Restoration of biofuel production levels and increased tolerance under ionic liquid stress is enabled by a mutation in the essential Escherichia coli gene cydC
Abstract
Background: Microbial production of chemicals from renewable carbon sources enables a sustainable route to many bioproducts. Sugar streams, such as those derived from biomass pretreated with ionic liquids (IL), provide efficiently derived and cost-competitive starting materials. A limitation to this approach is that residual ILs in the pretreated sugar source can be inhibitory to microbial growth and impair expression of the desired biosynthetic pathway. Results: We utilized laboratory evolution to select Escherichia coli strains capable of robust growth in the presence of the IL, 1-ethyl-3-methyl-imidizolium acetate ([EMIM]OAc). Whole genome sequencing of the evolved strain identified a point mutation in an essential gene, cydC, which confers tolerance to two different classes of ILs at concentrations that are otherwise growth inhibitory. This mutation, cydC-D86G, fully restores the specific production of the bio-jet fuel candidate d-limonene, as well as the biogasoline and platform chemical isopentenol, in growth medium containing ILs. Similar amino acids at this position in cydC, such as cydC-D86V, also confer tolerance to [EMIM]OAc. We show that this [EMIM]OAc tolerance phenotype of cydC-D86G strains is independent of its wild-type function in activating the cytochrome bd-I respiratory complex. Using shotgun proteomics, we characterized the underlying differential cellular responses altered in this mutant.more »
- 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:
- 1618895
- Alternate Identifier(s):
- OSTI ID: 1506369
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- Microbial Cell Factories
- Additional Journal Information:
- Journal Name: Microbial Cell Factories Journal Volume: 17 Journal Issue: 1; Journal ID: ISSN 1475-2859
- Publisher:
- Springer Science + Business Media
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 09 BIOMASS FUELS; Ionic liquids; [EMIM]OAc; [C2C1im]OAc; Biofuels; Adaptation; Laboratory evolution; Isopentenol; Limonene; Strain engineering; cydC; Escherichia coli
Citation Formats
Eng, Thomas, Demling, Philipp, Herbert, Robin A., Chen, Yan, Benites, Veronica, Martin, Joel, Lipzen, Anna, Baidoo, Edward E. K., Blank, Lars M., Petzold, Christopher J., and Mukhopadhyay, Aindrila. Restoration of biofuel production levels and increased tolerance under ionic liquid stress is enabled by a mutation in the essential Escherichia coli gene cydC. United Kingdom: N. p., 2018.
Web. doi:10.1186/s12934-018-1006-8.
Eng, Thomas, Demling, Philipp, Herbert, Robin A., Chen, Yan, Benites, Veronica, Martin, Joel, Lipzen, Anna, Baidoo, Edward E. K., Blank, Lars M., Petzold, Christopher J., & Mukhopadhyay, Aindrila. Restoration of biofuel production levels and increased tolerance under ionic liquid stress is enabled by a mutation in the essential Escherichia coli gene cydC. United Kingdom. https://doi.org/10.1186/s12934-018-1006-8
Eng, Thomas, Demling, Philipp, Herbert, Robin A., Chen, Yan, Benites, Veronica, Martin, Joel, Lipzen, Anna, Baidoo, Edward E. K., Blank, Lars M., Petzold, Christopher J., and Mukhopadhyay, Aindrila. Mon .
"Restoration of biofuel production levels and increased tolerance under ionic liquid stress is enabled by a mutation in the essential Escherichia coli gene cydC". United Kingdom. https://doi.org/10.1186/s12934-018-1006-8.
@article{osti_1618895,
title = {Restoration of biofuel production levels and increased tolerance under ionic liquid stress is enabled by a mutation in the essential Escherichia coli gene cydC},
author = {Eng, Thomas and Demling, Philipp and Herbert, Robin A. and Chen, Yan and Benites, Veronica and Martin, Joel and Lipzen, Anna and Baidoo, Edward E. K. and Blank, Lars M. and Petzold, Christopher J. and Mukhopadhyay, Aindrila},
abstractNote = {Background: Microbial production of chemicals from renewable carbon sources enables a sustainable route to many bioproducts. Sugar streams, such as those derived from biomass pretreated with ionic liquids (IL), provide efficiently derived and cost-competitive starting materials. A limitation to this approach is that residual ILs in the pretreated sugar source can be inhibitory to microbial growth and impair expression of the desired biosynthetic pathway. Results: We utilized laboratory evolution to select Escherichia coli strains capable of robust growth in the presence of the IL, 1-ethyl-3-methyl-imidizolium acetate ([EMIM]OAc). Whole genome sequencing of the evolved strain identified a point mutation in an essential gene, cydC, which confers tolerance to two different classes of ILs at concentrations that are otherwise growth inhibitory. This mutation, cydC-D86G, fully restores the specific production of the bio-jet fuel candidate d-limonene, as well as the biogasoline and platform chemical isopentenol, in growth medium containing ILs. Similar amino acids at this position in cydC, such as cydC-D86V, also confer tolerance to [EMIM]OAc. We show that this [EMIM]OAc tolerance phenotype of cydC-D86G strains is independent of its wild-type function in activating the cytochrome bd-I respiratory complex. Using shotgun proteomics, we characterized the underlying differential cellular responses altered in this mutant. While wild-type E. coli cannot produce detectable amounts of either product in the presence of ILs at levels expected to be residual in sugars from pretreated biomass, the engineered cydC-D86G strains produce over 200 mg/L d-limonene and 350 mg/L isopentenol, which are among the highest reported titers in the presence of [EMIM]OAc.Conclusions: The optimized strains in this study produce high titers of two candidate biofuels and bioproducts under IL stress. Both sets of production strains surpass production titers from other IL tolerant mutants in the literature. Our application of laboratory evolution identified a gain of function mutation in an essential gene, which is unusual in comparison to other published IL tolerant mutants.[Figure not available: see fulltext.]},
doi = {10.1186/s12934-018-1006-8},
journal = {Microbial Cell Factories},
number = 1,
volume = 17,
place = {United Kingdom},
year = {Mon Oct 08 00:00:00 EDT 2018},
month = {Mon Oct 08 00:00:00 EDT 2018}
}
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https://doi.org/10.1186/s12934-018-1006-8
https://doi.org/10.1186/s12934-018-1006-8
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Cited by: 22 works
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Works referenced in this record:
An auto-inducible mechanism for ionic liquid resistance in microbial biofuel production
journal, March 2014
- Ruegg, Thomas L.; Kim, Eun-Mi; Simmons, Blake A.
- Nature Communications, Vol. 5, Issue 1
MicrobesOnline: an integrated portal for comparative and functional genomics
journal, November 2009
- Dehal, P. S.; Joachimiak, M. P.; Price, M. N.
- Nucleic Acids Research, Vol. 38, Issue suppl_1, p. D396-D400
Standard Flow Liquid Chromatography for Shotgun Proteomics in Bioenergy Research
journal, April 2015
- González Fernández-Niño, Susana M.; Smith-Moritz, A. Michelle; Chan, Leanne Jade G.
- Frontiers in Bioengineering and Biotechnology, Vol. 3
Evolved hexose transporter enhances xylose uptake and glucose/xylose co-utilization in Saccharomyces cerevisiae
journal, January 2016
- Reider Apel, Amanda; Ouellet, Mario; Szmidt-Middleton, Heather
- Scientific Reports, Vol. 6, Issue 1
Lipophilicity parameters for ionic liquid cations and their correlation to in vitro cytotoxicity
journal, July 2007
- Ranke, Johannes; Müller, Anja; Bottin-Weber, Ulrike
- Ecotoxicology and Environmental Safety, Vol. 67, Issue 3
Analysis of physico-chemical properties of substrates of ABC and MFS multidrug transporters of pathogenic Candida albicans
journal, November 2010
- Puri, Nidhi; Prakash, Om; Manoharlal, Raman
- European Journal of Medicinal Chemistry, Vol. 45, Issue 11
Enrichment, isolation and characterization of fungi tolerant to 1-ethyl-3-methylimidazolium acetate: Ionic liquid-tolerant fungi
journal, February 2011
- Singer, S. W.; Reddy, A. P.; Gladden, J. M.
- Journal of Applied Microbiology, Vol. 110, Issue 4
Anti-microbial activities of ionic liquids
journal, December 2002
- Pernak, Juliusz; Sobaszkiewicz, Kinga; Mirska, Ilona
- Green Chemistry, Vol. 5, Issue 1
Panorama: A Targeted Proteomics Knowledge Base
journal, July 2014
- Sharma, Vagisha; Eckels, Josh; Taylor, Greg K.
- Journal of Proteome Research, Vol. 13, Issue 9
Room temperature ionic liquids as emerging solvents for the pretreatment of lignocellulosic biomass
journal, April 2011
- Mora-Pale, Mauricio; Meli, Luciana; Doherty, Thomas V.
- Biotechnology and Bioengineering, Vol. 108, Issue 6
Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009
- Li, H.; Durbin, R.
- Bioinformatics, Vol. 25, Issue 14
Under pressure: evolutionary engineering of yeast strains for improved performance in fuels and chemicals production
journal, April 2018
- Mans, Robert; Daran, Jean-Marc G.; Pronk, Jack T.
- Current Opinion in Biotechnology, Vol. 50
Designing ionic liquids: the chemical structure role in the toxicity
journal, September 2012
- Ventura, Sónia P. M.; Gonçalves, Ana M. M.; Sintra, Tânia
- Ecotoxicology, Vol. 22, Issue 1
Structure and Function of the Bacterial Heterodimeric ABC Transporter CydDC: STIMULATION OF ATPASE ACTIVITY BY THIOL AND HEME COMPOUNDS
journal, June 2014
- Yamashita, Masao; Shepherd, Mark; Booth, Wesley I.
- Journal of Biological Chemistry, Vol. 289, Issue 33
A Comprehensive, CRISPR-based Functional Analysis of Essential Genes in Bacteria
journal, June 2016
- Peters, Jason M.; Colavin, Alexandre; Shi, Handuo
- Cell, Vol. 165, Issue 6
Mechanism of imidazolium ionic liquids toxicity in Saccharomyces cerevisiae and rational engineering of a tolerant, xylose-fermenting strain
journal, January 2016
- Dickinson, Quinn; Bottoms, Scott; Hinchman, Li
- Microbial Cell Factories, Vol. 15, Issue 1
Analysis of a bacterial hygromycin B resistance gene by transcriptional and translational fusions and by DNA sequencing
journal, January 1983
- Kaster, Kevin R.; Burgett, Stanley G.; Rao, R. Nagaraja
- Nucleic Acids Research, Vol. 11, Issue 19
Identification and microbial production of a terpene-based advanced biofuel
journal, September 2011
- Peralta-Yahya, Pamela P.; Ouellet, Mario; Chan, Rossana
- Nature Communications, Vol. 2, Issue 1
The temperature-sensitive growth and survival phenotypes of Escherichia coli cydDC and cydAB strains are due to deficiencies in cytochrome bd and are corrected by exogenous catalase and reducing agents.
journal, November 1996
- Goldman, B. S.; Gabbert, K. K.; Kranz, R. G.
- Journal of Bacteriology, Vol. 178, Issue 21
Accumulation of ionic liquids in Escherichia coli cells
journal, January 2008
- Cornmell, Robert J.; Winder, Catherine L.; Tiddy, Gordon J. T.
- Green Chemistry, Vol. 10, Issue 8
The CydDC ABC transporter of Escherichia coli: new roles for a reductant efflux pump
journal, October 2015
- Shepherd, Mark
- Biochemical Society Transactions, Vol. 43, Issue 5
Metabolic engineering of Escherichia coli for 1-butanol production
journal, November 2008
- Atsumi, Shota; Cann, Anthony F.; Connor, Michael R.
- Metabolic Engineering, Vol. 10, Issue 6, p. 305-311
A targeted proteomics toolkit for high-throughput absolute quantification of Escherichia coli proteins
journal, November 2014
- Batth, Tanveer S.; Singh, Pragya; Ramakrishnan, Vikram R.
- Metabolic Engineering, Vol. 26
Rapid Quantification of Mutant Fitness in Diverse Bacteria by Sequencing Randomly Bar-Coded Transposons
journal, May 2015
- Wetmore, Kelly M.; Price, Morgan N.; Waters, Robert J.
- mBio, Vol. 6, Issue 3, Article No. e00306-15
The cytochrome bd respiratory oxygen reductases
journal, November 2011
- Borisov, Vitaliy B.; Gennis, Robert B.; Hemp, James
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 11
Global transcriptome response to ionic liquid by a tropical rain forest soil bacterium, Enterobacter lignolyticus
journal, May 2012
- Khudyakov, J. I.; D'haeseleer, P.; Borglin, S. E.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 32, p. E2173-E2182
Scale-up and evaluation of high solid ionic liquid pretreatment and enzymatic hydrolysis of switchgrass
journal, January 2013
- Li, Chenlin; Tanjore, Deepti; He, Wei
- Biotechnology for Biofuels, Vol. 6, Issue 1
CNVnator: An approach to discover, genotype, and characterize typical and atypical CNVs from family and population genome sequencing
journal, February 2011
- Abyzov, A.; Urban, A. E.; Snyder, M.
- Genome Research, Vol. 21, Issue 6
Synthesis of three advanced biofuels from ionic liquid-pretreated switchgrass using engineered Escherichia coli
journal, November 2011
- Bokinsky, G.; Peralta-Yahya, P. P.; George, A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 50, p. 19949-19954
A comprehensive strategy enabling high-resolution functional analysis of the yeast genome
journal, July 2008
- Breslow, David K.; Cameron, Dale M.; Collins, Sean R.
- Nature Methods, Vol. 5, Issue 8
Membrane topology and mutational analysis of Escherichia coli CydDC, an ABC-type cysteine exporter required for cytochrome assembly
journal, October 2004
- Cruz-Ramos, H.
- Microbiology, Vol. 150, Issue 10
Pretreatment technologies for an efficient bioethanol production process based on enzymatic hydrolysis: A review
journal, July 2010
- Alvira, P.; Tomás-Pejó, E.; Ballesteros, M.
- Bioresource Technology, Vol. 101, Issue 13, p. 4851-4861
Dimethyl Sulfoxide Assisted Ionic Liquid Pretreatment of Switchgrass for Isoprenol Production
journal, January 2018
- Wang, Shizeng; Zhao, Wenwen; Lee, Taek Soon
- ACS Sustainable Chemistry & Engineering, Vol. 6, Issue 3
Expression of the Bacillus subtilis sacB gene confers sucrose sensitivity on mycobacteria.
journal, February 1996
- Pelicic, V.; Reyrat, J. M.; Gicquel, B.
- Journal of Bacteriology, Vol. 178, Issue 4
Impact of ionic liquid pretreated plant biomass on Saccharomyces cerevisiae growth and biofuel production
journal, January 2011
- Ouellet, Mario; Datta, Supratim; Dibble, Dean C.
- Green Chemistry, Vol. 13, Issue 10
The cydD gene product, component of a heterodimeric ABC transporter, is required for assembly of periplasmic cytochrome c and of cytochrome bd in Escherichia coli
journal, April 1994
- Poole, Robert K.; Gibson, Frank; Wu, Guanghui
- FEMS Microbiology Letters, Vol. 117, Issue 2
Rapid Evolution of Citrate Utilization by Escherichia coli by Direct Selection Requires citT and dctA
journal, February 2016
- Van Hofwegen, Dustin J.; Hovde, Carolyn J.; Minnich, Scott A.
- Journal of Bacteriology, Vol. 198, Issue 7
Essential genes as antimicrobial targets and cornerstones of synthetic biology
journal, November 2012
- Juhas, Mario; Eberl, Leo; Church, George M.
- Trends in Biotechnology, Vol. 30, Issue 11
Natural Variation in the Multidrug Efflux Pump SGE1 Underlies Ionic Liquid Tolerance in Yeast
journal, July 2018
- Higgins, Douglas A.; Young, Megan K. M.; Tremaine, Mary
- Genetics, Vol. 210, Issue 1
Metabolic engineering for the high-yield production of isoprenoid-based C5 alcohols in E. coli
journal, June 2015
- George, Kevin W.; Thompson, Mitchell G.; Kang, Aram
- Scientific Reports, Vol. 5, Issue 1
One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution.
journal, April 1989
- Chung, C. T.; Niemela, S. L.; Miller, R. H.
- Proceedings of the National Academy of Sciences, Vol. 86, Issue 7
Generation of a platform strain for ionic liquid tolerance using adaptive laboratory evolution
journal, November 2017
- Mohamed, Elsayed T.; Wang, Shizeng; Lennen, Rebecca M.
- Microbial Cell Factories, Vol. 16, Issue 1
Features of promising technologies for pretreatment of lignocellulosic biomass
journal, April 2005
- Mosier, Nathan; Wyman, Charles; Dale, Bruce
- Bioresource Technology, Vol. 96, Issue 6, p. 673-686
BreakDancer: an algorithm for high-resolution mapping of genomic structural variation
journal, August 2009
- Chen, Ken; Wallis, John W.; McLellan, Michael D.
- Nature Methods, Vol. 6, Issue 9
Development of an E. coli strain for one-pot biofuel production from ionic liquid pretreated cellulose and switchgrass
journal, January 2016
- Frederix, Marijke; Mingardon, Florence; Hu, Matthew
- Green Chemistry, Vol. 18, Issue 15
Impact of two ionic liquids, 1-ethyl-3-methylimidazolium acetate and 1-ethyl-3-methylimidazolium methylphosphonate, on Saccharomyces cerevisiae: metabolic, physiologic, and morphological investigations
journal, January 2015
- Mehmood, Nasir; Husson, Eric; Jacquard, Cédric
- Biotechnology for Biofuels, Vol. 8, Issue 1
Characterization of the Acetate-Producing Pathways in Escherichia coli
journal, January 2005
- Dittrich, Cheryl R.; Bennett, George N.; San, Ka-Yiu
- Biotechnology Progress, Vol. 21, Issue 4
Metabolic engineering of Escherichia coli for limonene and perillyl alcohol production
journal, September 2013
- Alonso-Gutierrez, Jorge; Chan, Rossana; Batth, Tanveer S.
- Metabolic Engineering, Vol. 19
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
Simple screening method to identify toxic/non-toxic ionic liquids: Agar diffusion test adaptation
journal, September 2012
- Ventura, Sónia P. M.; de Barros, Rafael L. F.; Sintra, Tânia
- Ecotoxicology and Environmental Safety, Vol. 83
Transformation of E. coli by Electroporation
journal, June 2006
- Sambrook, Joseph; Russell, David W.
- Cold Spring Harbor Protocols, Vol. 2006, Issue 1
Transcriptional reprogramming in yeast using dCas9 and combinatorial gRNA strategies
journal, March 2017
- Jensen, Emil D.; Ferreira, Raphael; Jakočiūnas, Tadas
- Microbial Cell Factories, Vol. 16, Issue 1
Tolerance engineering in bacteria for the production of advanced biofuels and chemicals
journal, August 2015
- Mukhopadhyay, Aindrila
- Trends in Microbiology, Vol. 23, Issue 8
Development of a Native Escherichia coli Induction System for Ionic Liquid Tolerance
journal, July 2014
- Frederix, Marijke; Hütter, Kimmo; Leu, Jessica
- PLoS ONE, Vol. 9, Issue 7
Identification of the cydC locus required for expression of the functional form of the cytochrome d terminal oxidase complex in Escherichia coli.
journal, May 1987
- Georgiou, C. D.; Fang, H.; Gennis, R. B.
- Journal of Bacteriology, Vol. 169, Issue 5
Direct Ethanol Production from Ionic Liquid-Pretreated Lignocellulosic Biomass by Cellulase-Displaying Yeasts
journal, November 2016
- Yamada, Ryosuke; Nakashima, Kazunori; Asai-Nakashima, Nanami
- Applied Biochemistry and Biotechnology, Vol. 182, Issue 1
Improving membrane protein expression and function using genomic edits
journal, October 2017
- Jensen, Heather M.; Eng, Thomas; Chubukov, Victor
- Scientific Reports, Vol. 7, Issue 1
Novel coiled-coil cell division factor ZapB stimulates Z ring assembly and cell division
journal, May 2008
- Ebersbach, Gitte; Galli, Elisa; Møller-Jensen, Jakob
- Molecular Microbiology, Vol. 68, Issue 3
Base-Catalyzed Depolymerization of Solid Lignin-Rich Streams Enables Microbial Conversion
journal, August 2017
- Rodriguez, Alberto; Salvachúa, Davinia; Katahira, Rui
- ACS Sustainable Chemistry & Engineering, Vol. 5, Issue 9
The Sequence Alignment/Map format and SAMtools
journal, June 2009
- Li, H.; Handsaker, B.; Wysoker, A.
- Bioinformatics, Vol. 25, Issue 16
Isopentenyl diphosphate (IPP)-bypass mevalonate pathways for isopentenol production
journal, March 2016
- Kang, Aram; George, Kevin W.; Wang, George
- Metabolic Engineering, Vol. 34
Demonstrating a separation-free process coupling ionic liquid pretreatment, saccharification, and fermentation with Rhodosporidium toruloides to produce advanced biofuels
journal, January 2018
- Sundstrom, Eric; Yaegashi, Junko; Yan, Jipeng
- Green Chemistry, Vol. 20, Issue 12
Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads
journal, June 2009
- Ye, K.; Schulz, M. H.; Long, Q.
- Bioinformatics, Vol. 25, Issue 21
Tracking the roots of cellulase hyperproduction by the fungus Trichoderma reesei using massively parallel DNA sequencing
journal, September 2009
- Le Crom, S.; Schackwitz, W.; Pennacchio, L.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 38
CydDC-mediated reductant export in Escherichia coli controls the transcriptional wiring of energy metabolism and combats nitrosative stress
journal, March 2016
- Holyoake, Louise V.; Hunt, Stuart; Sanguinetti, Guido
- Biochemical Journal, Vol. 473, Issue 6
Works referencing / citing this record:
Restoration of biofuel production levels and increased tolerance under ionic liquid stress is enabled by a mutation in the essential Escherichia coli gene cydC
text, January 2018
- Eng, Thomas; Demling, Philipp; Herbert, Robin A.
- RWTH Aachen University
Engineering Corynebacterium glutamicum to produce the biogasoline isopentenol from plant biomass hydrolysates
journal, February 2019
- Sasaki, Yusuke; Eng, Thomas; Herbert, Robin A.
- Biotechnology for Biofuels, Vol. 12, Issue 1
Immobilization of cellulase in the non-natural ionic liquid environments to enhance cellulase activity and functional stability
journal, January 2019
- Zhou, Min; Ju, Xin; Li, Liangzhi
- Applied Microbiology and Biotechnology, Vol. 103, Issue 6
Guanidine Riboswitch-Regulated Efflux Transporters Protect Bacteria against Ionic Liquid Toxicity
journal, April 2019
- Higgins, Douglas A.; Gladden, John M.; Kimbrel, Jeff A.
- Journal of Bacteriology, Vol. 201, Issue 13