genome
    journal, January 2013


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    • Liti, Gianni; Carter, David M.; Moses, Alan M.
    • Nature, Vol. 458, Issue 7236
    • DOI: 10.1038/nature07743

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    • Almeida, Pedro; Gonçalves, Carla; Teixeira, Sara
    • Nature Communications, Vol. 5, Issue 1
    • DOI: 10.1038/ncomms5044

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    • DOI: 10.1038/nmeth1010

    A High-Definition View of Functional Genetic Variation from Natural Yeast Genomes
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    • Bergström, Anders; Simpson, Jared T.; Salinas, Francisco
    • Molecular Biology and Evolution, Vol. 31, Issue 4
    • DOI: 10.1093/molbev/msu037

    Understanding cost drivers and economic potential of two variants of ionic liquid pretreatment for cellulosic biofuel production
    journal, January 2014

    • Konda, Nvsn; Shi, Jian; Singh, Seema
    • Biotechnology for Biofuels, Vol. 7, Issue 1
    • DOI: 10.1186/1754-6834-7-86

    Comparison of dilute acid and ionic liquid pretreatment of switchgrass: Biomass recalcitrance, delignification and enzymatic saccharification
    journal, July 2010


    Drug:H+ antiporters in chemical stress response in yeast
    journal, January 2009

    • Sá-Correia, Isabel; dos Santos, Sandra C.; Teixeira, Miguel C.
    • Trends in Microbiology, Vol. 17, Issue 1
    • DOI: 10.1016/j.tim.2008.09.007

    Contrasting evolutionary genome dynamics between domesticated and wild yeasts
    journal, April 2017

    • Yue, Jia-Xing; Li, Jing; Aigrain, Louise
    • Nature Genetics, Vol. 49, Issue 6
    • DOI: 10.1038/ng.3847

    Nutrient regulation of oligopeptide transport in Saccharomyces cerevisiae
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    A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast
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    Functional profiling of the Saccharomyces cerevisiae genome
    journal, July 2002


    Fermentable sugars by chemical hydrolysis of biomass
    journal, March 2010

    • Binder, J. B.; Raines, R. T.
    • Proceedings of the National Academy of Sciences, Vol. 107, Issue 10, p. 4516-4521
    • DOI: 10.1073/pnas.0912073107

    Room-Temperature Ionic Liquids. Solvents for Synthesis and Catalysis
    journal, August 1999

    • Welton, Thomas
    • Chemical Reviews, Vol. 99, Issue 8, p. 2071-2084
    • DOI: 10.1021/cr980032t

    Global analysis of phosphorylation and ubiquitylation cross-talk in protein degradation
    journal, June 2013

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