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 ([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 surfacemore »
- Authors:
-
[2];
[2];
[2];
[1];
[1];
[2]
- Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
- Univ. of Wisconsin, Madison, WI (United States)
- Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (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); 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. https://doi.org/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. https://doi.org/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 = {Wed Jul 25 00:00:00 EDT 2018},
month = {Wed Jul 25 00:00:00 EDT 2018}
}
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Works referencing / citing this record:
Improving ionic liquid tolerance in Saccharomyces cerevisiae through heterologous expression and directed evolution of an ILT1 homolog from Yarrowia lipolytica
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