Skip to main content

Advertisement

SpringerLink
Log in

New technologies provide more metabolic engineering strategies for bioethanol production in Zymomonas mobilis

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Bioethanol has been considered as a potentially renewable energy source, and metabolic engineering plays an important role in the production of biofuels. As an efficient ethanol-producing bacterium, Zymomonas mobilis has garnered special attention due to its high sugar uptake, ethanol yield, and tolerance. Different metabolic engineering strategies have been used to establish new metabolic pathways for Z. mobilis to broaden its substrate range, remove competing pathways, and enhance its tolerance to ethanol and lignocellulosic hydrolysate inhibitors. Recent advances in omics technology, computational modeling and simulation, system biology, and synthetic biology contribute to the efficient re-design and manipulation of microbes via metabolic engineering at the whole-cell level. In this review, we summarize the progress of some new technologies used for metabolic engineering to improve bioethanol production and tolerance in Z. mobilis. Some successful examples of metabolic engineering used to develop strains for ethanol production are described in detail. Lastly, some important strategies for future metabolic engineering efforts are also highlighted.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Agrawal M, Chen RR (2011) Discovery and characterization of a xylose reductase from Zymomonas mobilis ZM4. Biotechnol Lett 33(11):2127–2133

    Article  CAS  PubMed  Google Scholar 

  • Agrawal M, Mao Z, Chen RR (2011) Adaptation yields a highly efficient xylose-fermenting Zymomonas mobilis strain. Biotechnol Bioeng 108(4):777–785

    Article  CAS  PubMed  Google Scholar 

  • Agrawal M, Wang Y, Chen RR (2012) Engineering efficient xylose metabolism into an acetic acid-tolerant Zymomonas mobilis strain by introducing adaptation-induced mutations. Biotechnol Lett 34(10):1825–1832

    Article  PubMed  Google Scholar 

  • Alper H, Fischer C, Nevoigt E, Stephanopoulos G, Langer R (2005a) Tuning genetic control through promoter engineering. Proc Natl Acad Sci USA 102(36):12678–12683

  • Alper H, Jin YS, Moxley JF, Stephanopoulos G (2005b) Identifying gene targets for the metabolic engineering of lycopene biosynthesis in Escherichia coli. Metab Eng 7(3):155–164

    Article  CAS  PubMed  Google Scholar 

  • Altintas MM, Eddy CK, Zhang M, McMillan JD, Kompala DS (2006) Kinetic modeling to optimize pentose fermentation in Zymomonas mobilis. Biotechnol Bioeng 94(2):273–295

    Article  CAS  PubMed  Google Scholar 

  • Bochner B, Gomez V, Ziman M, Yang S, Brown SD (2010) Phenotype microarray profiling of Zymomonas mobilis ZM4. Appl Biochem Biotechnol 161(1–8):116–123

    Article  CAS  PubMed  Google Scholar 

  • Brestic-Goachet N, Gunasekaran P, Cami B, Baratti JC (1989) Transfer and expression of an erwinia chrysanthemi cellulase gene in Zymomonas mobilis. J Gen Microbiol 135(4):893–902

    CAS  Google Scholar 

  • Brestic-Goachet N, Gunasekaran P, Cami B, Baratti JC (1990) Transfer and expression of a Bacillus licheniformis α-amylase gene in Zymomonas mobilis. Arch Microbiol 153(3):219–225

    Article  CAS  Google Scholar 

  • Bro C, Regenberg B, Förster J, Nielsen J (2006) In silico aided metabolic engineering of Saccharomyces cerevisiae for improved bioethanol production. Metab Eng 8(2):102–111

  • Cao QH, Li T, Shao HH, Tan XM, Zhang YZ (2016) Three new shuttle vectors for heterologous expression in Zymomonas mobilis. J Biotechnol 19:33–40

    CAS  Google Scholar 

  • Cao QH, Shao HH, Qiu H, Li T, Zhang YZ, Tan XM (2017a) Using the CRISPR/Cas9 system to eliminate native plasmids of Zymomonas mobilis ZM4. Biosci Biotechnol Biochem 81(3):453–459

    Article  CAS  PubMed  Google Scholar 

  • Cao S, Zhou X, Jin W, Wang F, Tu R, Han S, Chen H, Chen C, Xie GJ, Ma F (2017b) Improving of lipid productivity of the oleaginous microalgae Chlorella pyrenoidosa via atmospheric and room temperature plasma (ARTP). Bioresour Technol 244:1400–1406

    Article  CAS  PubMed  Google Scholar 

  • Charoensuk K, Sakurada T, Tokiyama A, Murata M, Kosaka T, Thanonkeo P, Yamada M (2017) Thermotolerant genes essential for survival at a critical high temperature in thermotolerant ethanologenic Zymomonas mobilis TISTR 548. Biotechnol Biofuels 10(1):204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho SH, Lei R, Henninger TD, Contreras LM (2014) Discovery of ethanol-responsive small RNAs in Zymomonas mobilis. Appl Environ Microbiol 80(14):4189–4198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho SH, Haning K, Shen W, Blome C, Li RX, Yang SH, Contreras LM (2017) Identification and characterization of 5' untranslated regions (5' UTRs) in Zymomonas mobilis as regulatory biological parts. Front Microbiol 8:2432

  • Clift D, Mcewan WA, Labzin LI, Konieczny V, Mogessie B, James LC, Schuh M (2017) A method for the acute and rapid degradation of endogenous proteins. Cell 171(7):1692–1706.e18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deanda K, Zhang M, Eddy C, Picataggio S (1996) Development of an arabinose-fermenting Zymomonas mobilis strain by metabolic pathway engineering. Appl Environ Microbiol 62(12):4465–4470

    CAS  PubMed  PubMed Central  Google Scholar 

  • Degreif D, Rond TD, Bertl A, Keasling JD, Budin I (2017) Lipid engineering reveals regulatory roles for membrane fluidity in yeast flocculation and oxygen-limited growth. Metab Eng 41:46–56

    Article  CAS  PubMed  Google Scholar 

  • Dong HW, Bao J, Ryu DD, Zhong JJ (2011) Design and construction of improved new vectors for Zymomonas mobilis recombinants. Biotechnol Bioeng 108(7):1616–1627

    Article  CAS  PubMed  Google Scholar 

  • Douka E, Christogianni A, Koukkou AI, Afendra AS, Drainas C (2001) Use of a green fluorescent protein gene as a reporter in Zymomonas mobilis and Halomonas elongata. FEMS Microbiol Lett 201(2):221–227

    Article  CAS  PubMed  Google Scholar 

  • Drainas C, Vartholomatos G, Panopoulos NJ (1995) The ice nucleation gene from pseudomonas syringae as a sensitive gene reporter for promoter analysis in Zymomonas mobilis. Appl Environ Microbiol 61(1):273–277

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dunn KL, Rao CV (2014) Expression of a xylose-specific transporter improves ethanol production by metabolically engineered Zymomonas mobilis. Appl Microbiol Biotechnol 98(15):6897–6905

    Article  CAS  PubMed  Google Scholar 

  • Farwick A, Bruder S, Schadeweg V, Oreb M, Boles E (2014) Engineering of yeast hexose transporters to transport D-xylose without inhibition by D-glucose. Proc Natl Acad Sci USA 111(14):5159–5164

  • Fischer CR, Klein-Marcuschamer D, Stephanopoulos G (2008) Selection and optimization of microbial hosts for biofuels production. Metab Eng 10(6):295–304

    Article  CAS  PubMed  Google Scholar 

  • Franden MA, Pilath HM, Mohagheghi A, Pienkos PT, Zhang M (2013) Inhibition of growth of Zymomonas mobilis by model compounds found in lignocellulosic hydrolysates. Biotechnol Biofuels 6:99

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaida SM, Alhinai 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(18):8726–8737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galazka JM, Tian C, Beeson WT, Martinez B, Glass NL, Cate JH (2010) Cellodextrin transport in yeast for improved biofuel production. Science 330(6000):84–86

    Article  CAS  PubMed  Google Scholar 

  • Gao Q, Zhang M, McMillan JD, Kompala DS (2002) Characterization of heterologous and native enzyme activity profiles in metabolically engineered Zymomonas mobilis strains during batch fermentation of glucose and xylose mixtures. Appl Biochem Biotechnol 98-100:341–355

    Article  CAS  PubMed  Google Scholar 

  • Gliessman JR, Kremer TA, Sangani AA, Jones-Burrage SE, McKinlay JB (2017) Pantothenate auxotrophy in Zymomonas mobilis ZM4 is due to a lack of aspartate decarboxylase activity. FEMS Microbiol Lett 364(13)

  • Goodarzi H, Bennett BD, Amini S, Reaves ML, Hottes AK, Rabinowitz JD, Tavazoie S (2010) Regulatory and metabolic rewiring during laboratory evolution of ethanol tolerance in E. coli. Mol Syst Biol 6:378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ha SJ, Wei Q, Kim SR, Galazka JM, Cate JH, Jin YS (2015) Cofermentation of cellobiose and galactose by an engineered Saccharomyces cerevisiae strain. Appl Environ Microbiol 77(16):5822–5825

    Article  CAS  Google Scholar 

  • Hanly TJ, Urello M, Henson MA (2012) Dynamic flux balance modeling of S. cerevisiae and E. coli co-cultures for efficient consumption of glucose/xylose mixtures. Appl Microbiol Biotechnol 93(6):2529–2541

    Article  CAS  PubMed  Google Scholar 

  • Haripriya R, Vasan TP (2015) Harbouring of bacterial cellulase gene into Zymomonas mobilis for cellulosic ethanol production. European J Biotechnol Biosci 3(3):24–30

    Google Scholar 

  • Hayashi T, Kato T, Furukawa K (2012) Respiratory chain analysis of Zymomonas mobilis mutants producing high levels of ethanol. Appl Environ Microbiol 78(16):5622–5629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashi T, Kato T, Watakabe S, Song W, Aikawa S, Furukawa K (2015) The respiratory chain provides salt stress tolerance by maintaining a low NADH/NAD+ ratio in Zymomonas mobilis. Microbiology 161(12):2384–2394

    Article  CAS  PubMed  Google Scholar 

  • He MX, Wu B, Shui ZX, Hu QC, Wang WG, Tan FR, Tang XY, Zhu QL, Pan K, Li Q, Su XH (2012a) Transcriptome profiling of Zymomonas mobilis under ethanol stress. Biotechnol Biofuels 5(1):75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He MX, Wu B, Shui ZX, Hu QC, Wang WG, Tan FR, Tang XY, Zhu QL, Pan K, Li Q, Su XH (2012b) Transcriptome profiling of Zymomonas mobilis under furfural stress. Appl Microbiol Biotechnol 95(1):189–199

    Article  CAS  PubMed  Google Scholar 

  • He MX, Wu B, Qin H, Ruan ZY, Tan FR, Wang JL, Shui ZX, Dai LC, Zhu QL, Pan K, Tang XY, Wang WG, Hu QC (2014) Zymomonas mobilis: a novel platform for future biorefineries. Biotechnol Biofuels 7(1):101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeon YJ, Svenson CJ, Rogers PL (2005) Over-expression of xylulokinase in a xylose-metabolising recombinant strain of Zymomonas mobilis. FEMS Microbiol Lett 244(1):85–92

    Article  CAS  PubMed  Google Scholar 

  • Joachimstahl E, Jh HKJ, Rogers PL (1998) A mutant of Zymomonas mobilis ZM4 capable of ethanol production from glucose in the presence of high acetate concentrations. Biotechnol Lett 20(2):137–142

    Article  Google Scholar 

  • Jones CM, Hernández Lozada NJ, Pfleger BF (2015) Efflux systems in bacteria and their metabolic engineering applications. Appl Microbiol Biotechnol 99(22):9381–9393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim IS, Barrow KD, Rogers PL (2000) Nuclear magnetic resonance studies of acetic acid inhibition of rec Zymomonas mobilis ZM4(pZB5). Appl Biochem Biotechnol 84-86(1–9):357–370

    Article  CAS  PubMed  Google Scholar 

  • Kremer TA, LaSarre B, Posto AL, McKinlay JB (2015) N2 gas is an effective fertilizer for bioethanol production by Zymomonas mobilis. Proc Natl Acad Sci USA 112(7):2222–2226

  • Lee JH, Skotnicki ML, Rogers PL (1982) Kinetic studies on a flocculent strain of Zymomonas mobilis. Biotechnol Lett 4(9):615–620

    Article  CAS  Google Scholar 

  • Lee SY, Kim HU, Park JH, Park JM, Kim TY (2009) Metabolic engineering of microorganisms: general strategies and drug production. Drug Discov Today 14(1–2):78–88

    Article  CAS  PubMed  Google Scholar 

  • Lee KY, Park JM, Kim TY, Yun H, Lee SY (2010) The genome-scale metabolic network analysis of Zymomonas mobilis ZM4 explains physiological features and suggests ethanol and succinic acid production strategies. Microb Cell Fact 9:94

  • Leksawasdi N, Joachimsthal EL, Rogers PL (2001) Mathematical modelling of ethanol production from glucose/xylose mixtures by recombinant Zymomonas mobilis. Biotechnol Lett 23(13):1087–1093

    Article  CAS  Google Scholar 

  • Linger JG, Adney WS, Darzins A (2010) Heterologous expression and extracellular secretion of cellulolytic enzymes by Zymomonas mobilis. Appl Environ Microbiol 76(19):6360–6369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu YF, Hsieh CW, Chang YS, Wung BS (2017) Effect of acetic acid on ethanol production by Zymomonas mobilis mutant strains through continuous adaptation. BMC Biotechnol 17:63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu R, Liang L, Garst AD, Choudhury A, VSI N, Beckham GT, Gill RT (2018) Directed combinatorial mutagenesis of Escherichia coli for complex phenotype engineering. Metab Eng 47:10–20

    Article  CAS  PubMed  Google Scholar 

  • Luo Z, Bao J (2015) Secretive expression of heterologous β-glucosidase in Zymomonas mobilis. Bioresour Bioprocess 2:29

  • Ma YY, Dong HN, Zou SL, Hong JF, Zhang MH (2012) Comparison of glucose/xylose co-fermentation by recombinant Zymomonas mobilis under different genetic and environmental conditions. Biotechnol Lett 34(7):1297–1304

    Article  CAS  PubMed  Google Scholar 

  • Ma F, Chung MT, Yao Y, Nidetz R, Lee LM, Liu AP, Feng Y, Kurabayashi K, Yang GY (2018) Efficient molecular evolution to generate enantioselective enzymes using a dual-channel microfluidic droplet screening platform. Nat Commun 9(1):1030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Misawa N, Okamoto T, Nakamura K (1988) Expression of a cellulase gene in Zymomonas mobilis. J Biotechnol 7(3):167–177

    Article  CAS  Google Scholar 

  • Mohagheghi A, Evans K, Chou YC, Zhang M (2002) Cofermentation of glucose, xylose, and arabinose by genomic DNA-integrated xylose/arabinose fermenting strain of Zymomonas mobilis AX101. Appl Biochem Biotechnol 98:885–898

  • Mohagheghi A, Linger J, Smith H, Yang S, Dowe N, Pienkos PT (2014) Improving xylose utilization by recombinant Zymomonas mobilis strain 8b through adaptation using 2-deoxyglucose. Biotechnol Biofuels 7(1):19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohagheghi A, Linger JG, Yang SH, Smith H, Dowe N, Zhang M, Pienkos PT (2015) Improving a recombinant Zymomonas mobilis strain 8b through continuous adaptation on dilute acid pretreated corn stover hydrolysate. Biotechnol Biofuels 8(1):55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ng CY, Farasat I, Maranas CD, Salis HM (2015) Rational design of a synthetic Entner–Doudoroff pathway for improved and controllable NADPH regeneration. Metab Eng 29:86–96

    Article  CAS  PubMed  Google Scholar 

  • Nicolaou SA, Gaida SM, Papoutsakis ET (2010) A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: from biofuels and chemicals, to biocatalysis and bioremediation. Metab Eng 12(4):307–331

    Article  CAS  PubMed  Google Scholar 

  • Okamoto T, Yamano S, Ikeaga H, Nakamura K (1994) Cloning of the Acetobacter xylinum cellulase gene and its expression in Escherichia coli and Zymomonas mobilis. Appl Microbiol Biotechnol 42(4):563–568

    Article  CAS  PubMed  Google Scholar 

  • Panesar PS, Marwaha SS, Kennedy JF (2006) Zymomonas mobilis: an alternative ethanol producer. J Chem Technol Biotechnol 81(4):623–635

    Article  CAS  Google Scholar 

  • Parisutham V, Kim TH, Lee SK (2014) Feasibilities of consolidated bioprocessing microbes: from pretreatment to biofuel production. Bioresour Technol 161(3):431–440

    Article  CAS  PubMed  Google Scholar 

  • Park JH, Lee KH, Kim TY, Lee SY (2007) Metabolic engineering of Escherichia coli for the production of L-valine based on transcriptome analysis and in silico gene knockout simulation. Proc Natl Acad Sci USA 104(19):7797–7802

  • Pentjuss A, Odzina I, Kostromins A, Fell DA, Stalidzans E, Kalnenieks U (2013) Biotechnological potential of respiring Zymomonas mobilis: a stoichiometric analysis of its central metabolism. J Biotechnol 165(1):1–10

    Article  CAS  PubMed  Google Scholar 

  • Pfleger BF, Pitera DJ, Smolke CD, Keasling JD (2006) Combinatorial engineering of intergenic regions in operons tunes expression of multiple genes. Nat Biotechnol 24(8):1027–1032

    Article  CAS  PubMed  Google Scholar 

  • Pratish G, Patrick H, Andrew E, Martin VJJ, Radhakrishnan M (2013) Novel approach to engineer strains for simultaneous sugar utilization. Metab Eng 20(5):63–72

    Google Scholar 

  • Reyes LH, Winkler J, Kao KC (2012) Visualizing evolution in real-time method for strain engineering. Front Microbiol 3(3):198

    PubMed  PubMed Central  Google Scholar 

  • Rogers PL, Jeon YJ, Lee KJ, Lawford HG (2007) Zymomonas mobilis for fuel ethanol and higher value products. Adv Biochem Engin/Biotechnol 108:263–288

    Article  CAS  Google Scholar 

  • Rutkis R, Kalnenieks U, Stalidzans E, Fell DA (2013) Kinetic modelling of the Zymomonas mobilis Entner-Doudoroff pathway: insights into control and functionality. Microbiology 159(12):2674–2689

  • Samappito J, Yamada M, Klanrit P, Thanonkeo P (2018) Characterization of a thermo-adapted strain of Zymomonas mobilis for ethanol production at high temperature. 3 Biotech 8(11):474

    Article  PubMed  Google Scholar 

  • Seo JS, Chong H, Park HS, Yoon KO, Jung C, Kim JJ, Hong JH, Kim H, Kim JH, Kil JI, Park CJ, Oh HM, Lee JS, Jin SJ, Um HW, Lee HJ, Oh SJ, Kim JY, Kang HL, Lee SY, Lee KJ, Kang HS (2005) The genome sequence of the ethanologenic bacterium Zymomonas mobilis ZM4. Nat Biotechnol 23(1):63–68

    Article  CAS  PubMed  Google Scholar 

  • Seo JS, Chong HY, Kim JH, Kim JY (2007) Method for mass production of primary metabolites, strain for mass production of primary metabolites, and method for preparation thereof https://wwwsurechemblorg/document/WO-2007094646-A1 Accessed 23 Aug 2007

  • Shui ZX, Qin H, Wu B, Ruan ZY, Wang LS, Tan FR, Wang JL, Tang XY, Dai LC, Hu GQ, He MX (2015) Adaptive laboratory evolution of ethanologenic Zymomonas mobilis strain tolerant to furfural and acetic acid inhibitors. Appl Microbiol Biotechnol 99(13):5739–5748

    Article  CAS  PubMed  Google Scholar 

  • Skotnicki ML, Warr RG, Goodman AE, Lee KJ, Rogers PL (1983) High productivity ethanol fermentation using Zymomonas mobilis. Biochem Soc Symp 48:53–86

    CAS  PubMed  Google Scholar 

  • Sootsuwan K, Thanonkeo P, Keeratirakha N, Thanonkeo S, Jaisil P, Yamada M (2013) Sorbitol required for cell growth and ethanol production by Zymomonas mobilis under heat, ethanol, and osmotic stresses. Biotechnol Biofuels 6(1):180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strazdina I, Balodite E, Lasa Z, Rutkis R, Galinina N, Kalnenieks U (2018) Aerobic catabolism and respiratory lactate bypass in Ndh-negative Zymomonas mobilis. Metab Eng Commun 7:e00081

    Article  PubMed  PubMed Central  Google Scholar 

  • Su P, Delaney SF, Rogers PL (1989) Cloning and expression of a β-glucosidase gene from Xanthomonas albilineans in Escherichia coli and Zymomonas mobilis. J Biotechnol 9(2):139–152

    Article  CAS  Google Scholar 

  • Swings J, De Ley J (1977) The biology of Zymomonas. Bacteriol Rev 41(1):1–46

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tan FR, Dai LC, Wu B, Qin H, Shui ZX, Wang JL, Zhu QL, Hu QC, Ruan ZY, He MX (2015) Improving furfural tolerance of Zymomonas mobilis by rewiring a sigma factor RpoD protein. Appl Microbiol Biotechnol 99(12):5363–5371

    Article  CAS  PubMed  Google Scholar 

  • Tan FR, Wu B, Dai LC, Qin H, Shui ZX, Wang JL, Zhu QL, Hu GQ, He MX (2016) Using global transcription machinery engineering (gTME) to improve ethanol tolerance of Zymomonas mobilis. Microb Cell Factories 15(1):4

    Article  CAS  Google Scholar 

  • Todhanakasem T, Yodsanga S, Sowatad A, Kanokratana P, Thanonkeo P, Champreda V (2018) Inhibition analysis of inhibitors derived from lignocellulose pretreatment on the metabolic activity of Zymomonas mobilis biofilm and planktonic cells and the proteomic responses. Biotechnol Bioeng 115(1):70–81

    Article  CAS  PubMed  Google Scholar 

  • Tsantili IC, Karim MN, Klapa MI (2007) Quantifying the metabolic capabilities of engineered Zymomonas mobilis using linear programming analysis. Microb Cell Fact 6:8

  • Vasan PT, Sobana Piriya P, Immanual Gilwax Prabhu D, John Vennison S (2011) Cellulosic ethanol production by Zymomonas mobilis harboring an endoglucanase gene from Enterobacter cloacae. Bioresour Technol 102(3):2585–2589

    Article  CAS  PubMed  Google Scholar 

  • Venkatesh S (2015) Cloning and expression of cellulase genes from trichoderma reesei into Zymomonas mobilis for cellulosic ethanol production. Ph.D. Dissertation, Anna University

  • Wang GJ, Wang ZS, Zhang YW, Zhang YZ (2012) Cloning and expression of amyE gene from Bacillus subtilis in Zymomonas mobilis and direct production of ethanol from soluble starch. Biotechnol Bioprocess Eng 17(4):780–786

    Article  CAS  Google Scholar 

  • Wang C, Liu C, Hong J, Zhang K, Ma Y, Zou S, Zhang M (2013) Unmarked insertional inactivation in the gfo gene improves growth and ethanol production by Zymomonas mobilis ZM4 in sucrose without formation of sorbitol as a by-product, but yields opposite effects in high glucose. Biochem Eng J 72(0):61–69

    Article  CAS  Google Scholar 

  • Wang JL, Wu B, Qin H, You Y, Liu S, Shui ZX, Tan FR, Wang YW, Zhu QL, Li YB, Ruan ZY, Ma KD, Dai LC, Hu GQ, He MX (2016) Engineered Zymomonas mobilis for salt tolerance using EZ-Tn5-based transposon insertion mutagenesis system. Microb Cell Fact 15(1):101

  • Wang X, Gao Q, Bao J (2017) Enhancement of furan aldehydes conversion in Zymomonas mobilis by elevating dehydrogenase activity and cofactor regeneration. Biotechnol Biofuels 10(1):24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, He Q, Yang Y, Wang J, Haning K, Hu Y, Wu B, He M, Zhang Y, Bao J, Contreras LM, Yang SH (2018) Advances and prospects in metabolic engineering of Zymomonas mobilis. Metab Eng 50:57–73

  • Weir PM, Chase T (1995) Effect of proteolipid on Zymomonas fermentation of 25% glucose media. J Ind Microbiol 15(5):442–445

    Article  CAS  Google Scholar 

  • Weisser P, Kramer R, Sprenger GA (1996) Expression of the Escherichia coli pmi gene, encoding phosphomannose-isomerase in Zymomonas mobilis, leads to utilization of mannose as a novel growth substrate, which can be used as a selective marker. Appl Environ Microbiol 62:4155–4161

    CAS  PubMed  PubMed Central  Google Scholar 

  • Widiastuti H, Kim JY, Selvarasu S, Karimi IA, Kim H, Seo JS, Lee DY (2011) Genome-scale modeling and in silico analysis of ethanologenic bacteria Zymomonas mobilis. Biotechnol Bioeng 108(3):655–665

  • Wu B, He MX, Feng H, Shui ZX, Tang XY, Hu QC, Zhang YZ (2014) Construction of a novel secretion expression system guided by native signal peptide of PhoD in Zymomonas mobilis. Biosci Biotechnol Biochem 78(4):708–713

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Yang Y, Ren C, Yang C, Yang S, Gu Y, Jiang W (2015) Molecular modulation of pleiotropic regulator CcpA for glucose and xylose coutilization by solvent-producing Clostridium acetobutylicum. Metab Eng 28:169–179

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Li T, Cao QH, Li XD, Zhang YZ, Tan XM (2017) RecET recombination system driving chromosomal target gene replacement in Zymomonas mobilis. J Biotechnol 30:118–124

    CAS  Google Scholar 

  • Yanase H, Kotani T, Yasuda M, Matsuzawa A, Tonomura K (1991) Metabolism of galactose in Zymomonas mobilis. Appl Microbiol Biotechnol 35:364–368

    Article  CAS  PubMed  Google Scholar 

  • Yanase H, Nozaki K, Okamoto K (2005) Ethanol production from cellulosic materials by genetically engineered Zymomonas mobilis. Biotechnol Lett 27(4):259–263

    Article  CAS  PubMed  Google Scholar 

  • Yang SH, Pappas KM, Hauser LJ, Land ML, Chen GL, Hurst GB, Pan CL, Kouvelis VN, Typas MA, Pelletier DA, Klingeman DM, Chang YJ, Samatova NF, Brown SD (2009a) Improved genome annotation for Zymomonas mobilis. Nat Biotechnol 27(10):893–894

    Article  CAS  PubMed  Google Scholar 

  • Yang SH, Tschaplinski TJ, Engle NL, Carroll SL, Martin SL, Davison BH, Palumbo AV, Rodriguez M, Brown SD (2009b) Transcriptomic and metabolomic profiling of Zymomonas mobilis during aerobic and anaerobic fermentations. BMC Genomics 10:34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SH, Land ML, Klingeman DM, Pelletier DA, Lu T-YS, Martin SL, Guo H-B, Smith JC, Brown SD (2010a) Paradigm for industrial strain improvement identifies sodium acetate tolerance loci in Zymomonas mobilis and Saccharomyces cerevisiae. Proc Natl Acad Sci USA 107(23):10395–10400

  • Yang SH, Pelletier DA, Lu TYS, Brown SD (2010b) The Zymomonas mobilis regulator hfq contributes to tolerance against multiple lignocellulosic pretreatment inhibitors. BMC Microbiol 10:135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SH, Pan CL, Tschaplinski TJ, Hurst GB, Engle NL, Zhou W, Dam P, Xu Y, Rodriguez M, Dice L, Johnson CM, Davison BH, Brown SD (2013) Systems biology analysis of Zymomonas mobilis ZM4 ethanol stress responses. PLoS One 8(7):e68886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SH, Pan C, Hurst GB, Dice L, Davison BH, Brown SD (2014a) Elucidation of Zymomonas mobilis physiology and stress responses by quantitative proteomics and transcriptomics. Front Microbiol 5(3):246

    PubMed  PubMed Central  Google Scholar 

  • Yang SH, Franden MA, Brown SD, Chou YC, Pienkos PT, Zhang M (2014b) Insights into acetate toxicity in Zymomonas mobilis 8b using different substrates. Biotechnol Biofuels 7(1):140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SH, Linger J, Franden MA, Pienkos PT, Zhang M (2015) Biocatalysts with enhanced inhibitor tolerance. https://www.osti.gov/servlets/purl/1228373. Accessed 08 Dec 2015

  • Yang SH, Fei Q, Zhang YP, Contreras LM, Utturkar SM, Brown SD, Himmel ME, Zhang M (2016) Zymomonas mobilis as a model system for production of biofuels and biochemicals. Microb Biotechnol 9(6):699–717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Hu M, Tang Y, Geng B, Qiu M, He Q, Chen S, Wang X, Yang SH (2018) Progress and perspective on lignocellulosic hydrolysate inhibitor tolerance improvement in Zymomonas mobilis. Bioresour Bioprocess 5(1):6

    Article  Google Scholar 

  • Yi X, Gu HQ, Gao QQ, Liu ZL, Bao J (2015) Transcriptome analysis of Zymomonas mobilis ZM4 reveals mechanisms of tolerance and detoxification of phenolic aldehyde inhibitors from lignocellulose pretreatment. Biotechnol Biofuels 8:153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon KH, Park SH, Pack MY (1988) Transfer of Bacillus subtilis endo-β-1,4-glucanase gene into Zymomonas anaerobia. Biotechnol Lett 10(3):213–216

    Article  CAS  Google Scholar 

  • Young LJ, Hyun SB, Yu BJ, Hyoung LJ, Hee LS, Sun KM, Koob MD, Chang KS (2008) Phenotypic engineering by reprogramming gene transcription using novel artificial transcription factors in Escherichia coli. Nucleic Acids Res 36(16):e102

    Article  CAS  Google Scholar 

  • Yu L, Xu M, Tang IC, Yang ST (2015) Metabolic engineering of Clostridium tyrobutyricum for n-butanol production through co-utilization of glucose and xylose. Biotechnol Bioeng 112(10):2134–2141

    Article  CAS  PubMed  Google Scholar 

  • Zhang M, Eddy C, Deanda K, Finkelstein M, Picataggio S (1995) Metabolic engineering of a pentose metabolism pathway in ethanologenic Zymomonas mobilis. Science 267(5195):240–243

    Article  CAS  PubMed  Google Scholar 

  • Zhang M, Chou YC, Howe W, Eddy C, Evans K, Mohagheghi A (2007) Zymomonas pentose-sugar fermenting strains and uses thereof. https://www.osti.gov/servlets/purl/909424. Accessed 29 May 2007

  • Zhang LH, Lang YJ, Wang CX, Nagata S (2008) Promoting effect of compatible solute ectoine on the ethanol fermentation by Zymomonas mobilis CICC10232. Process Biochem 43(6):642–646

  • Zhang Y, Ma R, Zhao Z, Zhou Z, Lu W, Zhang W, Chen M (2010) irrE, an exogenous gene from Deinococcus radiodurans, improves the growth of and ethanol production by a Zymomonas mobilis strain under ethanol and acid stress. J Microbiol Biotechnol 20(7):1156–1162

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Wang TY, Zhou W, Jia XH, Wang HY (2013) Use of a Tn5-based transposon system to create a cost-effective Zymomonas mobilis for ethanol production from lignocelluloses. Microb Cell Fact 12(1):41

  • Zhang K, Shao H, Cao Q, He MX, Wu B, Feng H (2015) Transcriptional analysis of adaptation to high glucose concentrations in Zymomonas mobilis. Appl Microbiol Biotechnol 99(4):2009–2022

    Article  CAS  PubMed  Google Scholar 

  • Zhao N, Bai Y, Liu CG, Zhao XQ, Xu JF, Bai FW (2014) Flocculating Zymomonas mobilis is a promising host to be engineered for fuel ethanol production from lignocellulosic biomass. Biotechnol J 9(3):362–371

    Article  CAS  PubMed  Google Scholar 

  • Zhu L, Cai Z, Zhang Y, Li Y (2014) Engineering stress tolerance of Escherichia coli by stress-induced mutagenesis (SIM)-based adaptive evolution. Biotechnol J 9(1):120–127

    Article  CAS  PubMed  Google Scholar 

  • Zhu X, Zhao D, Qiu H, Fan F, Man S, Bi C, Zhang X (2017) The CRISPR/Cas9-facilitated multiplex pathway optimization (CFPO) technique and its application to improve the Escherichia coli xylose utilization pathway. Metab Eng 43(Pt A):37–45

    Article  CAS  PubMed  Google Scholar 

  • Zingaro KA, Papoutsakis ET (2013) GroESL overexpression imparts Escherichia coli tolerance to i-, n-, and 2-butanol, 1,2,4-butanetriol and ethanol with complex and unpredictable patterns. Metab Eng 15:196–205

    Article  CAS  PubMed  Google Scholar 

  • Zou SL, Hong LF, Wang C, Jing X, Zhang MH (2012) Construction of an unmarked Zymomonas mobilis mutant using a site-specific FLP recombinase. Food Technol Biotechnol 50(4):406–411

    CAS  Google Scholar 

Download references

Funding

This work was supported by grants from the Key Project of Natural Science of the Education Department of Henan Province, China (17A180028), the Youth Foundation of Henan Normal University (2015QK18), the National Research project Cultivation Foundation of Henan Normal University (2017PL08), and the Doctoral Scientific Research Start-up Foundation of Henan Normal University (5101049170167).

Author information

Authors and Affiliations

  1. Henan Province Engineering Laboratory for Bioconversion Technology of Functional Microbes, College of Life Sciences, Henan Normal University, Xinxiang, 453007, Henan, China

    Kun Zhang, Xinxin Lu, Yi Li, Xiaobing Jiang, Lei Liu & Hailei Wang

Authors
  1. Kun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xinxin Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaobing Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lei Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hailei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hailei Wang.

Ethics declarations

Competing interests

The authors declare that they have no competing interests.

Ethical approval

This study does not contain any studies with human participants or animals performed by any of the authors. All authors read and approved the final manuscript.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, K., Lu, X., Li, Y. et al. New technologies provide more metabolic engineering strategies for bioethanol production in Zymomonas mobilis. Appl Microbiol Biotechnol 103, 2087–2099 (2019). https://doi.org/10.1007/s00253-019-09620-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-019-09620-6

Keywords

Search

Navigation