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

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.

doi:10.1534/genetics.118.301161

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

Journal Article · 25 July 2018 · Genetics

DOI: https://doi.org/10.1534/genetics.118.301161 · OSTI ID:1477368

Higgins, Douglas A. ^[1]; Young, Megan K. M. ^[2]; Tremaine, Mary ^[2]; Sardi, Maria ^[2]; Fletcher, Jenna M. ^[2]; Agnew, Margaret ^[2]; Liu, Lisa ^[2]; Dickinson, Quinn ^[2];

^[2];

^[2]; Gasch, Audrey P. ^[2]; Singer, Steven W. ^[3];

^[1]; Landick, Robert ^[2];

^[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)

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); UC Laboratory Fees Research Program (LFRP) (UCRI)

Grant/Contract Number:: AC02-05CH11231; SC0018409; FC02-07ER64494

OSTI ID:: 1477368

Journal Information:: Genetics, Journal Name: Genetics Journal Issue: 1 Vol. 210; ISSN 0016-6731

Publisher:: Genetics Society of AmericaCopyright Statement

Country of Publication:: United States

Language:: English

References (134)

Biomass deconstruction to sugars Blanch, Harvey W.; Simmons, Blake A.; Klein-Marcuschamer, Daniel Biotechnology Journal, Vol. 6, Issue 9 https://doi.org/10.1002/biot.201000180	journal	August 2011
The Anticancer Potential of Ionic Liquids Dias, Ana Rita; Costa-Rodrigues, João; Fernandes, Maria Helena ChemMedChem, Vol. 12, Issue 1 https://doi.org/10.1002/cmdc.201600480	journal	December 2016
A rapid method for localized mutagenesis of yeast genes Muhlrad, Denise; Hunter, Rosalyn; Parker, Roy Yeast, Vol. 8, Issue 2 https://doi.org/10.1002/yea.320080202	journal	February 1992
Enabling glucose/xylose co-transport in yeast through the directed evolution of a sugar transporter Li, Haibo; Schmitz, Olivia; Alper, Hal S. Applied Microbiology and Biotechnology, Vol. 100, Issue 23 https://doi.org/10.1007/s00253-016-7879-8	journal	October 2016
Ionic liquid pretreatment as emerging approaches for enhanced enzymatic hydrolysis of lignocellulosic biomass Elgharbawy, Amal A.; Alam, Md Zahangir; Moniruzzaman, Muhammad Biochemical Engineering Journal, Vol. 109 https://doi.org/10.1016/j.bej.2016.01.021	journal	May 2016
Comparison of dilute acid and ionic liquid pretreatment of switchgrass: Biomass recalcitrance, delignification and enzymatic saccharification Li, Chenlin; Knierim, Bernhard; Manisseri, Chithra Bioresource Technology, Vol. 101, Issue 13 https://doi.org/10.1016/j.biortech.2009.10.066	journal	July 2010
The Genomic Landscape and Evolutionary Resolution of Antagonistic Pleiotropy in Yeast Qian, Wenfeng; Ma, Di; Xiao, Che Cell Reports, Vol. 2, Issue 5 https://doi.org/10.1016/j.celrep.2012.09.017	journal	November 2012
Distinct Domestication Trajectories in Top-Fermenting Beer Yeasts and Wine Yeasts Gonçalves, Margarida; Pontes, Ana; Almeida, Pedro Current Biology, Vol. 26, Issue 20 https://doi.org/10.1016/j.cub.2016.08.040	journal	October 2016
Efficient engineering of marker-free synthetic allotetraploids of Saccharomyces Alexander, William G.; Peris, David; Pfannenstiel, Brandon T. Fungal Genetics and Biology, Vol. 89 https://doi.org/10.1016/j.fgb.2015.11.002	journal	April 2016
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/s0022-2836(05)80360-2	journal	October 1990
Biological Activity of Ionic Liquids and Their Application in Pharmaceutics and Medicine Egorova, Ksenia S.; Gordeev, Evgeniy G.; Ananikov, Valentine P. Chemical Reviews, Vol. 117, Issue 10 https://doi.org/10.1021/acs.chemrev.6b00562	journal	January 2017
Room-Temperature Ionic Liquids. Solvents for Synthesis and Catalysis Welton, Thomas Chemical Reviews, Vol. 99, Issue 8, p. 2071-2084 https://doi.org/10.1021/cr980032t	journal	August 1999
Population genomics of domestic and wild yeasts Liti, Gianni; Carter, David M.; Moses, Alan M. Nature, Vol. 458, Issue 7236 https://doi.org/10.1038/nature07743	journal	February 2009
An auto-inducible mechanism for ionic liquid resistance in microbial biofuel production Ruegg, Thomas L.; Kim, Eun-Mi; Simmons, Blake A. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4490	journal	March 2014
A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum Almeida, Pedro; Gonçalves, Carla; Teixeira, Sara Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5044	journal	June 2014
Global analysis of phosphorylation and ubiquitylation cross-talk in protein degradation Swaney, Danielle L.; Beltrao, Pedro; Starita, Lea Nature Methods, Vol. 10, Issue 7 https://doi.org/10.1038/nmeth.2519	journal	June 2013
Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC Li, Mamie Z.; Elledge, Stephen J. Nature Methods, Vol. 4, Issue 3 https://doi.org/10.1038/nmeth1010	journal	February 2007
Targeted introduction of heritable point mutations into the plant mitochondrial genome Forner, Joachim; Kleinschmidt, Dennis; Meyer, Etienne H. Nature Plants, Vol. 8, Issue 3 https://doi.org/10.1038/s41477-022-01108-y	journal	March 2022
Ionic liquid tolerant hyperthermophilic cellulases for biomass pretreatment and hydrolysis Datta, Supratim; Holmes, Bradley; Park, Joshua I. Green Chemistry, Vol. 12, Issue 2, p. 338-345 https://doi.org/10.1039/b916564a	journal	January 2010
Impact of ionic liquid pretreated plant biomass on Saccharomyces cerevisiae growth and biofuel production Ouellet, Mario; Datta, Supratim; Dibble, Dean C. Green Chemistry, Vol. 13, Issue 10 https://doi.org/10.1039/c1gc15327g	journal	January 2011
Fermentable sugars by chemical hydrolysis of biomass Binder, J. B.; Raines, R. T. Proceedings of the National Academy of Sciences, Vol. 107, Issue 10, p. 4516-4521 https://doi.org/10.1073/pnas.0912073107	journal	March 2010
Global transcriptome response to ionic liquid by a tropical rain forest soil bacterium, Enterobacter lignolyticus Khudyakov, J. I.; D'haeseleer, P.; Borglin, S. E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 32, p. E2173-E2182 https://doi.org/10.1073/pnas.1112750109	journal	May 2012
Heptahelical protein PQLC2 is a lysosomal cationic amino acid exporter underlying the action of cysteamine in cystinosis therapy Jezegou, A.; Llinares, E.; Anne, C. Proceedings of the National Academy of Sciences, Vol. 109, Issue 50 https://doi.org/10.1073/pnas.1211198109	journal	November 2012
Engineering of yeast hexose transporters to transport D-xylose without inhibition by D-glucose Farwick, A.; Bruder, S.; Schadeweg, V. Proceedings of the National Academy of Sciences, Vol. 111, Issue 14 https://doi.org/10.1073/pnas.1323464111	journal	March 2014
The Targeting of Cystinosin to the Lysosomal Membrane Requires a Tyrosine-based Signal and a Novel Sorting Motif Cherqui, Stéphanie; Kalatzis, Vasiliki; Trugnan, Germain Journal of Biological Chemistry, Vol. 276, Issue 16 https://doi.org/10.1074/jbc.m010562200	journal	January 2001
TopPred II: an improved software for membrane protein structure predictions Claros, Manuel G.; Heijne, Gunnar von Bioinformatics, Vol. 10, Issue 6 https://doi.org/10.1093/bioinformatics/10.6.685	journal	January 1994
Phenotypic evaluation and characterization of 21 industrial Saccharomyces cerevisiae yeast strains Kong, In Iok; Turner, Timothy Lee; Kim, Heejin FEMS Yeast Research, Vol. 18, Issue 1 https://doi.org/10.1093/femsyr/foy001	journal	January 2018
Comparative Genomics of Saccharomyces cerevisiae Natural Isolates for Bioenergy Production Wohlbach, Dana J.; Rovinskiy, Nikolay; Lewis, Jeffrey A. Genome Biology and Evolution, Vol. 6, Issue 9 https://doi.org/10.1093/gbe/evu199	journal	September 2014
Isolation and characterization of SGE1: a yeast gene that partially suppresses the gal11 mutation in multiple copies. Amakasu, H.; Suzuki, Y.; Nishizawa, M. Genetics, Vol. 134, Issue 3 https://doi.org/10.1093/genetics/134.3.675	journal	July 1993
A High-Definition View of Functional Genetic Variation from Natural Yeast Genomes Bergström, Anders; Simpson, Jared T.; Salinas, Francisco Molecular Biology and Evolution, Vol. 31, Issue 4 https://doi.org/10.1093/molbev/msu037	journal	January 2014
Repeated Cis-Regulatory Tuning of a Metabolic Bottleneck Gene during Evolution Kuang, Meihua Christina; Kominek, Jacek; Alexander, William G. Molecular Biology and Evolution, Vol. 35, Issue 8 https://doi.org/10.1093/molbev/msy102	journal	May 2018
A new efficient gene disruption cassette for repeated use in budding yeast Guldener, U. Nucleic Acids Research, Vol. 24, Issue 13 https://doi.org/10.1093/nar/24.13.2519	journal	July 1996
A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast Gueldener, U. Nucleic Acids Research, Vol. 30, Issue 6 https://doi.org/10.1093/nar/30.6.e23	journal	March 2002
Nutrient regulation of oligopeptide transport in Saccharomyces cerevisiae Wiles, A. M. Microbiology, Vol. 152, Issue 10 https://doi.org/10.1099/mic.0.29055-0	journal	October 2006
Ubiquitin-Dependent Sorting in Endocytosis Piper, R. C.; Dikic, I.; Lukacs, G. L. Cold Spring Harbor Perspectives in Biology, Vol. 6, Issue 1 https://doi.org/10.1101/cshperspect.a016808	journal	January 2014
The 100-genomes strains, an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen Strope, Pooja K.; Skelly, Daniel A.; Kozmin, Stanislav G. Genome Research, Vol. 25, Issue 5 https://doi.org/10.1101/gr.185538.114	journal	April 2015
Saccharomyces eubayanus and Saccharomyces arboricola reside in North Island native New Zealand forests Gayevskiy, Velimir; Goddard, Matthew R. Environmental Microbiology, Vol. 18, Issue 4 https://doi.org/10.1111/1462-2920.13107	journal	December 2015
Harnessing Genetic Diversity in Saccharomyces cerevisiae for Fermentation of Xylose in Hydrolysates of Alkaline Hydrogen Peroxide-Pretreated Biomass Sato, Trey K.; Liu, Tongjun; Parreiras, Lucas S. Applied and Environmental Microbiology, Vol. 80, Issue 2 https://doi.org/10.1128/aem.01885-13	journal	November 2013
High quality de novo sequencing and assembly of the Saccharomyces arboricolus genome Liti, Gianni; Ba, Alex N. Nguyen; Blythe, Martin BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-69	journal	January 2013
Understanding cost drivers and economic potential of two variants of ionic liquid pretreatment for cellulosic biofuel production Konda, Nvsn; Shi, Jian; Singh, Seema Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/1754-6834-7-86	journal	January 2014
Mechanism of imidazolium ionic liquids toxicity in Saccharomyces cerevisiae and rational engineering of a tolerant, xylose-fermenting strain Dickinson, Quinn; Bottoms, Scott; Hinchman, Li Microbial Cell Factories, Vol. 15, Issue 1 https://doi.org/10.1186/s12934-016-0417-7	journal	January 2016
Impact of two ionic liquids, 1-ethyl-3-methylimidazolium acetate and 1-ethyl-3-methylimidazolium methylphosphonate, on Saccharomyces cerevisiae: metabolic, physiologic, and morphological investigations Mehmood, Nasir; Husson, Eric; Jacquard, Cédric Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0206-2	journal	January 2015
Evidence for Domesticated and Wild Populations of Saccharomyces cerevisiae Fay, Justin C.; Benavides, Joseph A. PLoS Genetics, Vol. 1, Issue 1 https://doi.org/10.1371/journal.pgen.0010005	journal	January 2005
Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus Peris, David; Langdon, Quinn K.; Moriarty, Ryan V. PLOS Genetics, Vol. 12, Issue 7 https://doi.org/10.1371/journal.pgen.1006155	journal	July 2016
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 PLoS ONE, Vol. 9, Issue 9 https://doi.org/10.1371/journal.pone.0107499	journal	September 2014
The Awesome Power of Yeast Evolutionary Genetics: New Genome Sequences and Strain Resources for the Saccharomyces sensu stricto Genus Scannell, Devin R.; Zill, Oliver A.; Rokas, Antonis G3: Genes\|Genomes\|Genetics, Vol. 1, Issue 1 https://doi.org/10.1534/g3.111.000273	journal	June 2011
The Reference Genome Sequence of Saccharomyces cerevisiae : Then and Now Engel, Stacia R.; Dietrich, Fred S.; Fisk, Dianna G. G3: Genes\|Genomes\|Genetics, Vol. 4, Issue 3 https://doi.org/10.1534/g3.113.008995	journal	December 2013
Aromatic inhibitors derived from ammonia-pretreated lignocellulose hinder bacterial ethanologenesis by activating regulatory circuits controlling inhibitor efflux and detoxification Keating, David H.; Zhang, Yaoping; Ong, Irene M. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00402	journal	August 2014
HybPiper: Extracting Coding Sequence and Introns for Phylogenetics from High-Throughput Sequencing Reads Using Target Enrichment Johnson, Matthew G.; Gardner, Elliot M.; Liu, Yang Applications in Plant Sciences, Vol. 4, Issue 7 https://doi.org/10.3732/apps.1600016	journal	July 2016
TheSaccharomyces cerevisiae MFS SuperfamilySGE1 Gene Confers Resistance to Cationic Dyes Jacquot, Claudine; Julien, Raymond; Guilloton, Michel Yeast, Vol. 13, Issue 10 https://doi.org/10.1002/(SICI)1097-0061(199708)13:10<891::AID-YEA138>3.0.CO;2-U	journal	August 1997
The Sge1 protein ofSaccharomyces cerevisiae is a membrane-associated multidrug transporter Ehrenhofer-Murray, Ann E.; Keller Seitz, Monika U.; Sengstag, Christian Yeast, Vol. 14, Issue 1 https://doi.org/10.1002/(SICI)1097-0061(19980115)14:1<49::AID-YEA199>3.0.CO;2-T	journal	January 1998
Heterologous modules for efficient and versatile PCR-based gene targeting inSchizosaccharomyces pombe Bähler, Jürg; Wu, Jian-Qiu; Longtine, Mark S. Yeast, Vol. 14, Issue 10 https://doi.org/10.1002/(SICI)1097-0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y	journal	July 1998
Biomass deconstruction to sugars Blanch, Harvey W.; Simmons, Blake A.; Klein-Marcuschamer, Daniel Biotechnology Journal, Vol. 6, Issue 9 https://doi.org/10.1002/biot.201000180	journal	August 2011
The Anticancer Potential of Ionic Liquids Dias, Ana Rita; Costa-Rodrigues, João; Fernandes, Maria Helena ChemMedChem, Vol. 12, Issue 1 https://doi.org/10.1002/cmdc.201600480	journal	December 2016
An improved method for whole protein extraction from yeast Saccharomyces cerevisiae: Yeast protein extraction by LiAc/NaOH Zhang, Tingting; Lei, Jie; Yang, Hanjiang Yeast, Vol. 28, Issue 11 https://doi.org/10.1002/yea.1905	journal	October 2011
A rapid method for localized mutagenesis of yeast genes Muhlrad, Denise; Hunter, Rosalyn; Parker, Roy Yeast, Vol. 8, Issue 2 https://doi.org/10.1002/yea.320080202	journal	February 1992
Basic Local Alignment Search Tool Altschul, S. Journal of Molecular Biology, Vol. 215, Issue 3 https://doi.org/10.1006/jmbi.1990.9999	journal	October 1990
Crystal structure of the histone acetyltransferase Hpa2: a tetrameric member of the Gcn5-related N-acetyltransferase superfamily Angus-Hill, Melinda L.; Dutnall, Robert N.; Tafrov, Stefan T. Journal of Molecular Biology, Vol. 294, Issue 5 https://doi.org/10.1006/jmbi.1999.3338	journal	December 1999
The Saccharomyces cerevisiae SGE1 gene product: a novel drug-resistance protein within the major facilitator superfamily Ehrenhofer-Murray, AnnE.; W�rgler, FriedrichE.; Sengstag, Christian MGG Molecular & General Genetics, Vol. 244, Issue 3 https://doi.org/10.1007/BF00285456	journal	January 1994
PCR-mediated recombination and mutagenesis: SOEing together tailor-made genes Horton, Robert M. Molecular Biotechnology, Vol. 3, Issue 2 https://doi.org/10.1007/BF02789105	journal	April 1995
Enabling glucose/xylose co-transport in yeast through the directed evolution of a sugar transporter Li, Haibo; Schmitz, Olivia; Alper, Hal S. Applied Microbiology and Biotechnology, Vol. 100, Issue 23 https://doi.org/10.1007/s00253-016-7879-8	journal	October 2016
A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformaion of Escherichia coli Hoffman, Charles S.; Winston, Fred Gene, Vol. 57, Issue 2-3 https://doi.org/10.1016/0378-1119(87)90131-4	journal	January 1987
Multifunctional yeast high-copy-number shuttle vectors Christianson, Thomas W.; Sikorski, Robert S.; Dante, Michael Gene, Vol. 110, Issue 1 https://doi.org/10.1016/0378-1119(92)90454-W	journal	January 1992
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Getting started with yeast Sherman, Fred Guide to Yeast Genetics and Molecular and Cell Biology - Part B https://doi.org/10.1016/S0076-6879(02)50954-X	book	January 2002
Yeast protein kinase Ptk2 localizes at the plasma membrane and phosphorylates in vitro the C-terminal peptide of the H+-ATPase Eraso, Pilar; Mazón, María J.; Portillo, Francisco Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1758, Issue 2 https://doi.org/10.1016/j.bbamem.2006.01.010	journal	February 2006
Ionic liquid pretreatment as emerging approaches for enhanced enzymatic hydrolysis of lignocellulosic biomass Elgharbawy, Amal A.; Alam, Md Zahangir; Moniruzzaman, Muhammad Biochemical Engineering Journal, Vol. 109 https://doi.org/10.1016/j.bej.2016.01.021	journal	May 2016
Comparison of dilute acid and ionic liquid pretreatment of switchgrass: Biomass recalcitrance, delignification and enzymatic saccharification Li, Chenlin; Knierim, Bernhard; Manisseri, Chithra Bioresource Technology, Vol. 101, Issue 13 https://doi.org/10.1016/j.biortech.2009.10.066	journal	July 2010
The Genomic Landscape and Evolutionary Resolution of Antagonistic Pleiotropy in Yeast Qian, Wenfeng; Ma, Di; Xiao, Che Cell Reports, Vol. 2, Issue 5 https://doi.org/10.1016/j.celrep.2012.09.017	journal	November 2012
Evidence for a Far East Asian origin of lager beer yeast Bing, Jian; Han, Pei-Jie; Liu, Wan-Qiu Current Biology, Vol. 24, Issue 10 https://doi.org/10.1016/j.cub.2014.04.031	journal	May 2014
Distinct Domestication Trajectories in Top-Fermenting Beer Yeasts and Wine Yeasts Gonçalves, Margarida; Pontes, Ana; Almeida, Pedro Current Biology, Vol. 26, Issue 20 https://doi.org/10.1016/j.cub.2016.08.040	journal	October 2016
Efficient engineering of marker-free synthetic allotetraploids of Saccharomyces Alexander, William G.; Peris, David; Pfannenstiel, Brandon T. Fungal Genetics and Biology, Vol. 89 https://doi.org/10.1016/j.fgb.2015.11.002	journal	April 2016
Drug:H+ antiporters in chemical stress response in yeast Sá-Correia, Isabel; dos Santos, Sandra C.; Teixeira, Miguel C. Trends in Microbiology, Vol. 17, Issue 1 https://doi.org/10.1016/j.tim.2008.09.007	journal	January 2009
Biological Activity of Ionic Liquids and Their Application in Pharmaceutics and Medicine Egorova, Ksenia S.; Gordeev, Evgeniy G.; Ananikov, Valentine P. Chemical Reviews, Vol. 117, Issue 10 https://doi.org/10.1021/acs.chemrev.6b00562	journal	January 2017
Room-Temperature Ionic Liquids. Solvents for Synthesis and Catalysis Welton, Thomas Chemical Reviews, Vol. 99, Issue 8, p. 2071-2084 https://doi.org/10.1021/cr980032t	journal	August 1999
Functional profiling of the Saccharomyces cerevisiae genome Giaever, Guri; Chu, Angela M.; Ni, Li Nature, Vol. 418, Issue 6896 https://doi.org/10.1038/nature00935	journal	July 2002
Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae Schacherer, Joseph; Shapiro, Joshua A.; Ruderfer, Douglas M. Nature, Vol. 458, Issue 7236 https://doi.org/10.1038/nature07670	journal	February 2009
Population genomics of domestic and wild yeasts Liti, Gianni; Carter, David M.; Moses, Alan M. Nature, Vol. 458, Issue 7236 https://doi.org/10.1038/nature07743	journal	February 2009
An auto-inducible mechanism for ionic liquid resistance in microbial biofuel production Ruegg, Thomas L.; Kim, Eun-Mi; Simmons, Blake A. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4490	journal	March 2014
A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum Almeida, Pedro; Gonçalves, Carla; Teixeira, Sara Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5044	journal	June 2014
Contrasting evolutionary genome dynamics between domesticated and wild yeasts Yue, Jia-Xing; Li, Jing; Aigrain, Louise Nature Genetics, Vol. 49, Issue 6 https://doi.org/10.1038/ng.3847	journal	April 2017
Global analysis of phosphorylation and ubiquitylation cross-talk in protein degradation Swaney, Danielle L.; Beltrao, Pedro; Starita, Lea Nature Methods, Vol. 10, Issue 7 https://doi.org/10.1038/nmeth.2519	journal	June 2013
Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC Li, Mamie Z.; Elledge, Stephen J. Nature Methods, Vol. 4, Issue 3 https://doi.org/10.1038/nmeth1010	journal	February 2007
High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method Gietz, R. Daniel; Schiestl, Robert H. Nature Protocols, Vol. 2, Issue 1 https://doi.org/10.1038/nprot.2007.13	journal	January 2007
Ancient genomes reveal social and genetic structure of Late Neolithic Switzerland Furtwängler, Anja; Rohrlach, A. B.; Lamnidis, Thiseas C. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15560-x	journal	April 2020
Ionic liquid tolerant hyperthermophilic cellulases for biomass pretreatment and hydrolysis Datta, Supratim; Holmes, Bradley; Park, Joshua I. Green Chemistry, Vol. 12, Issue 2, p. 338-345 https://doi.org/10.1039/b916564a	journal	January 2010
Impact of ionic liquid pretreated plant biomass on Saccharomyces cerevisiae growth and biofuel production Ouellet, Mario; Datta, Supratim; Dibble, Dean C. Green Chemistry, Vol. 13, Issue 10 https://doi.org/10.1039/c1gc15327g	journal	January 2011
Fermentable sugars by chemical hydrolysis of biomass Binder, J. B.; Raines, R. T. Proceedings of the National Academy of Sciences, Vol. 107, Issue 10, p. 4516-4521 https://doi.org/10.1073/pnas.0912073107	journal	March 2010
Global transcriptome response to ionic liquid by a tropical rain forest soil bacterium, Enterobacter lignolyticus Khudyakov, J. I.; D'haeseleer, P.; Borglin, S. E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 32, p. E2173-E2182 https://doi.org/10.1073/pnas.1112750109	journal	May 2012
Heptahelical protein PQLC2 is a lysosomal cationic amino acid exporter underlying the action of cysteamine in cystinosis therapy Jezegou, A.; Llinares, E.; Anne, C. Proceedings of the National Academy of Sciences, Vol. 109, Issue 50 https://doi.org/10.1073/pnas.1211198109	journal	November 2012
Engineering of yeast hexose transporters to transport D-xylose without inhibition by D-glucose Farwick, A.; Bruder, S.; Schadeweg, V. Proceedings of the National Academy of Sciences, Vol. 111, Issue 14 https://doi.org/10.1073/pnas.1323464111	journal	March 2014
The Targeting of Cystinosin to the Lysosomal Membrane Requires a Tyrosine-based Signal and a Novel Sorting Motif Cherqui, Stéphanie; Kalatzis, Vasiliki; Trugnan, Germain Journal of Biological Chemistry, Vol. 276, Issue 16 https://doi.org/10.1074/jbc.M010562200	journal	January 2001
TopPred II: an improved software for membrane protein structure predictions Claros, Manuel G.; Heijne, Gunnar von Bioinformatics, Vol. 10, Issue 6 https://doi.org/10.1093/bioinformatics/10.6.685	journal	January 1994
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data Kearse, M.; Moir, R.; Wilson, A. Bioinformatics, Vol. 28, Issue 12 https://doi.org/10.1093/bioinformatics/bts199	journal	April 2012
The 3' to 5' degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3' to 5' exonucleases of the exosome complex Anderson, J. S. J. The EMBO Journal, Vol. 17, Issue 5 https://doi.org/10.1093/emboj/17.5.1497	journal	March 1998
Phenotypic evaluation and characterization of 21 industrial Saccharomyces cerevisiae yeast strains Kong, In Iok; Turner, Timothy Lee; Kim, Heejin FEMS Yeast Research, Vol. 18, Issue 1 https://doi.org/10.1093/femsyr/foy001	journal	January 2018
Comparative Genomics of Saccharomyces cerevisiae Natural Isolates for Bioenergy Production Wohlbach, Dana J.; Rovinskiy, Nikolay; Lewis, Jeffrey A. Genome Biology and Evolution, Vol. 6, Issue 9 https://doi.org/10.1093/gbe/evu199	journal	September 2014
Isolation and characterization of SGE1: a yeast gene that partially suppresses the gal11 mutation in multiple copies. Amakasu, H.; Suzuki, Y.; Nishizawa, M. Genetics, Vol. 134, Issue 3 https://doi.org/10.1093/genetics/134.3.675	journal	July 1993
RTM1: a member of a new family of telomeric repeated genes in yeast. Ness, F.; Aigle, M. Genetics, Vol. 140, Issue 3 https://doi.org/10.1093/genetics/140.3.945	journal	July 1995
A High-Definition View of Functional Genetic Variation from Natural Yeast Genomes Bergström, Anders; Simpson, Jared T.; Salinas, Francisco Molecular Biology and Evolution, Vol. 31, Issue 4 https://doi.org/10.1093/molbev/msu037	journal	January 2014
Repeated Cis-Regulatory Tuning of a Metabolic Bottleneck Gene during Evolution Kuang, Meihua Christina; Kominek, Jacek; Alexander, William G. Molecular Biology and Evolution, Vol. 35, Issue 8 https://doi.org/10.1093/molbev/msy102	journal	May 2018
A new efficient gene disruption cassette for repeated use in budding yeast Guldener, U. Nucleic Acids Research, Vol. 24, Issue 13 https://doi.org/10.1093/nar/24.13.2519	journal	July 1996
A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast Gueldener, U. Nucleic Acids Research, Vol. 30, Issue 6 https://doi.org/10.1093/nar/30.6.e23	journal	March 2002
Nutrient regulation of oligopeptide transport in Saccharomyces cerevisiae Wiles, A. M. Microbiology, Vol. 152, Issue 10 https://doi.org/10.1099/mic.0.29055-0	journal	October 2006
Ubiquitin-Dependent Sorting in Endocytosis Piper, R. C.; Dikic, I.; Lukacs, G. L. Cold Spring Harbor Perspectives in Biology, Vol. 6, Issue 1 https://doi.org/10.1101/cshperspect.a016808	journal	January 2014
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data McKenna, A.; Hanna, M.; Banks, E. Genome Research, Vol. 20, Issue 9 https://doi.org/10.1101/gr.107524.110	journal	July 2010
Integrative phenomics reveals insight into the structure of phenotypic diversity in budding yeast Skelly, D. A.; Merrihew, G. E.; Riffle, M. Genome Research, Vol. 23, Issue 9 https://doi.org/10.1101/gr.155762.113	journal	May 2013
The 100-genomes strains, an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen Strope, Pooja K.; Skelly, Daniel A.; Kozmin, Stanislav G. Genome Research, Vol. 25, Issue 5 https://doi.org/10.1101/gr.185538.114	journal	April 2015
Novel Protein Domains and Repeats in Drosophila melanogaster: Insights into Structure, Function, and Evolution Ponting, C. P. Genome Research, Vol. 11, Issue 12 https://doi.org/10.1101/gr.198701	journal	November 2001
Saccharomyces eubayanus and Saccharomyces arboricola reside in North Island native New Zealand forests Gayevskiy, Velimir; Goddard, Matthew R. Environmental Microbiology, Vol. 18, Issue 4 https://doi.org/10.1111/1462-2920.13107	journal	December 2015
Identification of RCN1 and RSA3 as ethanol-tolerant genes in Saccharomyces cerevisiae using a high copy barcoded library Anderson, Michael J.; Barker, Sarah L.; Boone, Charlie FEMS Yeast Research, Vol. 12, Issue 1 https://doi.org/10.1111/j.1567-1364.2011.00762.x	journal	December 2011
Functional Characterization of the S. cerevisiae Genome by Gene Deletion and Parallel Analysis Winzeler, E. A. Science, Vol. 285, Issue 5429 https://doi.org/10.1126/science.285.5429.901	journal	August 1999
Harnessing Genetic Diversity in Saccharomyces cerevisiae for Fermentation of Xylose in Hydrolysates of Alkaline Hydrogen Peroxide-Pretreated Biomass Sato, Trey K.; Liu, Tongjun; Parreiras, Lucas S. Applied and Environmental Microbiology, Vol. 80, Issue 2 https://doi.org/10.1128/AEM.01885-13	journal	November 2013
The S-Phase Cyclin Clb5 Promotes rRNA Gene (rDNA) Stability by Maintaining Replication Initiation Efficiency in rDNA Goto, Mayuko; Sasaki, Mariko; Kobayashi, Takehiko Molecular and Cellular Biology, Vol. 41, Issue 5 https://doi.org/10.1128/mcb.00324-20	journal	April 2021
Novel role for the Saccharomyces cerevisiae oligopeptide transporter Opt2 in drug detoxificationIn memory of Ghassan Belhadj. Aouida, Mustapha; Khodami-Pour, Ali; Ramotar, Dindial Biochemistry and Cell Biology, Vol. 87, Issue 4 https://doi.org/10.1139/O09-045	journal	August 2009
High quality de novo sequencing and assembly of the Saccharomyces arboricolus genome Liti, Gianni; Ba, Alex N. Nguyen; Blythe, Martin BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-69	journal	January 2013
Understanding cost drivers and economic potential of two variants of ionic liquid pretreatment for cellulosic biofuel production Konda, Nvsn; Shi, Jian; Singh, Seema Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/1754-6834-7-86	journal	January 2014
Fine-scale population structure and evidence for local adaptation in Australian giant black tiger shrimp (Penaeus monodon) using SNP analysis Vu, Nga T. T.; Zenger, Kyall R.; Guppy, Jarrod L. BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-020-07084-x	journal	September 2020
Mechanism of imidazolium ionic liquids toxicity in Saccharomyces cerevisiae and rational engineering of a tolerant, xylose-fermenting strain Dickinson, Quinn; Bottoms, Scott; Hinchman, Li Microbial Cell Factories, Vol. 15, Issue 1 https://doi.org/10.1186/s12934-016-0417-7	journal	January 2016
Engineering of Saccharomyces cerevisiae for anthranilate and methyl anthranilate production Kuivanen, Joosu; Kannisto, Matti; Mojzita, Dominik Microbial Cell Factories, Vol. 20, Issue 1 https://doi.org/10.1186/s12934-021-01532-3	journal	February 2021
Impact of two ionic liquids, 1-ethyl-3-methylimidazolium acetate and 1-ethyl-3-methylimidazolium methylphosphonate, on Saccharomyces cerevisiae: metabolic, physiologic, and morphological investigations Mehmood, Nasir; Husson, Eric; Jacquard, Cédric Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0206-2	journal	January 2015
Saccharomyces cerevisiae single-copy plasmids for auxotrophy compensation, multiple marker selection, and for designing metabolically cooperating communities Mülleder, Michael; Campbell, Kate; Matsarskaia, Olga F1000Research, Vol. 5 https://doi.org/10.12688/f1000research.9606.1	journal	January 2016
Evidence for Domesticated and Wild Populations of Saccharomyces cerevisiae Fay, Justin C.; Benavides, Joseph A. PLoS Genetics, Vol. 1, Issue 1 https://doi.org/10.1371/journal.pgen.0010005	journal	January 2005
Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus Peris, David; Langdon, Quinn K.; Moriarty, Ryan V. PLOS Genetics, Vol. 12, Issue 7 https://doi.org/10.1371/journal.pgen.1006155	journal	July 2016
Genome-wide association across Saccharomyces cerevisiae strains reveals substantial variation in underlying gene requirements for toxin tolerance Sardi, Maria; Paithane, Vaishnavi; Place, Michael PLOS Genetics, Vol. 14, Issue 2 https://doi.org/10.1371/journal.pgen.1007217	journal	February 2018
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 PLoS ONE, Vol. 9, Issue 9 https://doi.org/10.1371/journal.pone.0107499	journal	September 2014
The Awesome Power of Yeast Evolutionary Genetics: New Genome Sequences and Strain Resources for the Saccharomyces sensu stricto Genus Scannell, Devin R.; Zill, Oliver A.; Rokas, Antonis G3: Genes\|Genomes\|Genetics, Vol. 1, Issue 1 https://doi.org/10.1534/g3.111.000273	journal	June 2011
The Reference Genome Sequence of Saccharomyces cerevisiae : Then and Now Engel, Stacia R.; Dietrich, Fred S.; Fisk, Dianna G. G3: Genes\|Genomes\|Genetics, Vol. 4, Issue 3 https://doi.org/10.1534/g3.113.008995	journal	December 2013
Impact of two ionic liquids, 1-ethyl-3-methylimidazolium acetate and 1-ethyl-3-methylimidazolium methylphosphonate, on Saccharomyces cerevisiae : metabolic, physiologic, and morphological investigations Mehmood, Nasir; Husson, Eric; Jacquard, Cédric RWTH Aachen University https://doi.org/10.18154/rwth-2015-00863	text	January 2015
Aromatic inhibitors derived from ammonia-pretreated lignocellulose hinder bacterial ethanologenesis by activating regulatory circuits controlling inhibitor efflux and detoxification Keating, David H.; Zhang, Yaoping; Ong, Irene M. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00402	journal	August 2014
MFS transporters required for multidrug/multixenobiotic (MD/MX) resistance in the model yeast: understanding their physiological function through post-genomic approaches dos Santos, Sandra C.; Teixeira, Miguel C.; Dias, Paulo J. Frontiers in Physiology, Vol. 5 https://doi.org/10.3389/fphys.2014.00180	journal	May 2014
HybPiper: Extracting Coding Sequence and Introns for Phylogenetics from High-Throughput Sequencing Reads Using Target Enrichment Johnson, Matthew G.; Gardner, Elliot M.; Liu, Yang Applications in Plant Sciences, Vol. 4, Issue 7 https://doi.org/10.3732/apps.1600016	journal	July 2016
A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w Cingolani, Pablo; Platts, Adrian; Wang, Le Lily Fly, Vol. 6, Issue 2 https://doi.org/10.4161/fly.19695	journal	April 2012
Dosage compensation can buffer copy-number variation in wild yeast Hose, James; Yong, Chris Mun; Sardi, Maria eLife, Vol. 4 https://doi.org/10.7554/eLife.05462	journal	May 2015

Cited By (6)

Engineering Corynebacterium glutamicum to produce the biogasoline isopentenol from plant biomass hydrolysates Sasaki, Yusuke; Eng, Thomas; Herbert, Robin A. Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1381-3	journal	February 2019
Improving ionic liquid tolerance in Saccharomyces cerevisiae through heterologous expression and directed evolution of an ILT1 homolog from Yarrowia lipolytica Reed, Kevin B.; Wagner, James M.; d’Oelsnitz, Simon Journal of Industrial Microbiology & Biotechnology, Vol. 46, Issue 12 https://doi.org/10.1007/s10295-019-02228-9	journal	August 2019
Guanidine Riboswitch-Regulated Efflux Transporters Protect Bacteria against Ionic Liquid Toxicity Higgins, Douglas A.; Gladden, John M.; Kimbrel, Jeff A. Journal of Bacteriology, Vol. 201, Issue 13 https://doi.org/10.1128/jb.00069-19	journal	April 2019
Restoration of biofuel production levels and increased tolerance under ionic liquid stress is enabled by a mutation in the essential Escherichia coli gene cydC Eng, Thomas; Demling, Philipp; Herbert, Robin A. Microbial Cell Factories, Vol. 17, Issue 1 https://doi.org/10.1186/s12934-018-1006-8	journal	October 2018
Engineering Corynebacterium glutamicum to produce the biogasoline isopentenol from plant biomass hydrolysates Sasaki, Yusuke; Eng, Thomas; Herbert, Robin A. Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1381-3	journal	February 2019
Restoration of biofuel production levels and increased tolerance under ionic liquid stress is enabled by a mutation in the essential Escherichia coli gene cydC Eng, Thomas; Demling, Philipp; Herbert, Robin A. RWTH Aachen University https://doi.org/10.18154/rwth-2019-00645	text	January 2018

Linked Research (2)

Similar Records

Guanidine Riboswitch-Regulated Efflux Transporters Protect Bacteria against Ionic Liquid Toxicity

Journal Article · 2019 · Journal of Bacteriology · OSTI ID:1544473

Higgins, Douglas A.; Gladden, John M.; Kimbrel, Jeff A.; +3 more

L-lactic acid production from D-xylose with Candida sonorensis expressing a heterologous lactate dehydrogenase encoding gene

Journal Article · 2014 · Microbial Cell Factories · OSTI ID:1626888

Koivuranta, Kari T.; Ilmén, Marja; Wiebe, Marilyn G.; +3 more

YPK9 and WHI2 Negatively Interact during Oxidative Stress

Journal Article · 2021 · Microorganisms · OSTI ID:1877675

Joseph, Florenal; Miller, Darach; Evgrafov, Oleg V.; +1 more

Related Subjects

09 BIOMASS FUELS
59 BASIC BIOLOGICAL SCIENCES
BIOFUELS
MAJOR FACILITATOR SUPERFAMILY
NATURAL VARIATION
SACCHAROMYCES CEREVISIAE
TOXIN TOLERANCE
YEASTIONIC LIQUID

Supplemental Material for Higgins et al., 2018 Higgins, Douglas A.; Young, Megan K.; Tremaine, Mary https://doi.org/10.25386/GENETICS.6731201 The current record is supplemented by this collection	collection	January 2018
Supplemental Material for Higgins et al., 2018 Higgins, Douglas A.; Young, Megan K.; Tremaine, Mary https://doi.org/10.25386/genetics.6731201.v1 The current record is supplemented by this collection	collection	January 2018