Biosynthesis of butenoic acid through fatty acid biosynthesis pathway in Escherichia coli
- 529 Downloads
- 3 Citations
Abstract
Butenoic acid is a C4 short-chain unsaturated fatty acid mainly used in the preparation of resins, pharmaceuticals, and fine chemicals. However, butenoic acid derived from petroleum is costly and unfriendly to the environment. Here, we report a novel biosynthetic strategy to produce butenoic acid by utilizing the intermediate of fatty acid biosynthesis pathway in engineered Escherichia coli. A thioesterase gene (B. thetaiotaomicron thioesterase (bTE)) from Bacteroides thetaiotaomicron was heterologously expressed in E. coli to specifically convert butenoyl-acyl carrier protein (ACP), a fatty acid biosynthesis intermediate, to butenoic acid. The titer of butenoic acid ranged from 0.07 to 11.4 mg/L in four different E. coli strains with varied expressing vectors. Deletion of endogenous fadD gene (encoding acyl-CoA synthetase) to block fatty acid oxidation improved the butenoic acid production in all strains to some extent. The highest butenoic acid accumulation of 18.7 mg/L was obtained in strain XP-2 (BL21-∆fadD/pET28a-bTE). Moreover, partially inhibiting the enoyl-ACP reductase (FabI) of strain XP-2 by triclosan increased butenoic acid production by threefold, and the butenoic acid titer was further increased to 161.4 mg/L by supplying glucose and tryptone in the M9 medium. Fed-batch fermentation of this strain further enhanced butenoic acid production to 4.0 g/L within 48 h. The butenoic acid tolerance assay revealed that this strain could tolerate 15–20 g/L of butenoic acid.
Keywords
Butenoic acid Escherichia coli Bacteroides thetaiotaomicron thioesterase Fatty acid biosynthesisNotes
Acknowledgments
This work was supported by the National Natural Science Foundation of China (31170040, 31200081) and Chinese Academy of Sciences (KGZD-EW-606).
Supplementary material
References
- Abdel-Rahman MA, Tashiro Y, Sonomoto K (2013) Recent advances in lactic acid production by microbial fermentation processes. Biotechnol Adv 31:877–902PubMedCrossRefGoogle Scholar
- Ai GM, Zhu JX, Dong XZ, Sun T (2013) Simultaneous characterization of methane and carbon dioxide produced by cultured methanogens using gas chromatography/isotope ratio mass spectrometry and gas chromatography/mass spectrometry. Rapid Commun Mass Spectrom 27:1935–1944PubMedCrossRefGoogle Scholar
- Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2:2006.0008PubMedCentralPubMedCrossRefGoogle Scholar
- Barnes EM (1975) Long chain fatty acyl-thioesterases I and II from Escherichia coli. Meth Enzymol 35:102–109PubMedCrossRefGoogle Scholar
- Barnes EM, Swindell A, Wakil SJ (1970) Purification and properties of a palmityl thioesterase II from Escherichia coli. J Biol Chem 245:3122–3128PubMedGoogle Scholar
- Black PN, DiRusso C, Metzger A, Heimert T (1992) Cloning, sequencing, and expression of the fadD gene of Escherichia coli encoding acyl coenzyme A synthetase. J Biol Chem 267:25513–25520PubMedGoogle Scholar
- Cantu DC, Chen Y, Reilly PJ (2010) Thioesterases: a new perspective based on their primary and tertiary structures. Protein Sci 19:1281–1295PubMedCentralPubMedCrossRefGoogle Scholar
- Cho H, Cronan J (1993) Escherichia coli thioesterase I, molecular cloning and sequencing of the structural gene and identification as a periplasmic enzyme. J Biol Chem 268:9238–9245PubMedGoogle Scholar
- Cronan JE, Thomas J (2009) Bacterial fatty acid synthesis and its relationships with polyketide synthetic pathways. Methods Enzymol 459:395–433PubMedCentralPubMedCrossRefGoogle Scholar
- Cummings J, Pomare E, Branch W, Naylor C, Macfarlane G (1987) Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28:1221–1227PubMedCentralPubMedCrossRefGoogle Scholar
- Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640–6645PubMedCentralPubMedCrossRefGoogle Scholar
- Davis MS, Solbiati J, Cronan JE (2000) Overproduction of acetyl-CoA carboxylase activity increases the rate of fatty acid biosynthesis in Escherichia coli. J Biol Chem 275:28593–28598PubMedCrossRefGoogle Scholar
- Dehesh K, Edwards P, Hayes T, Cranmer AM, Fillatti J (1996) Two novel thioesterases are key determinants of the bimodal distribution of acyl chain length of Cuphea palustris seed oil. Plant Physiol 110:203–210PubMedCentralPubMedCrossRefGoogle Scholar
- Dellomonaco C, Clomburg JM, Miller EN, Gonzalez R (2011) Engineered reversal of the β-oxidation cycle for the synthesis of fuels and chemicals. Nature 476:355–359PubMedCrossRefGoogle Scholar
- Escalada MG, Harwood JL, Maillard JY, Ochs D (2005) Triclosan inhibition of fatty acid synthesis and its effect on growth of Escherichia coli and Pseudomonas aeruginosa. J Antimicrob Chemother 55:879–882PubMedCrossRefGoogle Scholar
- Fujita Y, Matsuoka H, Hirooka K (2007) Regulation of fatty acid metabolism in bacteria. Mol Microbiol 66:829–839PubMedCrossRefGoogle Scholar
- Ghanta M, Fahey D, Subramaniam B (2013) Environmental impacts of ethylene production from diverse feedstocks and energy sources. Appl Petrochem Res 4:167–179CrossRefGoogle Scholar
- Handke P, Lynch SA, Gill RT (2011) Application and engineering of fatty acid biosynthesis in Escherichia coli for advanced fuels and chemicals. Metab Eng 13:28–37PubMedCrossRefGoogle Scholar
- He L, Xu YQ, Zhang XH (2008) Medium factor optimization and fermentation kinetics for phenazine-1-carboxylic acid production by Pseudomonas sp M18G. Biotechnol Bioeng 100:250–259PubMedCrossRefGoogle Scholar
- Heath RJ, Rock CO (2000) Microbiology: a triclosan-resistant bacterial enzyme. Nature 406:145–146PubMedCrossRefGoogle Scholar
- Hu G, Li J, Zeng G (2013) Recent development in the treatment of oily sludge from petroleum industry: a review. J Hazard Mater 261:470–490PubMedCrossRefGoogle Scholar
- Jang M, Kamens RM (2001) Characterization of secondary aerosol from the photooxidation of toluene in the presence of NOx and 1-propene. Environ Sci Technol 35:3626–3639PubMedCrossRefGoogle Scholar
- Jeffries TW (2005) Ethanol fermentation on the move. Nat Biotechnol 23:40–41PubMedCrossRefGoogle Scholar
- Jensen KF (1993) The Escherichia coli K-12 “wild types” W3110 and MG1655 have an rph frameshift mutation that leads to pyrimidine starvation due to low pyrE expression levels. J Bacteriol 175:3401–3407PubMedCentralPubMedGoogle Scholar
- Jing FY, Cantu D, Tvaruzkova J, Chipman J, Nikolau B, Yandeau-Nelson M, Reilly P (2011) Phylogenetic and experimental characterization of an acyl-ACP thioesterase family reveals significant diversity in enzymatic specificity and activity. BMC Biochem 12:44PubMedCentralPubMedCrossRefGoogle Scholar
- Kang Y, Durfee T, Glasner JD, Qiu Y, Frisch D, Winterberg KM, Blattner FR (2004) Systematic mutagenesis of the Escherichia coli genome. J Bacteriol 186:4921–4930PubMedCentralPubMedCrossRefGoogle Scholar
- Lan EI, Liao JC (2013) Microbial synthesis of n-butanol, isobutanol, and other higher alcohols from diverse resources. Bioresour Technol 135:339–349PubMedCrossRefGoogle Scholar
- Li J, Zhao JB, Zhao M, Yang YL, Jiang WH, Yang S (2010) Screening and characterization of butanol-tolerant micro-organisms. Lett Appl Microbiol 50:373–379PubMedCrossRefGoogle Scholar
- Lofty WA, Ghanem KM, El-Helow ER (2007) Citric acid production by a novel Aspergillus niger isolate: II. Optimization of process parameters through statistical experimental designs. Bioresour Technol 98:3470–3477CrossRefGoogle Scholar
- Lu H, Tonge PJ (2008) Inhibitors of FabI, an enzyme drug target in the bacterial fatty acid biosynthesis pathway. Acc Chem Res 41:11–20PubMedCrossRefGoogle Scholar
- Ma R, Ouyang J, Li X, Lian ZN, Cai C (2012) Simultaneous determination of organic acids and saccharides in lactic acid fermentation broth from biomass using high performance liquid chromatography. Se Pu 30:62–66PubMedGoogle Scholar
- Masih M, Algahtani I, De Mello L (2010) Price dynamics of crude oil and the regional ethylene markets. Energy Econ 32:1435–1444CrossRefGoogle Scholar
- McMurry LM, Oethinger M, Levy SB (1998) Triclosan targets lipid synthesis. Nature 394:531–532PubMedCrossRefGoogle Scholar
- Nikolau BJ, Perera MA, Brachova L, Shanks B (2008) Platform biochemicals for a biorenewable chemical industry. Plant J Cell Mol Biol 54:536–545CrossRefGoogle Scholar
- Reitzer L (2003) Nitrogen assimilation and global regulation in Escherichia coli. Ann Rev Microbiol 57:155–176CrossRefGoogle Scholar
- Riesenberg D, Menzel K, Schulz V, Schumann K, Veith G, Zuber G, Knorre WA (1990) High cell density fermentation of recombinant Escherichia coli expressing human interferon alpha 1. Appl Microbiol Biotechnol 34:77–82PubMedCrossRefGoogle Scholar
- Rollat I, Samain H, Morel O (2006) Reshapable hair styling composition comprising (meth)acrylic copolymers of four or more monomers. US 07122175Google Scholar
- Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
- Saraydin D, Karadag E, Guven O (1998) The releases of agrochemicals from radiation induced acrylamide crotonic acid hydrogels. Polym Bull 41:577–584CrossRefGoogle Scholar
- Schneider J, Niermann K, Wendisch VF (2011) Production of the amino acids L-glutamate, L-lysine, L-ornithine and L-arginine from arabinose by recombinant Corynebacterium glutamicum. J Biotechnol 154:191–198PubMedCrossRefGoogle Scholar
- Schulz RP, Blumenstein J, Kohlpaintner C (2000) Crotonaldehyde and crotonic acid. Ullmann’s encyclopedia of chemical technology. Wiley, WeinheimGoogle Scholar
- Schummer C, Delhomme O, Appenzeller BMR, Wennig R, Millet M (2009) Comparison of MTBSTFA and BSTFA in derivatization reactions of polar compounds prior to GC/MS analysis. Talanta 77:1473–1482PubMedCrossRefGoogle Scholar
- Thomason LC, Costantino N, Court DL (2007) E. coli genome manipulation by P1 transduction. Curr Protoc Mol Biol 79:1.17.11–11.17.18Google Scholar
- Torella JP, Ford TJ, Kim SN, Chen AM, Way JC, Silver PA (2013) Tailored fatty acid synthesis via dynamic control of fatty acid elongation. Proc Natl Acad Sci U S A 110:11290–11295PubMedCentralPubMedCrossRefGoogle Scholar
- Tsay J-T, Oh W, Larson T, Jackowski S, Rock C (1992) Isolation and characterization of the beta-ketoacyl-acyl carrier protein synthase III gene (fabH) from Escherichia coli K-12. J Biol Chem 267:6807–6814PubMedGoogle Scholar
- Vanderheide E, Zwinkels M, Gerritsen A, Scholten J (1992) Oxidation of ethylene to acetaldehyde over a heterogenized surface-vanadate wacker catalyst in the absence of gaseous oxygen. Appl Catal A Gen 86:181–198CrossRefGoogle Scholar
- Verwoert I, Verbree E, Van der Linden K, Nijkamp H, Stuitje A (1992) Cloning, nucleotide sequence, and expression of the Escherichia coli fabD gene, encoding malonyl coenzyme A-acyl carrier protein transacylase. J Bacteriol 174:2851–2857PubMedCentralPubMedGoogle Scholar
- Voelker TA, Davies HM (1994) Alteration of the specificity and regulation of fatty acid synthesis of Escherichia coli by expression of a plant medium-chain acyl-acyl carrier protein thioesterase. J Bacteriol 176:7320–7327PubMedCentralPubMedGoogle Scholar
- Wakaki S, Yamamoto T, Enoki H (2008) Stabilizing agent for chlorine containing polymer used for chlorine containing polymer composition, contains epoxy-group containing acrylic resin, amino crotonic-acid ester, polyhydric alcohol and/or hindered amine or phenyl indole. WO2008087784-A1; JP2008195912-A; JP5192182-B2Google Scholar
- Wang Z, Yan M, Chen X, Li DS, Qin L, Li ZJ, Yao J, Liang XL (2013) Mixed culture of Saccharomyces cerevisiae and Acetobacter pasteurianus for acetic acid production. Biochem Eng J 79:41–45CrossRefGoogle Scholar
- Yuan L, Voelker TA, Hawkins DJ (1995) Modification of the substrate specificity of an acyl-acyl carrier protein thioesterase by protein engineering. Proc Natl Acad Sci U S A 92:10639–10643PubMedCentralPubMedCrossRefGoogle Scholar
- Zeiller J-J, Dumas H, Guyard-Dangremont V, Berard I, Contard F, Guerrier D, Ferrand G, Bonhomme Y (2012) Butenoic acid derivatives, processes for the preparation thereof, pharmaceutical compositions comprising them, and use for the treatment of dyslipidaemia, atherosclerosis and diabetes. US 08247448Google Scholar
- Zhang XJ, Li M, Agrawal A, San KY (2011) Efficient free fatty acid production in Escherichia coli using plant acyl-ACP thioesterases. Metab Eng 13:713–722PubMedCrossRefGoogle Scholar
- Zheng Y, Li L, Liu Q, Qin W, Yang J, Cao Y, Jiang X, Zhao G, Xian M (2012) Boosting the free fatty acid synthesis of Escherichia coli by expression of a cytosolic Acinetobacter baylyi thioesterase. Biotechnol Biofuels 5:76PubMedCentralPubMedCrossRefGoogle Scholar