Metabolic engineering of Escherichia coli for the production of butyric acid at high titer and productivity
Abstract
Background: Several anaerobic bacteria produce butyric acid, a commodity chemical with use in chemical, pharmaceutical, food and feed industries, using complex media with acetate as a co- product. Butyrate titer of various recombinant Escherichia coli did not exceed 10 g.l-1 in batch fermentations in any of the media tested. Results: A recombinant E. coli (strain LW393) that produced butyrate as the major fermentation product was constructed with genes from E. coli, Clostridium acetobutylicum and Treponema denticola. Strain LW393 produced 323 ± 6 mM (28.4 ± 0.4 g.l-1) butyric acid in batch fermentations in mineral salts medium with glucose as C-source at a yield of 0.37 ± 0.01 g.(g -1 glucose consumed) Supplementing this medium with yeast extract further increased butyric acid titer to 375 ± 4 mM. . Butyrate accounted for 90% of the total products produced by the culture. -1 -1 Average volumetric productivity of butyrate with xylose as C-source was 0.89 ± 0.07 g.l .h . Conclusions: The butyrate titer reported in this study is about 2.5-3-times higher than the values reported for other recombinant E. coli and this is achieved in mineral salts medium with an expectation of lower purification and production cost of butyrate.
- Authors:
-
- Univ. of Florida, Gainesville, FL (United States)
- Univ. of Florida, Gainesville, FL (United States); Hubei Univ., Wuhan (China)
- Publication Date:
- Research Org.:
- Univ. of Florida, Gainesville, FL (United States)
- Sponsoring Org.:
- USDOE Office of Policy and International Affairs (PO); US Department of Agriculture (USDA); USDOE Office of International Affairs (IA)
- OSTI Identifier:
- 1613814
- Alternate Identifier(s):
- OSTI ID: 1766300
- Grant/Contract Number:
- PI0000031; 2012-67009-19596; 2011-10006-30358
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Biotechnology for Biofuels
- Additional Journal Information:
- Journal Volume: 12; Journal Issue: 1; Journal ID: ISSN 1754-6834
- Publisher:
- BioMed Central
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 09 BIOMASS FUELS; Biotechnology & Applied Microbiology; Energy & Fuels; Butyrate; Fermentation; E. coli; Xylose; Mineral salt medium; xylose; mineral salts medium
Citation Formats
Wang, Liang, Chauliac, Diane, Moritz, Brelan E., Zhang, Guimin, Ingram, Lonnie O., and Shanmugam, K. T. Metabolic engineering of Escherichia coli for the production of butyric acid at high titer and productivity. United States: N. p., 2019.
Web. doi:10.1186/s13068-019-1408-9.
Wang, Liang, Chauliac, Diane, Moritz, Brelan E., Zhang, Guimin, Ingram, Lonnie O., & Shanmugam, K. T. Metabolic engineering of Escherichia coli for the production of butyric acid at high titer and productivity. United States. https://doi.org/10.1186/s13068-019-1408-9
Wang, Liang, Chauliac, Diane, Moritz, Brelan E., Zhang, Guimin, Ingram, Lonnie O., and Shanmugam, K. T. Fri .
"Metabolic engineering of Escherichia coli for the production of butyric acid at high titer and productivity". United States. https://doi.org/10.1186/s13068-019-1408-9. https://www.osti.gov/servlets/purl/1613814.
@article{osti_1613814,
title = {Metabolic engineering of Escherichia coli for the production of butyric acid at high titer and productivity},
author = {Wang, Liang and Chauliac, Diane and Moritz, Brelan E. and Zhang, Guimin and Ingram, Lonnie O. and Shanmugam, K. T.},
abstractNote = {Background: Several anaerobic bacteria produce butyric acid, a commodity chemical with use in chemical, pharmaceutical, food and feed industries, using complex media with acetate as a co- product. Butyrate titer of various recombinant Escherichia coli did not exceed 10 g.l-1 in batch fermentations in any of the media tested. Results: A recombinant E. coli (strain LW393) that produced butyrate as the major fermentation product was constructed with genes from E. coli, Clostridium acetobutylicum and Treponema denticola. Strain LW393 produced 323 ± 6 mM (28.4 ± 0.4 g.l-1) butyric acid in batch fermentations in mineral salts medium with glucose as C-source at a yield of 0.37 ± 0.01 g.(g -1 glucose consumed) Supplementing this medium with yeast extract further increased butyric acid titer to 375 ± 4 mM. . Butyrate accounted for 90% of the total products produced by the culture. -1 -1 Average volumetric productivity of butyrate with xylose as C-source was 0.89 ± 0.07 g.l .h . Conclusions: The butyrate titer reported in this study is about 2.5-3-times higher than the values reported for other recombinant E. coli and this is achieved in mineral salts medium with an expectation of lower purification and production cost of butyrate.},
doi = {10.1186/s13068-019-1408-9},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 12,
place = {United States},
year = {Fri Mar 22 00:00:00 EDT 2019},
month = {Fri Mar 22 00:00:00 EDT 2019}
}
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Works referenced in this record:
A Quantitative System-Scale Characterization of the Metabolism of Clostridium acetobutylicum
journal, November 2015
- Yoo, Minyeong; Bestel-Corre, Gwenaelle; Croux, Christian
- mBio, Vol. 6, Issue 6
Refactoring redox cofactor regeneration for high-yield biocatalysis of glucose to butyric acid in Escherichia coli
journal, May 2013
- Lim, Jae Hyung; Seo, Sang Woo; Kim, Se Yeon
- Bioresource Technology, Vol. 135
The no-SCAR (Scarless Cas9 Assisted Recombineering) system for genome editing in Escherichia coli
journal, October 2015
- Reisch, Chris R.; Prather, Kristala L. J.
- Scientific Reports, Vol. 5, Issue 1
Butyrate production under aerobic growth conditions by engineered Escherichia coli
journal, May 2017
- Kataoka, Naoya; Vangnai, Alisa S.; Pongtharangkul, Thunyarat
- Journal of Bioscience and Bioengineering, Vol. 123, Issue 5
Parametric studies of ethanol production form xylose and other sugars by recombinantEscherichia coli
journal, July 1991
- Beall, David S.; Ohta, K.; Ingram, L. O.
- Biotechnology and Bioengineering, Vol. 38, Issue 3
Flux through Citrate Synthase Limits the Growth of Ethanologenic Escherichia coli KO11 during Xylose Fermentation
journal, March 2002
- Underwood, S. A.; Buszko, M. L.; Shanmugam, K. T.
- Applied and Environmental Microbiology, Vol. 68, Issue 3
Construction and Characterization of ack Deleted Mutant of Clostridium tyrobutyricum for Enhanced Butyric Acid and Hydrogen Production
journal, January 2006
- Liu, Xiaoguang; Zhu, Ying; Yang, Shang-Tian
- Biotechnology Progress, Vol. 22, Issue 5
Acetone-butanol fermentation revisited.
journal, January 1986
- Jones, D. T.; Woods, D. R.
- Microbiological Reviews, Vol. 50, Issue 4
Low salt medium for lactate and ethanol production by recombinant Escherichia coli B
journal, December 2006
- Martinez, Alfredo; Grabar, T. B.; Shanmugam, K. T.
- Biotechnology Letters, Vol. 29, Issue 3, p. 397-404
A review of the potential mechanisms for the lowering of colorectal oncogenesis by butyrate
journal, June 2012
- Fung, Kim Y. C.; Cosgrove, Leah; Lockett, Trevor
- British Journal of Nutrition, Vol. 108, Issue 5
Direct Hydrogenation of Biomass-Derived Butyric Acid to n -Butanol over a Ruthenium-Tin Bimetallic Catalyst
journal, August 2014
- Lee, Jong-Min; Upare, Pravin P.; Chang, Jong-San
- ChemSusChem, Vol. 7, Issue 11
Butyric acid – a well-known molecule revisited
journal, January 2017
- Borycka-Kiciak, Katarzyna; Banasiewicz, Tomasz; Rydzewska, Grażyna
- Gastroenterology Review, Vol. 2
Recent advances and strategies in process and strain engineering for the production of butyric acid by microbial fermentation
journal, April 2018
- Luo, Hongzhen; Yang, Rongling; Zhao, Yuping
- Bioresource Technology, Vol. 253
In Situ Biocatalytic Synthesis of Butyl Butyrate in Diesel and Engine Evaluations
journal, November 2017
- Sjöblom, Magnus; Risberg, Per; Filippova, Alfia
- ChemCatChem, Vol. 9, Issue 24
Comprehensive characterization of toxicity of fermentative metabolites on microbial growth
journal, November 2017
- Wilbanks, Brandon; Trinh, Cong T.
- Biotechnology for Biofuels, Vol. 10, Issue 1
The Future of Butyric Acid in Industry
journal, January 2012
- Dwidar, Mohammed; Park, Jae-Yeon; Mitchell, Robert J.
- The Scientific World Journal, Vol. 2012
Fermentation of sweet sorghum derived sugars to butyric acid at high titer and productivity by a moderate thermophile Clostridium thermobutyricum at 50 °C
journal, December 2015
- Wang, Liang; Ou, Mark S.; Nieves, Ismael
- Bioresource Technology, Vol. 198
Frontiers in microbial 1-butanol and isobutanol production
journal, January 2016
- Chen, Chang-Ting; Liao, James C.
- FEMS Microbiology Letters, Vol. 363, Issue 5
Engineering the metabolism of Escherichia coli W3110 for the conversion of sugar to redox-neutral and oxidized products: Homoacetate production
journal, January 2003
- Causey, T. B.; Zhou, S.; Shanmugam, K. T.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 3, p. 825-832
Modeling of batch experimental kinetics and application to fed-batch fermentation of Clostridium tyrobutyricum for enhanced butyric acid production
journal, December 2010
- Song, Hyohak; Eom, Moon-Ho; Lee, Sira
- Biochemical Engineering Journal, Vol. 53, Issue 1
New insights into the butyric acid metabolism of Clostridium acetobutylicum
journal, May 2012
- Lehmann, Dörte; Radomski, Nadine; Lütke-Eversloh, Tina
- Applied Microbiology and Biotechnology, Vol. 96, Issue 5
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products
journal, May 2000
- Datsenko, K. A.; Wanner, B. L.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 12, p. 6640-6645
Butyric acid-producing anaerobic bacteria as a novel probiotic treatment approach for inflammatory bowel disease
journal, November 2009
- Van Immerseel, F.; Ducatelle, R.; De Vos, M.
- Journal of Medical Microbiology, Vol. 59, Issue 2
Engineered Production of Short Chain Fatty Acid in Escherichia coli Using Fatty Acid Synthesis Pathway
journal, July 2016
- Jawed, Kamran; Mattam, Anu Jose; Fatma, Zia
- PLOS ONE, Vol. 11, Issue 7
One-Step Sequence- and Ligation-Independent Cloning as a Rapid and Versatile Cloning Method for Functional Genomics Studies
journal, May 2012
- Jeong, Jae-Yeon; Yim, Hyung-Soon; Ryu, Ji-Young
- Applied and Environmental Microbiology, Vol. 78, Issue 15
Isolation and Characterization of Acid-Tolerant, Thermophilic Bacteria for Effective Fermentation of Biomass-Derived Sugars to Lactic Acid
journal, May 2006
- Patel, M. A.; Ou, M. S.; Harbrucker, R.
- Applied and Environmental Microbiology, Vol. 72, Issue 5, p. 3228-3235
The mechanism of inhibition by H2 of H2-evolution by hydrogenases
journal, January 2013
- Fourmond, Vincent; Baffert, Carole; Sybirna, Kateryna
- Chemical Communications, Vol. 49, Issue 61
Butyrate production in engineered Escherichia coli with synthetic scaffolds: Butyrate Production in Engineered Escherichia coli
journal, April 2013
- Baek, Jang-Mi; Mazumdar, Suman; Lee, Sang-Woo
- Biotechnology and Bioengineering, Vol. 110, Issue 10
Fermentative production of short-chain fatty acids in Escherichia coli
journal, July 2014
- Volker, Alexandra R.; Gogerty, David S.; Bartholomay, Christian
- Microbiology, Vol. 160, Issue 7
A novel prokaryotic trans -2-enoyl-CoA reductase from the spirochete Treponema denticola
journal, March 2007
- Tucci, Sara; Martin, William
- FEBS Letters, Vol. 581, Issue 8
Metabolic Engineering of Escherichia coli for Production of Butyric Acid
journal, May 2014
- Saini, Mukesh; Wang, Zei Wen; Chiang, Chung-Jen
- Journal of Agricultural and Food Chemistry, Vol. 62, Issue 19
Butyric acid-based feed additives help protect broiler chickens from Salmonella Enteritidis infection
journal, May 2009
- Fernández-Rubio, C.; Ordóñez, C.; Abad-González, J.
- Poultry Science, Vol. 88, Issue 5
Metabolic flexibility of a butyrate pathway mutant of Clostridium acetobutylicum
journal, March 2017
- Yoo, Minyeong; Croux, Christian; Meynial-Salles, Isabelle
- Metabolic Engineering, Vol. 40
Metabolic engineering of Clostridium acetobutylicum for butyric acid production with high butyric acid selectivity
journal, May 2014
- Jang, Yu-Sin; Im, Jung Ae; Choi, So Young
- Metabolic Engineering, Vol. 23
A novel prokaryotic trans-2-enoyl-CoA reductase from the spirochete Treponema denticola
journal, September 2007
- Tucci, Sara; Martin, William
- Chemistry and Physics of Lipids, Vol. 149
In Situ Biocatalytic Synthesis of Butyl Butyrate in Diesel and Engine Evaluations
journal, November 2017
- Sjöblom, Magnus; Risberg, Per; Filippova, Alfia
- ChemCatChem, Vol. 9, Issue 24
Direct Hydrogenation of Biomass-Derived Butyric Acid to n -Butanol over a Ruthenium-Tin Bimetallic Catalyst
journal, August 2014
- Lee, Jong-Min; Upare, Pravin P.; Chang, Jong-San
- ChemSusChem, Vol. 7, Issue 11
Low salt medium for lactate and ethanol production by recombinant Escherichia coli B
journal, December 2006
- Martinez, Alfredo; Grabar, T. B.; Shanmugam, K. T.
- Biotechnology Letters, Vol. 29, Issue 3, p. 397-404
The fermentation pathways of Escherichia coli
journal, September 1989
- Clark, D.
- FEMS Microbiology Reviews, Vol. 63, Issue 3
Modeling of batch experimental kinetics and application to fed-batch fermentation of Clostridium tyrobutyricum for enhanced butyric acid production
journal, December 2010
- Song, Hyohak; Eom, Moon-Ho; Lee, Sira
- Biochemical Engineering Journal, Vol. 53, Issue 1
Fermentation of sweet sorghum derived sugars to butyric acid at high titer and productivity by a moderate thermophile Clostridium thermobutyricum at 50 °C
journal, December 2015
- Wang, Liang; Ou, Mark S.; Nieves, Ismael
- Bioresource Technology, Vol. 198
Recent advances and strategies in process and strain engineering for the production of butyric acid by microbial fermentation
journal, April 2018
- Luo, Hongzhen; Yang, Rongling; Zhao, Yuping
- Bioresource Technology, Vol. 253
Butyrate production under aerobic growth conditions by engineered Escherichia coli
journal, May 2017
- Kataoka, Naoya; Vangnai, Alisa S.; Pongtharangkul, Thunyarat
- Journal of Bioscience and Bioengineering, Vol. 123, Issue 5
Metabolic flexibility of a butyrate pathway mutant of Clostridium acetobutylicum
journal, March 2017
- Yoo, Minyeong; Croux, Christian; Meynial-Salles, Isabelle
- Metabolic Engineering, Vol. 40
Construction and Characterization of ack Deleted Mutant of Clostridium tyrobutyricum for Enhanced Butyric Acid and Hydrogen Production
journal, January 2006
- Liu, Xiaoguang; Zhu, Ying; Yang, Shang-Tian
- Biotechnology Progress, Vol. 22, Issue 5
Metabolic Engineering of Escherichia coli for Production of Butyric Acid
journal, May 2014
- Saini, Mukesh; Wang, Zei Wen; Chiang, Chung-Jen
- Journal of Agricultural and Food Chemistry, Vol. 62, Issue 19
Design of stable and self-regulated microbial consortia for chemical synthesis
journal, March 2022
- Li, Xianglai; Zhou, Zhao; Li, Wenna
- Nature Communications, Vol. 13, Issue 1
The no-SCAR (Scarless Cas9 Assisted Recombineering) system for genome editing in Escherichia coli
journal, October 2015
- Reisch, Chris R.; Prather, Kristala L. J.
- Scientific Reports, Vol. 5, Issue 1
Engineering the metabolism of Escherichia coli W3110 for the conversion of sugar to redox-neutral and oxidized products: Homoacetate production
journal, January 2003
- Causey, T. B.; Zhou, S.; Shanmugam, K. T.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 3, p. 825-832
Frontiers in microbial 1-butanol and isobutanol production
journal, January 2016
- Chen, Chang-Ting; Liao, James C.
- FEMS Microbiology Letters, Vol. 363, Issue 5
Fermentative production of short-chain fatty acids in Escherichia coli
journal, July 2014
- Volker, Alexandra R.; Gogerty, David S.; Bartholomay, Christian
- Microbiology, Vol. 160, Issue 7
Volatile Fatty Acids and the Inhibition of
Escherichia coli
Growth by Rumen Fluid
journal, January 1969
- Wolin, Meyer J.
- Applied Microbiology, Vol. 17, Issue 1
Classic Spotlight: Electron Bifurcation, a Unifying Concept for Energy Conservation in Anaerobes
journal, April 2016
- Metcalf, William W.
- Journal of Bacteriology, Vol. 198, Issue 9
Construction of a butyrate-producing E. coli strain without the use of heterologous genes
journal, November 2010
- Seregina, T. A.; Shakulov, R. S.; Debabov, V. G.
- Applied Biochemistry and Microbiology, Vol. 46, Issue 8
Comprehensive characterization of toxicity of fermentative metabolites on microbial growth
journal, November 2017
- Wilbanks, Brandon; Trinh, Cong T.
- Biotechnology for Biofuels, Vol. 10, Issue 1
Engineered Production of Short Chain Fatty Acid in Escherichia coli Using Fatty Acid Synthesis Pathway
journal, July 2016
- Jawed, Kamran; Mattam, Anu Jose; Fatma, Zia
- PLOS ONE, Vol. 11, Issue 7
Butyric acid-based feed additives help protect broiler chickens from Salmonella Enteritidis infection
journal, May 2009
- Fernández-Rubio, C.; Ordóñez, C.; Abad-González, J.
- Poultry Science, Vol. 88, Issue 5
Butyric acid – a well-known molecule revisited
journal, January 2017
- Borycka-Kiciak, Katarzyna; Banasiewicz, Tomasz; Rydzewska, Grażyna
- Gastroenterology Review, Vol. 2
Works referencing / citing this record:
Enhanced Production of High‐Value Cyclopropane Fatty Acid in Yeast Engineered for Increased Lipid Synthesis and Accumulation
journal, October 2018
- Peng, Huadong; He, Lizhong; Haritos, Victoria S.
- Biotechnology Journal, Vol. 14, Issue 4
Volatile fatty acids as novel building blocks for oil‐based chemistry via oleaginous yeast fermentation
journal, October 2019
- Llamas, Mercedes; Magdalena, Jose Antonio; González‐Fernández, Cristina
- Biotechnology and Bioengineering, Vol. 117, Issue 1
Perspectives for the biotechnological production of biofuels from CO2 and H2 using Ralstonia eutropha and other ‘Knallgas’ bacteria
journal, January 2019
- Brigham, Christopher
- Applied Microbiology and Biotechnology, Vol. 103, Issue 5
Syngas-aided anaerobic fermentation for medium-chain carboxylate and alcohol production: the case for microbial communities
journal, October 2019
- Baleeiro, Flávio C. F.; Kleinsteuber, Sabine; Neumann, Anke
- Applied Microbiology and Biotechnology, Vol. 103, Issue 21-22
Recent advances in the applications of promoter engineering for the optimization of metabolite biosynthesis
journal, January 2019
- Xu, Ning; Wei, Liang; Liu, Jun
- World Journal of Microbiology and Biotechnology, Vol. 35, Issue 2
Modeling the Interplay between Photosynthesis, CO2 Fixation, and the Quinone Pool in a Purple Non-Sulfur Bacterium
journal, September 2019
- Alsiyabi, Adil; Immethun, Cheryl M.; Saha, Rajib
- Scientific Reports, Vol. 9, Issue 1
A comprehensive metabolic map for production of bio-based chemicals
journal, January 2019
- Lee, Sang Yup; Kim, Hyun Uk; Chae, Tong Un
- Nature Catalysis, Vol. 2, Issue 1
Starter consortia for on-farm cocoa fermentation and their quality attributes
journal, November 2019
- Saunshi, Yallappa Basappa; Sandhya, Mudrakola Vidya Sagar; Rastogi, Navin Kumar
- Preparative Biochemistry & Biotechnology, Vol. 50, Issue 3
Impact of forced fatty acid synthesis on metabolism and physiology of Saccharomyces cerevisiae
journal, August 2018
- Gossing, Michael; Smialowska, Agata; Nielsen, Jens
- FEMS Yeast Research, Vol. 18, Issue 8
Effects of overexpression of STB5 in Saccharomyces cerevisiae on fatty acid biosynthesis, physiology and transcriptome
journal, March 2019
- Bergman, Alexandra; Vitay, Dóra; Hellgren, John
- FEMS Yeast Research, Vol. 19, Issue 3
Effects of a high-cultivation temperature on the physiology of three different Yarrowia lipolytica strains
journal, October 2019
- Hackenschmidt, S.; Bracharz, F.; Daniel, R.
- FEMS Yeast Research, Vol. 19, Issue 7
Boosting Secondary Metabolite Production and Discovery through the Engineering of Novel Microbial Biosensors
journal, July 2018
- de Frias, Ulysses Amancio; Pereira, Greicy Kelly Bonifacio; Guazzaroni, María-Eugenia
- BioMed Research International, Vol. 2018
Peroxisomes and peroxisomal transketolase and transaldolase enzymes are essential for xylose alcoholic fermentation by the methylotrophic thermotolerant yeast, Ogataea (Hansenula) polymorpha
journal, July 2018
- Kurylenko, Olena O.; Ruchala, Justyna; Vasylyshyn, Roksolana V.
- Biotechnology for Biofuels, Vol. 11, Issue 1
Nutrient composition and safety evaluation of simulated isobutanol distillers dried grains with solubles and associated fermentation metabolites when fed to male Ross 708 broiler chickens (Gallus domesticus)
journal, July 2019
- Roper, Jason M.; Smith, Brenda L.; Caverly Rae, Jessica M.
- PLOS ONE, Vol. 14, Issue 7
Hydrogel Microparticles Functionalized with Engineered Escherichia coli as Living Lactam Biosensors
journal, December 2019
- Ma, Conghui; Li, Jie; Zhang, Boyin
- Sensors, Vol. 19, Issue 24
Principles and practice of designing microbial biocatalysts for fuel and chemical production
journal, March 2021
- Shanmugam, K. T.; Ingram, Lonnie O.
- Journal of Industrial Microbiology and Biotechnology, Vol. 49, Issue 2