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The challenges and prospects of Escherichia coli as an organic acid production host under acid stress

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Abstract

Objective

Organic acids have a wide range of applications and have attracted the attention of many industries, and their large-scale applications have led fermentation production to low-cost development. Among them, the microbial fermentation method, especially using Escherichia coli as the production host, has the advantages of fast growth and low energy consumption, and has gradually shown better advantages and prospects in organic acid fermentation production.

Importance

However, when the opportunity comes, the acidified environment caused by the acid products accumulated during the fermentation process also challenges E. coli. The acid sensitivity of E. coli is a core problem that needs to be solved urgently. The addition of neutralizers in traditional operations led to the emergence of osmotic stress inadvertently, the addition of strong acid substances to recover products in the salt state not only increases production costs, but the discharged sewage is also harmful to the environment.

Elaboration

This article summarizes the current status of the application of E. coli in the production of organic acids, and based on the impact of acid stress on the physiological state of cells and the impact of industrial production profits, put forward some new conjectures that can make up for the deficiencies in existing research and application.

Implication

At this point, the diversified transformation of E. coli has become a chassis microbe that is more suitable for industrial fermentation, enhancing industrial application value.

Key points

• E. coli is a potential host for high value-added organic acids production.

• Classify the damage mechanism and coping strategies of E. coli when stimulated by acid molecules.

• Multi-dimensional expansion tools are needed to create acid-resistant E. coli chassis.

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References

  • Accardi A, Miller C (2004) Secondary active transport mediated by a prokaryotic homologue of ClC Cl- channels. Nature 427:803–807

    Article  CAS  PubMed  Google Scholar 

  • Ahn JH, Jang YS, Lee SY (2016) Production of succinic acid by metabolically engineered microorganisms. Curr Opin Biotechnol 42:54–66

    Article  CAS  PubMed  Google Scholar 

  • Aiso T, Kamiya S, Yonezawa H, Gamou S (2014) Overexpression of an antisense RNA, ArrS, increases the acid resistance of Escherichia coli. Microbiol-Sgm 160:954–961

    Article  CAS  Google Scholar 

  • Basilio D, Noack K, Picollo A, Accardi A (2014) Conformational changes required for H(+)/Cl(-) exchange mediated by a CLC transporter. Nat Struct Mol Biol 21:456–463. https://doi.org/10.1038/nsmb.2814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biot-Pelletier D, Martin VJ (2014) Evolutionary engineering by genome shuffling. Appl Microbiol Biotechnol 98:3877–3887. https://doi.org/10.1007/s00253-014-5616-8

    Article  CAS  PubMed  Google Scholar 

  • Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997) The complete genome sequence of Escherichia coli K-12. Science 277:1453–1462. https://doi.org/10.1126/science.277.5331.1453

    Article  CAS  PubMed  Google Scholar 

  • Booth IR, Blount P (2012) The MscS and MscL families of mechanosensitive channels act as microbial emergency release valves. J Bacteriol 194:4802–4809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bozell JJ, Petersen GR (2010) Technology development for the production of biobased products from biorefinery carbohydrates-the US Department of Energy’s “Top 10” revisited. Green Chem 12:539–554

    Article  CAS  Google Scholar 

  • Brown JL, Ross T, McMeekin TA, Nichols PD (1997) Acid habituation of Escherichia coli and the potential role of cyclopropane fatty acids in low pH tolerance. Int J Food Microbiol 37:163–173

    Article  CAS  PubMed  Google Scholar 

  • Carpenter CE, Broadbent JR (2009) External concentration of organic acid anions and pH: key independent variables for studying how organic acids inhibit growth of bacteria in mildly acidic foods. J Food Sci 74:R12-15. https://doi.org/10.1111/j.1750-3841.2008.00994.x

    Article  CAS  PubMed  Google Scholar 

  • Castanie-Cornet MP, Penfound TA, Smith D, Elliott JF, Foster JW (1999) Control of acid resistance in Escherichia coli. J Bacteriol 181:3525–3535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castano-Cerezo S, Bernal V, Post H, Fuhrer T, Cappadona S, Sanchez-Diaz NC, Sauer U, Heck AJR, Altelaar AMF, Canovas M (2014) Protein acetylation affects acetate metabolism, motility and acid stress response in Escherichia coli. Mol Syst Biol 10

  • Chang P, Grey S, Hsiang-Yuan C, Ken C, Lu W,  Shen CR (2017) Engineering efficient production of itaconic acid from diverse substrates in Escherichia coli. J. Biotechnol. 24973-81. https://doi.org/10.1016/j.jbiotec.2017.03.026

  • Chen YY, Ganzle MG (2016) Influence of cyclopropane fatty acids on heat, high pressure, acid and oxidative resistance in Escherichia coli. Int J Food Microbiol 222:16–22. https://doi.org/10.1016/j.ijfoodmicro.2016.01.017

    Article  CAS  PubMed  Google Scholar 

  • Chen YX, Boggess EE, Ocasio ER, Warner A, Kerns L, Drapal V, Gossling C, Ross W, Gourse RL, Shao ZY, Dickerson J, Mansell TJ, Jarboe LR (2020) Reverse engineering of fatty acid-tolerant Escherichia coli identifies design strategies for robust microbial cell factories. Metab Eng 61:120–130. https://doi.org/10.1016/j.ymben.2020.05.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen TJ, Wang JQ, Yang R, Li JC, Lin M, Lin ZL (2011) Laboratory-evolved mutants of an exogenous global regulator, IrrE from Deinococcus radiodurans, enhance stress tolerances of Escherichia coli. PLoS One 6

  • Cheng KK, Zeng J, Jian JH, Zhu JF, Zhang GX, Liu DH (2019) Model-based temperature control for improving lactic acid production from glycerol. RSC Adv 9:11614–11620. https://doi.org/10.1039/c9ra01323g

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clausen T, Kaiser M, Huber R, Ehrmann M (2011) HTRA proteases: regulated proteolysis in protein quality control. Nat Rev Mol Cell Biol 12:152–162. https://doi.org/10.1038/nrm3065

    Article  CAS  PubMed  Google Scholar 

  • Costello SM, Plummer AM, Fleming PJ, Fleming KG (2016) Dynamic periplasmic chaperone reservoir facilitates biogenesis of outer membrane proteins. Proc Natl Acad Sci U S A 113:E4794-4800. https://doi.org/10.1073/pnas.1601002113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Danhier F, Ansorena E, Silva JM, Coco R, Le Breton A, Preat V (2012) PLGA-based nanoparticles: an overview of biomedical applications. J Control Release 161:505–522

    Article  CAS  PubMed  Google Scholar 

  • Deng Y, Ma N, Zhu KJ, Mao Y, Wei XT, Zhao YY (2018) Balancing the carbon flux distributions between the TCA cycle and glyoxylate shunt to produce glycolate at high yield and titer in Escherichia coli. Metab Eng 46:28–34

    Article  CAS  PubMed  Google Scholar 

  • Dhar R, Slusky JS (2021) Outer membrane protein evolution. Curr Opin Struct Biol 68:122–128. https://doi.org/10.1016/j.sbi.2021.01.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Djukic-Vukovic A, Mladenovic D, Ivanovic J, Pejin J, Mojovic L (2019) Towards sustainability of lactic acid and poly-lactic acid polymers production. Renew Sust Energ Rev 108:238–252

    Article  CAS  Google Scholar 

  • Du B, Yang L, Lloyd CJ, Fang X, Palsson BO (2019) Genome-scale model of metabolism and gene expression provides a multi-scale description of acid stress responses in Escherichia coliEscherichia coli. PLoS Comput Biol 15:e1007525. https://doi.org/10.1371/journal.pcbi.1007525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du B, Olson CA, Sastry AV, Fang X, Phaneuf PV, Chen K, Wu MY, Szubin R, Xu SB, Gao Y, Hefner Y, Feist AM, Palsson BO (2020) Adaptive laboratory evolution of Escherichia coli under acid stress. Microbiol-Sgm 166:141–148. https://doi.org/10.1099/mic.0.000867

    Article  CAS  Google Scholar 

  • Eguchi Y, Ishii E, Hata K, Utsumi R (2011) Regulation of acid resistance by connectors of two-component signal transduction systems in Escherichia coliEscherichia coli. J Bacteriol 193:1222–1228

    Article  CAS  PubMed  Google Scholar 

  • Eklund T (1983) The antimicrobial effect of dissociated and undissociated sorbic acid at different pH levels. J Appl Bacteriol 54:383–389

    Article  CAS  PubMed  Google Scholar 

  • Finch AJ, Kim JR (2018) Thermophilic proteins as versatile scaffolds for protein engineering. Microorganisms 6

  • Foster JW (2004) Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol 2:898–907

    Article  CAS  PubMed  Google Scholar 

  • Fu XM, Wang Y, Shao HQ, Ma J, Song XW, Zhang M, Chang ZY (2018) DegP functions as a critical protease for bacterial acid resistance. Febs J 285:3525–3538. https://doi.org/10.1111/febs.14627

    Article  CAS  PubMed  Google Scholar 

  • Fu XM, Wang YX, Wang JH, Garza E, Manow R, Zhou SD (2017) Semi-industrial scale (30 m(3)) fed-batch fermentation for the production of D-lactate by Escherichia coli strain HBUT-D15. J Ind Microbiol Biotechnol 44:221–228. https://doi.org/10.1007/s10295-016-1877-9

  • Gaida SM, Al-Hinai MA, Indurthi DC, Nicolaou SA, Papoutsakis ET (2013) Synthetic tolerance: three noncoding small RNAs, DsrA, ArcZ and RprA, acting supra-additively against acid stress. Nucleic Acids Res 41:8726–8737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gajiwala KS, Burley SK (2000) HDEA, a periplasmic protein that supports acid resistance in pathogenic enteric bacteria. J Mol Biol 295:605–612

    Article  CAS  PubMed  Google Scholar 

  • Galarneau A, Primeau M, Trudeau LE, Michnick SW (2002) beta-Lactamase protein fragment complementation assays as in vivo and in vitro sensors of protein-protein interactions. Nat Biotechnol 20:619–622

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Jiang L, Zhu LY, Xu Q, Xu X, Huang H (2016) Tailoring of global transcription sigma D factor by random mutagenesis to improve Escherichia coli tolerance towards low-pHs. J Biotechnol 224:55–63. https://doi.org/10.1016/j.jbiotec.2016.03.012

    Article  CAS  PubMed  Google Scholar 

  • Gong S, Richard H, Foster JW (2003) YjdE (AdiC) is the arginine: agmatine antiporter essential for arginine-dependent acid resistance in Escherichia coli. J Bacteriol 185:4402–4409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodson M, Rowbury R (1989) Habituation to normally lethal acidity by prior growth of Escherichia coli at a sub-lethal acid pH value. Lett Appl Microbiol 8:77–79

    Article  Google Scholar 

  • Grabar, T., Gong, W., and Yocum, R.R. (2018). Metabolic evolution of Escherichia coli strains that produce organic acids. (Google Patents).

  • Gregersen N, Bross P, Vang S, Christensen JH (2006) Protein misfolding and human disease. Annu Rev Genomics Hum Genet 7:103–124. https://doi.org/10.1146/annurev.genom.7.080505.115737

    Article  CAS  PubMed  Google Scholar 

  • Grogan DW, Cronan JE (1997) Cyclopropane ring formation in membrane lipids of bacteria. Microbiol Mol Biol Rev 61:429-

    Google Scholar 

  • Guettler MV, Jain MK, Soni BK (1996) Process for making succinic acid, microorganisms for use in the process and methods of obtaining the microorganisms. (Google Patents)

  • Guin D, Gruebele M (2019) Weak chemical interactions that drive protein evolution: crowding, sticking, and quinary structure in folding and function. Chem Rev 119:10691–10717. https://doi.org/10.1021/acs.chemrev.8b00753

    Article  CAS  PubMed  Google Scholar 

  • Hadicke O, Klamt S (2017) EColiCore2: a reference network model of the central metabolism of Escherichia coli and relationships to its genome-scale parent model (vol 7, 39617, 2017). Sci Rep 7

  • Harder, B.J., Bettenbrock, K., and Klamt, S. (2018). Temperature‐dependent dynamic control of the TCA cycle increases volumetric productivity of itaconic acid production by Escherichia coli. Biotechnol. Bioeng. 115: 156-164. https://doi.org/10.1002/bit.26446

  • Harper JW, Bennett EJ (2016) Proteome complexity and the forces that drive proteome imbalance. Nature 537:328–338. https://doi.org/10.1038/nature19947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475:324–332

    Article  CAS  PubMed  Google Scholar 

  • Haswell ES, Phillips R, Rees DC (2011) Mechanosensitive channels: what can they do and how do they do it? Structure 19:1356–1369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He YC, Xu JH, Su JH, Zhou L (2010) Bioproduction of glycolic acid from glycolonitrile with a new bacterial isolate of Alcaligenes sp ECU0401. Appl Biochem Biotechnol 160:1428–1440

    Article  CAS  PubMed  Google Scholar 

  • He D, Zhang M, Liu SB, Xie X, Chen PR (2019) Protease-mediated protein quality control for bacterial acid resistance. Cell Chem Biol 26:144-+

    Article  CAS  PubMed  Google Scholar 

  • He X, Xue T, Ma Y, Zhang J, Wang Z, Hong J, Hui L, Qiao J, Song H, Zhang M (2019b) Identification of functional butanol-tolerant genes from Escherichia coli mutants derived from error-prone PCR-based whole-genome shuffling. Biotechnol Biofuels 12:73. https://doi.org/10.1186/s13068-019-1405-z

    Article  PubMed  PubMed Central  Google Scholar 

  • Hong WZ, Jiao WW, Hu JC, Zhang JR, Liu C, Fu XM, Shen D, Xia B, Chang ZY (2005) Periplasmic protein HdeA exhibits chaperone-like activity exclusively within stomach pH range by transforming into disordered conformation. J Biol Chem 280:27029–27034

    Article  CAS  PubMed  Google Scholar 

  • Hong WZ, Wu YE, Fu XM, Chang ZY (2012) Chaperone-dependent mechanisms for acid resistance in enteric bacteria. Trends Microbiol 20:328–335

    Article  CAS  PubMed  Google Scholar 

  • Horn AH, Sticht H (2015) Synthetic protein scaffolds based on peptide motifs and cognate adaptor domains for improving metabolic productivity. Front Bioeng Biotechnol 3:191. https://doi.org/10.3389/fbioe.2015.00191

    Article  PubMed  PubMed Central  Google Scholar 

  • Hua X, Cao R, Zhou X, Xu Y (2019) One-step continuous/semi-continuous whole-cell catalysis production of glycolic acid by a combining bioprocess with in-situ cell recycling and electrodialysis. Bioresour Technol 273:515–520. https://doi.org/10.1016/j.biortech.2018.11.061

    Article  CAS  PubMed  Google Scholar 

  • Iyer R, Iverson TM, Accardi A, Miller C (2002) A biological role for prokaryotic ClC chloride channels. Nature 419:715–718

    Article  CAS  PubMed  Google Scholar 

  • Iyer R, Williams C, Miller C (2003) Arginine-agmatine antiporter in extreme acid resistance in Escherichia coli. J Bacteriol 185:6556–6561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang WL, Gupta RK, Deshpande MC, Schwendeman SP (2005) Biodegradable poly(lactic-co-glycolic acid) microparticles for injectable delivery of vaccine antigens. Adv Drug Delivery Rev 57:391–410

    Article  CAS  Google Scholar 

  • Johnson MD, Bell J, Clarke K, Chandler R, Pathak P, Xia YD, Marshall RL, Weinstock GM, Loman NJ, Winn PJ, Lund PA (2014) Characterization of mutations in the PAS domain of the EvgS sensor kinase selected by laboratory evolution for acid resistance in Escherichia coli. Mol Microbiol 93:911–927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanjee U, Houry WA (2013) Mechanisms of acid resistance in Escherichia coli. Annu Rev Microbiol 67:65–81

    Article  CAS  PubMed  Google Scholar 

  • Katsube S, Ando T, Yoneyama H (2019) L-alanine exporter, AlaE, of Escherichia coli functions as a safety valve to enhance survival under feast conditions. Int J Mol Sci 20

  • Kern R, Malki A, Abdallah J, Tagourti J, Richarme G (2007) Escherichia coli HdeB is an acid stress chaperone. J Bacteriol 189:603–610

    Article  CAS  PubMed  Google Scholar 

  • Khalil MB, Hou WM, Zhou H, Elisma F, Swayne LA, Blanchard AP, Yao ZM, Bennett SAL, Figeys D (2010) Lipidomics era: accomplishments and challenges. Mass Spectrom Rev 29:877–929. https://doi.org/10.1002/mas.20294

    Article  CAS  Google Scholar 

  • Kim GB, Kim WJ, Kim HU, Lee SY (2020) Machine learning applications in systems metabolic engineering. Curr Opin Biotechnol 64:1–9

    Article  CAS  PubMed  Google Scholar 

  • Kim, K., Kim, S.K., Park, Y.C., and Seo, J.H. (2014). Enhanced production of 3-hydroxypropionic acid from glycerol by modulation of glycerol metabolism in recombinant Escherichia coli. Bioresour. Technol. 156: 170-175. https://doi.org/10.1016/j.biortech.2014.01.009

  • Kim YE, Hipp MS, Bracher A, Hayer-Hartl M, Hartl FU (2013) Molecular chaperone functions in protein folding and proteostasis. Annu Rev Biochem 82(82):323–355

    Article  CAS  PubMed  Google Scholar 

  • Kocer A (2015) Mechanisms of mechanosensing - mechanosensitive channels, function and re-engineering. Curr Opin Chem Biol 29:120–127

    Article  CAS  PubMed  Google Scholar 

  • Koebnik R, Locher KP, Van Gelder P (2000) Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37:239–253. https://doi.org/10.1046/j.1365-2958.2000.01983.x

    Article  CAS  PubMed  Google Scholar 

  • Kolesova O, Simonetti G, Donati L, Pasqua G, Valletta A, Chronopoulou L, Palocci C (2018) Poly Lactic-co-Glycolic Acid (PLGA) uptake by Candida albicans cells as biodegradable controlled drug delivery carrier. Med Mycol 56:S154–S154

    Google Scholar 

  • Kroll RG, Booth IR (1983) The relationship between intracellular pH, the pH gradient and potassium transport in Escherichia coli. Biochem J 216:709–716. https://doi.org/10.1042/bj2160709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar A, Thakur A, Panesar PS (2019) Lactic acid and its separation and purification techniques: a review. Rev Environ Sci Biotechnol 18:823–853

    Article  Google Scholar 

  • Kung C, Martinac B, Sukharev S (2010) Mechanosensitive channels in microbes. Annu Rev Microbiol 64:313–329. https://doi.org/10.1146/annurev.micro.112408.134106

    Article  CAS  PubMed  Google Scholar 

  • Kurgan G, Kurgan L, Schneider A, Onyeabor M, Rodriguez-Sanchez Y, Taylor E, Martinez R, Carbonell P, Shi X, Gu H, Wang X (2019) Identification of major malate export systems in an engineered malate-producing Escherichia coli aided by substrate similarity search. Appl Microbiol Biotechnol 103:9001–9011. https://doi.org/10.1007/s00253-019-10164-y

    Article  CAS  PubMed  Google Scholar 

  • Lee SJ, Song H, Lee SY (2006) Genome-based metabolic engineering of Mannheimia succiniciproducens for succinic acid production. Appl Environ Microbiol 72:1939–1948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SY, Mattanovich D, Villaverde A (2012) Systems metabolic engineering, industrial biotechnology and microbial cell factories. Microb Cell Fact 11

  • Li, N., Zhang, B., Wang, Z.W., Tang, Y.J., Chen, T., and Zhao, X.M. (2014). Engineering Escherichia coli for fumaric acid production from glycerol. Bioresour. Technol. 174: 81-87. https://doi.org/10.1016/j.biortech.2014.09.147

  • Lin JS, Smith MP, Chapin KC, Baik HS, Bennett GN, Foster JW (1996) Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Appl Environ Microbiol 62:3094–3100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin H, Bennett GN, San K-YJMe (2005) Metabolic engineering of aerobic succinate production systems in Escherichia coli to improve process productivity and achieve the maximum theoretical succinate yield. Metab Eng 7:116–127

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Gao W, Zhao X, Wang JH, Garza E, Manow R, Zhou SD (2014) Pilot scale demonstration of D-lactic acid fermentation facilitated by Ca(OH)(2) using a metabolically engineered Escherichia coli. Bioresour Technol 169:559–565. https://doi.org/10.1016/j.biortech.2014.06.056

  • Loffhagen N, Hartig C, Geyer W, Voyevoda M, Harms H (2007) Competition between cis, trans and cyclopropane fatty acid formation and its impact on membrane fluidity. Eng Life Sci 7:67–74. https://doi.org/10.1002/elsc.200620168

    Article  CAS  Google Scholar 

  • Lu PL, Ma D, Chen YL, Guo YY, Chen GQ, Deng HT, Shi YG (2013) L-glutamine provides acid resistance for Escherichia coli through enzymatic release of ammonia. Cell Res 23:635–644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makadia HK, Siegel SJ (2011) Poly lactic-co-glycolic acid (PLGA) as biodegradable controlled drug delivery carrier. Polymers 3:1377–1397

    Article  CAS  PubMed  Google Scholar 

  • Martinez FAC, Balciunas EM, Salgado JM, Gonzalez JMD, Converti A, Oliveira RPD (2013) Lactic acid properties, applications and production: a review. Trends Food Sci Technol 30:70–83

    Article  CAS  Google Scholar 

  • Masuda N, Church GM (2003) Regulatory network of acid resistance genes in Escherichia coli. Mol Microbiol 48:699–712

    Article  CAS  PubMed  Google Scholar 

  • Maurer LM, Yohannes E, Bondurant SS, Radmacher M, Slonczewski JLJJob (2005) pH regulates genes for flagellar motility, catabolism, and oxidative stress in Escherichia coli K-12. J Bacteriol 187:304–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng SY, Bennett GN (1992) Nucleotide-sequence of the Escherichia-Coli cad operon - a system for neutralization of low extracellular Ph. J Bacteriol 174:2659–2669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michnick SW, Remy I, Campbell-Valois F-X, Vallée-Bélisle A, Pelletier JN (2000) Detection of protein-protein interactions by protein fragment complementation strategies. In: Methods Enzymol. Academic Press, pp 208–230

  • Mikos AG, Bao Y, Cima LG, Ingber DE, Vacanti JP, Langer R (1993) Preparation of poly(glycolic acid) bonded fiber structures for cell attachment and transplantation. J Biomed Mater Res 27:183–189. https://doi.org/10.1002/jbm.820270207

    Article  CAS  PubMed  Google Scholar 

  • Miles EW, Rhee S, Davies DR (1999) The molecular basis of substrate channeling. J Biol Chem 274:12193–12196. https://doi.org/10.1074/jbc.274.18.12193

    Article  CAS  PubMed  Google Scholar 

  • Moss RA, Fujita T, Okumura Y, Hua Z, Mendelsohn R, Senak L (1992) Comparative dynamic stabilities of cyclopropyl and olefinic model lipids in liposomes - a coordinated kinetic and spectroscopic study. Langmuir 8:1731–1735. https://doi.org/10.1021/la00043a008

    Article  CAS  Google Scholar 

  • Niu, W., Draths, K.M., and Frost, J.W. (2002). Benzene-free synthesis of adipic acid. Biotechnol. Prog. 18: 201-211. https://doi.org/10.1021/bp010179x

  • Nguyen DTT, Praveen P, Loh KC (2018) Zymomonas mobilis immobilization in polymeric membranes for improved resistance to lignocellulose-derived inhibitors in bioethanol fermentation. Biochem Eng J 140:29–37. https://doi.org/10.1016/j.bej.2018.09.003

    Article  CAS  Google Scholar 

  • Okino S, Suda M, Fujikura K, Inui M, Yukawa H (2008) Production of D-lactic acid by Corynebacterium glutamicum under oxygen deprivation. Appl Microbiol Biotechnol 78:449–454

    Article  CAS  PubMed  Google Scholar 

  • Orth JD, Conrad TM, Na J, Lerman JA, Nam H, Feist AM, Palsson BO (2011) A comprehensive genome-scale reconstruction of Escherichia coli metabolism-2011. Mol Syst Biol 7

  • Palmerin-Carreno DM, Hernandez-Orihuela AL, Martinez-Antonio A (2019) Production of D-lactate from avocado seed hydrolysates by metabolically engineered Escherichia coli JU15. Fermentation-Basel 5:26. https://doi.org/10.3390/fermentation5010026

    Article  CAS  Google Scholar 

  • Park K, Lee BC, Lim HH (2019) Mutation of external glutamate residue reveals a new intermediate transport state and anion binding site in a CLC Cl-/H+ antiporter. Proc Natl Acad Sci U S A 116:17345–17354. https://doi.org/10.1073/pnas.1901822116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peabody GL, Winkler J, Kao KC (2014) Tools for developing tolerance to toxic chemicals in microbial systems and perspectives on moving the field forward and into the industrial setting. Curr Opin Chem Eng 6:9–17

    Article  Google Scholar 

  • Pelletier JN, Campbell-Valois FX, Michnick SW (1998) Oligomerization domain-directed reassembly of active dihydrofolate reductase from rationally designed fragments. Proc Natl Acad Sci U S A 95:12141–12146. https://doi.org/10.1073/pnas.95.21.12141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petri R, Schmidt-Dannert C (2004) Dealing with complexity: evolutionary engineering and genome shuffling. Curr Opin Biotechnol 15:298–304. https://doi.org/10.1016/j.copbio.2004.05.005

    Article  CAS  PubMed  Google Scholar 

  • Pham HL, Wong A, Chua N, Teo WS, Yew WS, Chang MW (2017) Engineering a riboswitch-based genetic platform for the self-directed evolution of acid-tolerant phenotypes. Nat Commun 8:411. https://doi.org/10.1038/s41467-017-00511-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poger D, Mark AE (2015) A ring to rule them all: the effect of cyclopropane fatty acids on the fluidity of lipid bilayers. J Phys Chem B 119:5487–5495. https://doi.org/10.1021/acs.jpcb.5b00958

    Article  CAS  PubMed  Google Scholar 

  • Rathnasingh, C., Raj, S.M., Jo, J.E., and Park, S. (2009). Development and Evaluation of Efficient Recombinant Escherichia coli Strains for the Production of 3-Hydroxypropionic Acid From Glycerol. Biotechnol. Bioeng. 104: 729-739. https://doi.org/10.1002/bit.22429

  • Ricke SC (2003) Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poult Sci 82:632–639

    Article  CAS  PubMed  Google Scholar 

  • Roe AJ, O’Byrne C, McLaggan D, Booth IR (2002) Inhibition of Escherichia coli growth by acetic acid: a problem with methionine biosynthesis and homocysteine toxicity. Microbiology 148:2215–2222

    Article  CAS  PubMed  Google Scholar 

  • Royce LA, Boggess E, Fu Y, Liu P, Shanks JV, Dickerson J, Jarboe LR (2014) Transcriptomic analysis of carboxylic acid challenge in Escherichia coli: beyond membrane damage. PLoS One 9:e89580. https://doi.org/10.1371/journal.pone.0089580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz N, Kahne D, Silhavy TJ (2006) Advances in understanding bacterial outer-membrane biogenesis. Nat Rev Microbiol 4:57–66. https://doi.org/10.1038/nrmicro1322

    Article  CAS  PubMed  Google Scholar 

  • Salusjarvi L, Toivari M, Vehkomaki ML, Koivistoinen O, Mojzita D, Niemela K, Penttila M, Ruohonen L (2017) Production of ethylene glycol or glycolic acid from D-xylose in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 101:8151–8163

    Article  CAS  PubMed  Google Scholar 

  • Salusjarvi L, Havukainen S, Koivistoinen O, Toivari M (2019) Biotechnological production of glycolic acid and ethylene glycol: current state and perspectives. Appl Microbiol Biotechnol 103:2525–2535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sangeetha VH, Valapa RB, Nayak SK, Varghese TO (2018) Investigation on the Influence of EVA Content on the Mechanical and Thermal Characteristics of Poly(lactic acid) Blends. J Polym Environ 26:1–14

    Article  CAS  Google Scholar 

  • Santoscoy MC, Jarboe LR (2019) Streamlined assessment of membrane permeability and its application to membrane engineering of Escherichia coli for octanoic acid tolerance. J Ind Microbiol Biotechnol 46:843–853

    Article  CAS  PubMed  Google Scholar 

  • Scheel O, Zdebik AA, Lourdel S, Jentsch TJ (2005) Voltage-dependent electrogenic chloride/proton exchange by endosomal CLC proteins. Nature 436:424–427. https://doi.org/10.1038/nature03860

    Article  CAS  PubMed  Google Scholar 

  • Schmitt C, Bafna JA, Schmid B, Klingl S, Baier S, Hemmis B, Wagner R, Winterhalter M, Voll LM (2019) Manipulation of charge distribution in the arginine and glutamate clusters of the OmpG pore alters sugar specificity and ion selectivity. Biochim Biophys Acta Biomembr 1861:183021. https://doi.org/10.1016/j.bbamem.2019.07.009

    Article  CAS  PubMed  Google Scholar 

  • Shi YH, Sun HY, Lu DM, Le QH, Chen DX, Zhou YC (2006) Separation of glycolic acid from glycolonitrile hydrolysate by reactive extraction with tri-n-octylamine. Sep Purif Technol 49:20–26

    Article  CAS  Google Scholar 

  • Song, C.W., and Lee, S.Y. (2015). Combining rational metabolic engineering and flux optimization strategies for efficient production of fumaric acid. Appl. Microbiol. Biotechnol. 99: 8455-8464. https://doi.org/10.1007/s00253-015-6816-6

  • Steiner P, Sauer U (2003) Overexpression of the ATP-dependent helicase RecG improves resistance to weak organic acids in Escherichia coli. Appl Microbiol Biotechnol 63:293–299

    Article  CAS  PubMed  Google Scholar 

  • Stiffler MA, Poelwijk FJ, Brock KP, Stein RR, Riesselman A, Teyra J, Sidhu SS, Marks DS, Gauthier NP, Sander C (2020) Protein structure from experimental evolution. Cell Syst 10:15-24 e15. https://doi.org/10.1016/j.cels.2019.11.008

    Article  CAS  PubMed  Google Scholar 

  • Suarez DC, Kilikian BV (2000) Acetic acid accumulation in aerobic growth of recombinant Escherichia coli. Process Biochem 35:1051–1055

    Article  CAS  Google Scholar 

  • Tran KNT, Eom GT, Hong SH (2019) Improving L-serine production in Escherichia coli via synthetic protein scaffold of SerB, SerC, and EamA. Biochem Eng J 148:138–142

    Article  CAS  Google Scholar 

  • Trchounian K, Pinske C, Sawers RG, Trchounian A (2011) Dependence on the F0F1-ATP synthase for the activities of the hydrogen-oxidizing hydrogenases 1 and 2 during glucose and glycerol fermentation at high and low pH in Escherichia coli. J Bioenerg Biomembr 43:645–650. https://doi.org/10.1007/s10863-011-9397-9

    Article  CAS  PubMed  Google Scholar 

  • Tsuge Y, Yamamoto S, Kato N, Suda M, Vertes AA, Yukawa H, Inui M (2015) Overexpression of the phosphofructokinase encoding gene is crucial for achieving high production of D-lactate in Corynebacterium glutamicum under oxygen deprivation. Appl Microbiol Biotechnol 99:4679–4689

    Article  CAS  PubMed  Google Scholar 

  • Utrilla J, Licona-Cassani C, Marcellin E, Gosset G, Nielsen LK, Martinez A (2012) Engineering and adaptive evolution of Escherichia coli for D-lactate fermentation reveals GatC as a xylose transporter. Metab Eng 14:469–476. https://doi.org/10.1016/j.ymben.2012.07.007

    Article  CAS  PubMed  Google Scholar 

  • Vemuri GN, Eiteman MA, Altman E (2002) Effects of growth mode and pyruvate carboxylase on succinic acid production by metabolically engineered strains of Escherichia coli. Appl Environ Microbiol 68:1715–1727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vitkin E, Solomon O, Sultan S, Yakhini Z (2018) Genome-wide analysis of fitness data and its application to improve metabolic models. BMC Bioinformatics 19

  • Wang AY, Cronan JE (1994) The growth phase-dependent synthesis of cyclopropane fatty-acids in Escherichia coli is the result of an Rpos(Katf)-dependent promoter plus enzyme instability. Mol Microbiol 11:1009–1017. https://doi.org/10.1111/j.1365-2958.1994.tb00379.x

    Article  PubMed  Google Scholar 

  • Wang LM, Zhao B, Li FS, Xu K, Ma CQ, Tao F, Li QG, Xu P (2011) Highly efficient production of D-lactate by Sporolactobacillus sp. CASD with simultaneous enzymatic hydrolysis of peanut meal. Appl Microbiol Biotechnol 89:1009–1017. https://doi.org/10.1007/s00253-010-2904-9

    Article  CAS  PubMed  Google Scholar 

  • Warnecke T, Gill RT (2005) Organic acid toxicity, tolerance, and production in Escherichia coli biorefining applications. Microb Cell Fact 4:25. https://doi.org/10.1186/1475-2859-4-25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wasewar KL (2005) Separation of lactic acid: Recent advances. Chem Biochem Eng Q 19:159–172

    CAS  Google Scholar 

  • Wolff S, Weissman JS, Dillin AJC (2014) Differential scales of protein quality control. Cell 157:52–64

    Article  CAS  PubMed  Google Scholar 

  • Wu MK, Li XZ, Guo SF, Lemma WD, Zhang WM, Ma JF, Jia HH, Wu H, Jiang M, Ouyang PK (2017) Enhanced succinic acid production under acidic conditions by introduction of glutamate decarboxylase system in E. coli AFP111. Bioprocess Biosyst Eng 40:549–557. https://doi.org/10.1007/s00449-016-1720-8

    Article  CAS  PubMed  Google Scholar 

  • Xu Y, Zhao Z, Tong WH, Ding YM, Liu B, Shi YX, Wang JC, Sun SM, Liu M, Wang YH, Qi QS, Xian M, Zhao G (2020) An acid-tolerance response system protecting exponentially growing Escherichia coli. Nat Commun 11:1496. https://doi.org/10.1038/s41467-020-15350-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang S-T, El-Ensashy H, Thongchul N (2013) Bioprocessing technologies in biorefinery for sustainable production of fuels, chemicals, and polymers. John Wiley & Sons

  • Young EM, Zhao Z, Gielesen BEM, Wu L, Gordon DB, Roubos JA, Voigt CA (2018) Iterative algorithm-guided design of massive strain libraries, applied to itaconic acid production in yeast. Metab Eng 48:33–43

    Article  CAS  PubMed  Google Scholar 

  • Yu, Deng Ning, Ma Kangjia, Zhu Yin, Mao Xuetuan, Wei Yunying, Zhao (2018) Balancing the carbon flux distributions between the TCA cycle and glyoxylate shunt to produce glycolate at high yield and titer in Escherichia coli. Metab Eng 46: 28-34. https://doi.org/10.1016/j.ymben.2018.02.008

  • Yu X-C, Yang C, Ding J, Niu X, Hu Y, Jin CJB (2017) Characterizations of the interactions between Escherichia coli periplasmic chaperone HdeA and its native substrates during acid stress. Biochemistry 56:5748–5757

    Article  CAS  PubMed  Google Scholar 

  • Yung TW, Jonnalagadda S, Balagurunathan B, Zhao H (2016) Transcriptomic analysis of 3-hydroxypropanoic acid stress in Escherichia coli. Appl Biochem Biotechnol 178:527–543

    Article  CAS  PubMed  Google Scholar 

  • Zahoor A, Otten A, Wendisch VF (2014) Metabolic engineering of Corynebacterium glutamicum for glycolate production. J Biotechnol 192:366–375

    Article  CAS  PubMed  Google Scholar 

  • Zeikus JG, Jain MK, Elankovan P (1999) Biotechnology of succinic acid production and markets for derived industrial products. Appl Microbiol Biotechnol 51:545–552

    Article  CAS  Google Scholar 

  • Zhang XL, Jantama K, Moore JC, Jarboe LR, Shanmugam KT, Ingram LO (2009) Metabolic evolution of energy-conserving pathways for succinate production in Escherichia coli. Proc Natl Acad Sci U S A 106:20180–20185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang S, Cheng Y, Ma J, Wang Y, Chang Z, Fu X (2019) Degp degrades a wide range of substrate proteins in Escherichia coli under stress conditions. Biochem J 476:3549–3564. https://doi.org/10.1042/BCJ20190446

    Article  CAS  PubMed  Google Scholar 

  • Zhao, M., Huang, D., Zhang, X., Koffas, M.A., Zhou, J., and Deng, Y. (2018). Metabolic engineering of Escherichia coli for producing adipic acid through the reverse adipate-degradation pathway. Metab. Eng. 47: 254-262. https://doi.org/10.1016/j.ymben.2018.04.002

  • Zhu ZM, Ji XM, Wu ZM, Zhang J, Du GC (2018a) Improved acid-stress tolerance of Lactococcus lactis NZ9000 and Escherichia coli BL21 by overexpression of the anti-acid component recT. J Ind Microbiol Biotechnol 45:1091–1101

    Article  CAS  PubMed  Google Scholar 

  • Zhu ZM, Zhang J, Ji XM, Fang Z, Wu ZM, Chen J, Du GC (2018b) Evolutionary engineering of industrial microorganisms-strategies and applications. Appl Microbiol Biotechnol 102:4615–4627

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by the National First-class Discipline Program of Light Industry Technology and Engineering under Grant (LITE2018-08) and Independent research project of State Key Laboratory of Food Science and Technology (SKLF-ZZB-202015).

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Authors and Affiliations

  1. Engineering Research Center of Ministry of Education on Food Synthetic Biotechnology, Jiangnan University, 1800 Lihu Road, Wuxi, 214122, China

    Jinhua Yang, Juan Zhang & Guocheng Du

  2. Science Center for Future Foods, Jiangnan University, 1800 Lihu Road, Wuxi, 214122, China

    Jinhua Yang, Juan Zhang & Guocheng Du

  3. The Key Laboratory of Industrial Biotechnology, Ministry of Education, School of Biotechnology, Jiangnan University, Wuxi, 214122, China

    Jinhua Yang, Juan Zhang & Guocheng Du

  4. College of Food Science and Light Industry, Nanjing Tech University, Nanjing, 211800, China

    Zhengming Zhu

  5. Jiangsu Province Engineering Research Center of Food Synthetic Biotechnology, Jiangnan University, 1800 Lihu Road, Wuxi, 214122, China

    Jinhua Yang, Juan Zhang & Guocheng Du

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  1. Jinhua Yang
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  2. Juan Zhang
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  3. Zhengming Zhu
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  4. Guocheng Du
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JY, ZZ and JZ conceived and designed the review. JY wrote the manuscript. JZ and GD contributed to the revision of the manuscript draft. All authors read and approved the final manuscript.

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Yang, J., Zhang, J., Zhu, Z. et al. The challenges and prospects of Escherichia coli as an organic acid production host under acid stress. Appl Microbiol Biotechnol 105, 8091–8107 (2021). https://doi.org/10.1007/s00253-021-11577-4

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