Biotechnological conversion of glycerol from biofuels to 1,3-propanediol using Escherichia coli

• Authors: Hanna Przystałowska , Daniel Lipiński , Ryszard Słomski
• Languages of publication: EN

Abstracts

EN

In the face of shortage of fossil fuel supplies and climate warming triggered by excessive carbon dioxide emission, alternative resources for chemical industry have gained considerable attention. Renewable resources and their derivatives are of particular interest. Glycerol, which constitutes one of the by-products during biodiesel production, is such a substrate. Thus, generated excess glycerol may become an environmental problem, since it cannot be disposed of in the environment. The most promising products obtained from glycerol are polyols, including 1,3-propanediol, an important substrate in the production of synthetic materials, e.g. polyurethanes, unsaturated polyesters, and epoxy resins. Glycerol can be used as a carbon and energy source for microbial growth in industrial microbiology to produce 1,3-propanediol. This paper is a review of metabolic pathways of native producers and E. coli with the acquired ability to produce the diol via genetic manipulations. Culture conditions during 1,3-PDO production and genetic modifications of E. coli used in order to increase efficiency of glycerol bioconversion are also described in this paper.

Keywords

EN

bioconversion; biodiesel; carbon source; Escherichia coli; glycerol; 1,3-propanediol

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2015
• Volume: 62
• Issue: 1
• Pages: 23-34

Dates

published

2015

received

2014-09-05

revised

2014-11-20

accepted

2014-11-29

online

2015-02-24

Contributors

author

Hanna Przystałowska

• Poznan University of Life Sciences, Department of Biochemistry and Biotechnology, Poznań, Poland

author

Daniel Lipiński

• Poznan University of Life Sciences, Department of Biochemistry and Biotechnology

author

Ryszard Słomski

• Poznan University of Life Sciences, Department of Biochemistry and Biotechnology

References

• Ahrens K, Menzel K, Zeng AP, Deckwer WD (1998) Kinetic, dynamic, and pathway studies of glycerol metabolism by Klebsiella pneumoniae in anaerobic continuous culture: III. Enzymes and fluxes of glycerol dissimilation and 1,3-propanediol formation. Biotechnol Bioeng 59: 544-552.
• Barbirato F, Grivet JP, Soucaille P, Bories A (1996) 3-Hydroxypropionaldehyde, an inhibitory metabolite of glycerol fermentation to 1,3-propanediol by enterobacterial species. Appl Environ Microbiol 62: 1448-1451.
• Barbirato F, Himmi EH, Conte T, Bories A (1998) 1,3-Propanediol production by fermentation: an interesting way to valorize glycerin from the ester and ethanol industries. Ind Crops Prod 7: 281-289.
• Biebl H, Menzel K, Zeng AP, Deckwer WD (1999) Microbial production of 1,3-propanediol. Appl Microbiol Biotechnol 52: 289-297.
• Biebl H, Zeng AP, Menzel K, Deckwer WD (1998) Fermentation of glycerol to 1,3-propanediol and 2,3-butanediol by Klebsiella pneumoniae. Appl Microbiol Biotechnol 50: 24-29.
• Biebl H (2001) Fermentation of glycerol by Clostridium pasteurianum - batch and continuous culture studies. J Ind Microbiol Biotechnol 27: 18-26.
• Boenigk R, Bowien S, Gottschalk G (1993) Fermentation of glycerol to 1,3-propanediol in continuous cultures of Citrobacter freundii. Appl Microbiol Biotechnol 38: 453-457.
• Booth I R (2005) Glycerol and methylglyoxal metabolism. Escherichia coli and Salmonella: Cellular and Molecular Biology. Online ed. ASM Press, Washington, DC (Module 3.4.3).
• Borgnia MJ, Agre P (2001) Reconstitution and functional comparison of purified GlpF and AqpZ, the glicerol and water channels from Escherichia coli. Proc Natl Acad Sci USA 98: 2888-2893.
• Bouvet OM, Lenormand P, Ageron E, Grimont PA (1995) Taxonomic diversity of anaerobic glycerol dissimilation in the Enterobacteriaceae. Res Microbiol 146: 279-290.
• Bouvet OM, Lenormand P, Carlier P, Grimont PA (1994) Phenotypic diversity of anaerobic glycerol dissimilation shown by seven enterobacterial species. Res Microbiol 145: 129-139.
• Brown HS, Chuah HH (1997) Texturing of textile filament yarns based on poly(trimethylene terephthalate). Chem Fibers Int 47: 72-74.
• Cameron DC, Altaras NE, Hoffman ML, Shaw AJ (1998) Metabolic engineering of propanediol pathways. Biotechnol Prog 14: 116-125.
• Chen X, Du W, Liu D (2008) Response surface optimization of biocatalytic biodiesel production with acid oil. Biochem Eng J 40: 423-429.
• Chen Z, Liu H, Liu D (2009) Regulation of 3-hydroxypropionaldehyde accumulation in Klebsiella pneumoniae by overexpression of dhaT and dhaD genes. Enzyme Microb Technol 45: 305-309.
• Cheng KK, Liu DH, Sun Y, Liu WB (2004) 1,3-Propanediol production by Klebsiella pneumoniae under different aeration strategies. Biotechnol Lett 26: 911-915.
• Cheng KK, Zhang JA, Liu DH, Sun Y, Liu HJ, Yang MD, Xu JM (2007) Pilot-scale production of 1,3-propanediol using Klebsiella pneumoniae. Process Biochem 42: 740-744.
• Chotani G, Dodge T, Hsu A, Kumar M, LaDuca R, Trimbur D, Weyler W, Sanford K (2000) The commercial production of chemicals using pathway engineering. Biochim Biophys Acta 1543: 434-455.
• Chuah H, Brown HS, Dalton PA (1995) Corterra poly(trimethylene terephthalate) - a new performance carpet fiber. Int Fiber J
• Chuah H (1996) Corterra polytrimethylene terephthalate - new polymeric fiber for carpets. Chem Fibers Int 46: 424-428.
• Clomburg JM, Gonzalez R (2010) Metabolic engineering of Escherichia coli for the production of 1,2-propanediol from glycerol. Biotechnol Bioeng 108: 867-879.
• Colin T, Bories A, Lavigne C, Moulin G (2001) Effects of acetate and butyrate during glycerol fermentation by Clostridium butyricum. Curr Microbiol 43: 238-243.
• Da Silva GP, Mack M, Contiero J (2009) Glycerol: a promising and abundant carbon source for industrial microbiology. Biotechnol Adv 27: 30-39.
• Daniel R, Gottschalk G (1992) Growth temperature-dependent activity of glycerol dehydratase in Escherichia coli expressing the Citrobacter freundii dha regulon. FEMS Microbiol Lett 100: 281-286.
• Daniel R, Stuertz K, Gottschalk G (1995) Biochemical and molecular characterization of the oxidative branch of glycerol utilization by Citrobacter freundii. J Bacteriol 177: 4392-4401.
• Dąbrowski S, Pietrewicz-Kubicz D, Zabłotna E, Długołęcka A (2012) 1,3-propanediol production by Escherichia coli expressing genes of dha operon from Clostridium butyricum 2CR371.5. Acta Biochim Polon 59: 357-361.
• Deckwer WD (1995) Microbial conversion of glycerol to 1,3-propanediol. FEMS Microbiol Rev 16: 143-149.
• Demirbas MF, Balat M (2006) Recent advances on the production and utilization trends of biofuels: a global perspective. Energ Convers Manage 47: 2371-2381.
• Dharmadi Y, Murarka A, Gonzalez R (2006) Anaerobic fermentation of glycerol by Escherichia coli: a new platform for metabolic engineering. Biotechnol Bioeng 94: 821-829.
• Drożdżyńska A, Leja K, Czaczyk K (2011) Biotechnological Production of 1,3-Propanediol from Crude Glycerol. J Biotechnol Comput Biol Bionanotechnol 1: 92-100.
• Frazzetto G (2003) White Biotechnology. EMBO Rep 4: 835-837.
• Emptage M, Haynie SL, Laffend LA, Pucci JP, Whited G (2003) Process for the biological production of 1,3-propanediol with high titer. U.S. Patent; No 6514733.
• Forage R, Lin EC (1982) DHA system mediating aerobic and anaerobic dissimilasion of glycerol in Klebsiella pneumoniae NCIB418. J Bacteriol 151: 591-599.
• Gonzalez R, Murarka A, Dharmadi Y, Yazdani SS (2008) A new model for the anaerobic fermentation of glycerol in enteric bacteria: Trunk and auxiliary pathways in Escherichia coli. Metab Eng 10: 234-245.
• Gonzalez-Pajuelo M, Meynial-Salles I, Mendes F, Soucaille P, Vasconcelos I (2006) Microbial conversion of glycerol to 1,3-propanediol: physiological comparison of a natural producer, Clostridium butyricum VPI 3266, and an engineered strain, Clostridium acetobutylicum DGI (pSPD5). Appl Environ Microbiol 72: 96-101.
• González-Pajuelo M, Andrade JC, Vasconcelos I (2004) Production of 1,3-propanediol by Clostridium butyricum VPI 3266 using a synthetic medium and raw glycerol. J Ind Microbiol Biotechnol 31: 442-446.
• Hakobyan M, Sargsyan H, Bagramyan K (2005) Proton translocation coupled to formate oxidation in anaerobically grown fermenting Escherichia coli. Biophys Chem 115: 55-61.
• Hao J, Lin R, Zheng Z, Liu H, Liu D (2008a) Isolation and characterization of microorganisms able to produce 1,3-propanediol under aerobic conditions. World J Microbiol Biotechnol 24: 1731-1740.
• Hao J, Wang W, Tian J, Li J, Liu D (2008) Decrease of 3-hydroxypropionaldehyde accumulation in 1,3-propanediol production by over-expressing dha T gene in Klebsiella pneumoniae TUAC01. J Ind Microbiol Biotechnol 35: 735-741.
• Hao J, Xu F, Liu H, Liu D (2006) Downstream processing of 1,3-propanediol fermentation broth. J Chem Technol Biotechnol 81: 102-108.
• Hartlep M, Hussman W, Prayitno N, Meynial-Salles I, Zeng AP (2002) Study of two-stage processes for the microbial production of 1,3-propanediol from glycerol. Appl Microbiol Biotechnol 60: 60-66.
• Himmi EL, Bories A, Barbirato F (1999) Nutrient requirements for glycerol conversion to 1,3-propanediol by Clostridium butyricum. Bioresour Technol 67: 123-128.
• Homann T, Tag C, Biebl H, Deckwer WD, Schink B (1990) Fermentation of glycerol to 1,3-propanediol by Klebsiella and Citrobacter strains. Appl Microbiol Biotechnol 33: 121-126.
• Honda S, Toraya T, Fukui S (1980) In situ reactivation of glycerol-inactivated coenzyme B12-dependent enzymes, glycerol dehydratase, and diol dehydratase. J Bacteriol 143: 1458-1465.
• Huang H, Gong CS, Tsao GT (2002) Production of 1,3-propanediol by Klebsiella pneumoniae. Appl Biochem Biotechnol 98-100: 687-698.
• Igari S, Mori S, Takikawa Y (2000) Effects of molecular structure of aliphatic diols and polyalkylene glycol as lubricants on the wear of aluminum. Wear 244: 180-184.
• Johnson EA, Lin EC (1987) Klebsiella pneumoniae 1,3-propanediol: NAD+ oxidoreductase. J Bacteriol 169: 2050-2054.
• Kajiura H, Mori K, Shibata N, Toraya T (2007) Molecular basis for specificities of reactivating factors for adenosylcobalamin-dependent diol and glycerol dehydratases. FEBS J 274: 5556-5566.
• Katrlík J, Vostiar I, Sefcovicová J, Tkác J, Mastihuba V, Valach M, Stefuca V, Gemeiner P (2007) A novel microbial biosensor based on cells of Gluconobacter oxydans for the selective determination of 1,3-propanediol in the presence of glycerol and its application to bioprocess monitoring. Anal Bioanal Chem 388: 287-295.
• Knietsch A, Bowien S, Whited G, Gottschalk G, Daniel R (2003) Identification and characterization of coenzyme B12-dependent glycerol dehydratase- and diol dehydratase-encoding genes from metagenomic DNA libraries derived from enrichment cultures. Appl Env Microbiol 69: 3048-3060.
• Kraus GA (2008) Synthetic methods for the preparation of 1,3-propanediol. Clean 36: 648-651.
• Kubiak P, Leja K, Myszka K, Celińska E, Spychała M, Szymanowska-Powałowska D, Czaczyk K, Grajek W (2012) Physiological predisposition of various Clostridium species to synthetize 1,3-propanediol from glycerol. Process Biochem 47: 1308-1319.
• Kurian JVA (2005) New polymer platform for the future-Sorona® from corn derived 1,3-propanediol. J Polym Environ 13: 159-167
• Lawrence F.R., Sullivan R.H. (1972) Process for making a dioxane. U.S. Patent; No 3687981.
• Leja K, Czaczyk K, Myszka K (2011) Biotechnological synthesis of 1,3-propanediol using Clostridium spp. Afr J Biotechnol 10: 11093-11101.
• Lin EC (1976) Glycerol dissimilation and its regulation in bacteria. Annu Rev Microbiol 30: 535-578.
• Lin R, Liu H, Hao J, Cheng K, Liu D (2005) Enhancement of 1,3-propanediol production by Klebsiella pneumoniae with fumarate addition. Biotechnol Lett 27: 1755-1759.
• Liu H, Xu Y, Zheng Z, Liu D (2010) 1,3-Propanediol and its copolymers: Research, development and industrialization. Biotechnol J 5: 1137-1148.
• Lu D, Grayson P, Schulten K (2003) Glycerol conductance and physical asymmetry of the Escherichia coli glycerol facilitator GlpF. Biophys J 85: 2977-2987.
• Ma BB, Xu XL, Zhang GL, Wang LW, Wu M, Li C (2009) Microbial production of 1,3-propanediol by Klebsiella pneumoniae XJPD-Li under different aeration strategies. Appl Biochem Biotechnol 152: 127-134.
• Ma Z, Rao Z, Xu L, Liao X, Fang H, Zhuge B, Zhuge J (2009a) Production of 1,3-propanediol from glycerol by engineered Escherichia coli using a novel coexpression vector. Afr J Biotechnol 8: 5500-5505.
• Ma Z, Rao Z, Xu L, Liao X, Fang H, Zhuge B, Zhuge J (2010) Expression of dha Operon Required for 1,3-PD Formation in Escherichia coli and Saccharomyces cerevisiae. Curr Microbiol 60: 191-198.
• Malaoui H, Marczak R (2001) Influence of glucose on glycerol metabolism by wild-type and mutant strains of Clostridium butyricum E5 grown in chemostatic culture. Appl Microbiol Biotechnol 55: 226-233.
• Malaoui H, Marczak R (2000) Purification and characterization of the 1,3-propanediol dehydrogenase of Clostridium butyricum E5. Enzyme Microb Technol 27: 399-405.
• Malinowski J (1999) Evaluation of liquid extraction potentials for downstream separation of 1,3-propanediol. Biotechnol Tech 13: 127-130.
• Menzel K, Zeng AP, Deckwer WD (1997) High concentration and productivity of 1,3-propanediol from continuous fermentation of glycerol by Klebsiella pneumoniae. Enzyme Microb Technol 20: 82-86.
• Mori K, Tobimatsu T, Hara T, Toraya T (1997) Characterization, sequencing, and expression of the genes encoding a reactivating Factor for glycerol-inactivated adenosylcobalamin-dependent diol dehydratase. J Biol Chem 272: 32034-32041.
• Mu Y, Teng H, Zhang DJ, Wang W, Xiu ZL (2006) Microbial production of 1,3-propanediol by Klebsiella pneumoniae using crude glycerol biodiesel preparations. Biotechnol Lett 28: 1755-1759.
• Murarka A, Dharmadi Y, Yazdani SS, Gonzalez R (2008) Fermentative utilization of glycerol in Escherichia coli and its implications for the production of fuels and chemicals. Appl Environ Microbiol 74: 1124-1135.
• Nakamura CE, Whited GM (2003) Metabolic engineering for the microbial production of 1,3-propanediol. Curr Opin Biotechnol 14: 454-459.
• Nakas JP, Schaedle M, Parkinson CM, Coonley CE, Tanenbaum SW (1983) System development for linked-fermentation products of solvents from algal biomass. Appl Environ Microbiol 46: 1017-1023.
• Németh A, Kupcsulik B, Sevella B (2003) 1,3-propanediol oxidoreductase production with Klebsiella pneumoniae DSM2026. World J Microbiol Biotechnol 19: 659-663.
• Papanikolaou S, Fakas S, Fick M, Chevalot I, Galiotou-Panayotou M, Komaitis M, Marc I, Aggelis G (2008) Biotechnological valorisation of raw glycerol discharged after bio-diesel (fatty acid methyl esters) manufacturing process: Production of 1,3-propanediol, citric acid and single cell oil. Biomass Bioenerg 32: 60-71.
• Papanikolaou S, Fick M, Aggelis G (2004) The effect of raw glycerol concentration on the production of 1,3-propanediol by Clostridium butyricum. J Chem Technol Biotechnol 79: 1189-1196.
• Paulsen IT, Reizer J, Jin RZ, Lin EC, Saier MH Jr. (2000) Functional genomic studies of dihydroxyacetone utilization in Escherichia coli. Microbiology 146: 2343-2344.
• Qi X, Guo Q, Wei Y, Xu H, Huang R (2011) Construction of a Novel Recombinant Escherichia coli Strain Capable of Producing 1,3-propanediol. Adv Mat Res 396-398: 2499-2502.
• Ragauskas AJ, Williams CK, Davison BH, Britovsek G, Cairney J, Eckert CA (2006) The path forward for biofuels and biomaterial. Science 311: 484-489.
• Raynaud C, Sarcabal P, Meynial-Salles I, Croux C, Soucaille P (2003) Molecular characterization of the 1,3-propanediol (1,3-PD) operon of Clostridium butyricum. Proc Natl Acad Sci 100: 5010-5015.
• Rehman A, Matsumura M, Nomura N, Sato S (2008) Growth and 1,3-propanediol production on pre-treated sunflower oil bio-diesel raw glycerol using a strict anaerobe Clostridium butyricum. Curr Res Bacteriol 1: 7-16.
• Sauer M, Marx H, Mattanovich D (2008) Microbial production of 1,3-propanediol. Recent Pat Biotechnol 2: 191-197.
• Saxena RK, Anand P, Saran S, Isar J (2009) Microbial production of 1,3-propanediol: recent developments and emerging opportunities. Biotechnol Adv 27: 895-913.
• Schryvers A, Weiner JH (1982) The anaerobic sn-glycerol-3-phosphate dehydrogenase: cloning and expression of the glpA gene of Escherichia coli and identification of the glpA products. Can J Biochem 60: 224-231.
• Schutz H, Radler F (1984) Anaerobic reduction of glycerol to 1,3-propanediol by Lactobacillus brevis and Lactobacillus buchneri. Syst Appl Microbiol 5: 169-178.
• Seifert C, Bowien S, Gottschalk G, Daniel R (2001) Identification and expression of the genes and purification and characterization of the genes products involved in reactivation of coenzyme B12-dependent glycerol dehydratase of Citrobacter freundii. Eur J Biochem 268: 2369-2378.
• Seyfried M, Daniel R, Gottschalk G (1996) Cloning, sequencing, and over expression of the genes encoding coenz B12-dependent glycerol dehydratase of Citrobacter freundii. J Bacteriol 178: 5793-5796.
• Shell Chemical Company. (1995) Shell Chemical Company announces commercialization of new polymer (Press release).
• Skraly FA, Lytle BL, Cameron DC (1998) Construction and characterization of a 1,3-propanediol operon. Appl Environ Microbiol 64: 98-105.
• Sulzenbacher G, Alvarez K, van den Heuvel J, Versluis C, Spinelli S, Campanacci V, Valencia C, Cambillau C, Eklund H, Tegoni M (2004) Crystal structure of E.coli alcohol dehydrogenase YqhD: evidence of a covalently modified NADP coenzyme. J Mol Biol 342: 489-502.
• Sun J, Van den HJ, Soucaille P, Qu Y, Zeng AP (2003) Comparative genomic analysis of DHA regulon and related genes for anaerobic glycerol metabolism. Biotechnol Prog 19: 263-272.
• Szymanowska-Powałowska D, Piątkowska J, Leja K (2013) Microbial Purification of Postfermentation Medium after 1,3-PD Production from Raw Glycerol. Biomed Res Int Article ID 949107, 7 pages; http: //dx.doi.org/10.1155/2013/949107.
• Tang X, Tan Y, Zhu H, Zhao K, Shen W (2009) Microbial conversion of glycerol to 1,3-propanediol by an engineered strain of Escherichia coli. Appl Environ Microbiol 75: 1628-1634.
• Tobimatsu T, Hara T, Sakaguchi M, Kishimoto Y, Wada Y, Isoda M, Sakai T, Toraya T (1995) Molecular cloning, sequencing, and expression of the genes encoding adenosylcobalamin-dependent diol dehydrase of Klebsiella oxytoca. J Biol Chem 270: 7142-7148.
• Tong IT, Liao HH, Cameron DC (1991) 1,3-Propanediol production by Escherichia coli expressing genes from the Klebsiella pneumoniae DHA regulon. Appl Environ Microbiol 57: 3541-3546.
• Tong LT, Cameron DC (1992) Enhancement of 1,3-propanediol production by co-fermentation in Escherichia coli expressing genes from Klebsiella pneumoniae dha regulon genes. Appl Biochem Biotechnol 34-35: 149-159.
• Voegele RT, Sweet GD, Boos W (1993) Glycerol kinase of Escherichia coli is activated by interaction with the glycerol facilitator. J Bacteriol 175: 1087-1094.
• Walz AC, Demel RA, de Kruijff B, Mutzel R (2002) Aerobic sn-glycerol-3-phosphate dehydrogenase from Escherichia coli binds to the cytoplasmic membrane through an amphipathic α-helix. Biochem J 365: 471-479.
• Wang F, Qu H, Zhang D, Tian P, Tan T (2007) Production of 1,3-propanediol from glycerol by recombinant E.coli using incompatible plasmids system. Mol Biotechnol 37: 112-119.
• Wang W, Sun J, Hartlep M, Deckwer DW, Zeng AP (2003) Combined use of proteomic analysis and enzyme activity assays for metabolic pathway analysis of glycerol fermentation by Klebsiella pneumoniae. Biotechnol Bioeng 83: 525-536.
• Werle P, Morawietz M, Lundmark S, Sörensen K, Karvinen E, Lehtonen J (2006) Alcohols, Polyhydric. Ullmann's Encyclopedia of Industrial Chemistry, Wiley-VCH, Weinheim.
• Willke T, Vorlop K (2008) Biotransformation of glycerol into 1,3-propanediol. Eur J Lipid Sci Technol 110: 831-840.
• Xiu ZL, Chen X, Sun YQ, Zhang DJ (2007) Stoichiometric analysis and experimental investigation of glycerol-glucose cofermentation in Klebsiella pneumoniae under microaerobic conditions. Biochem Eng J 33: 42-52.
• Xiu ZL, Song BH, Wang ZT, Sun LH, Feng EM, Zeng AP (2004) Optimization of dissimilation of glycerol to 1,3-propanediol by Klebsiella pneumoniae in one- and two-stage anaerobic cultures. Biochem Eng J 19: 189-197.
• Xiu ZL, Zeng AP (2008) Present state and perspective of downstream processing of biologically produced 1,3-propanediol and 2,3-butanediol. Appl Microbiol Biotechnol 78: 917-926.
• Xu XL, Zhang GL, Wang LW, Ma BB, Li C (2009) Quantitative analysis on inactivation and reactivation of recombinant glycerol dehydratase from Klebsiella pneumoniae XJPD-Li. J Mol Catal B Enzym 56: 108-114.
• Xu YY, Du W, Liu DH, Zeng J (2003) A novel enzymatic route for biodiesel production from renewable oils in a solvent free medium. Biotechnol Lett 25: 1239-1241.
• Xu YZ, Guo NN, Zheng ZM, Ou XJ, Liu HJ, Liu DH (2009a) Metabolism in 1,3-propanediol fed-batch fermentation by a D-lactate deficient mutant of Klebsiella pneumoniae. Biotechnol Bioeng 104: 965-972.
• Yang FA, Hanna M, Sun R (2012) Value-added uses for crude glycerol-a byproduct of biodiesel production. Biotechnol Biofuels 5: 13.
• Yang G, Tian J, Li J (2007) Fermentation of 1,3-propanediol by a lactate deficient mutant of Klebsiella oxytoca under microaerobic conditions. Appl Microbiol Biotechnol 73: 1017-1024.
• Yazdani SS, Gonzalez R (2007) Anaerobic fermentation of glycerol: a path to economic viability for the biofuels industry. Curr Opin Biotech 18: 213-219.
• Zeng AP, Biebl H (2002) Bulk chemicals from biotechnology: the case of 1,3-propanediol production and the new trends. Adv Biochem Eng/Biotechnol 74: 239-259.
• Zeng AP, Biebl H, Schlieker H, Deckwer WD (1993) Pathway analysis of glycerol fermentation by Klebsiella pneumoniae: regulation of reducing equivalent balance and product inhibition. Enzyme Microb Technol 15: 771-779.
• Zeng AP, Ross A, Biebl H, Tag C, Günzel B, Deckwer WD (1994) Multiple product inhibition and growth modeling of Clostridium butyricum and Klebsiella pneumoniae in glycerol fermentation. Biotechnol Bioeng 44: 902-911.
• Zhang GL, Maa BB, Xua XL, Chun L, Wang L (2007) Fast conversion of glycerol to 1,3-propanediol by a new strain Klebsiella pneumoniae. Biochem Eng J 37: 256-260.
• Zhang Q, Teng H, Sun Y, Xiu Z, Zeng AP (2008) Metabolic flux and robustness analysis of glycerol metabolism in Klebsiella pneumoniae. Bioprocess Biosyst Eng 31: 127-135.
• Zhang X, Li Y, Zhuge B, Tang X, Shen W, Rao Z (2006a) Construction of a novel recombinant Escherichia coli strain capable of producing 1,3-propanediol and optimization of fermentation parameters by statistical design. World J Microbiol Biotechnol 22: 945-952.
• Zhang XM, Tang XM, Zhuge B, Shen W, Rao ZM, Fang HY, Zhuge J (2005) Construction of novel recombinant Escherichia coli capable of producing 1,3-propanediol. Sheng Wu Gong Cheng Xue Bao 21: 743-747.
• Zhang Y-HP (2011) What is vital (and not vital) to advance economically-competitive biofuels production. Process Biochem 46: 2091-2110.
• Zhang Z, Li Y, Du C, Liu M, Cao Z (2006) Inactivation of aldehyde dehydrogenase: a key factor for engineering 1,3-propanediol production by Klebsiella pneumoniae. Metab Eng 8: 578-586.
• Zheng P, Wereath K, Sun J, van den Heuvel J, Zeng AP (2006) Overexpression of genes of the dha regulon and its effects on the cell growth, glycerol fermentation to 1,3-propanediol and plasmid stability in Klebsiella pneumoniae. Process Biochem 41: 2160-2169.
• Zheng ZM, Xu YZ, Liu HJ, Guo NN, Cai ZZ, Liu DH (2008) Physiologic mechanisms of sequential products synthesis in 1,3-propanediol fed-batch fermentation by Klebsiella pneumoniae. Biotechnol Bioeng 100: 923-932.
• Zhu MM, Skraly FA, Cameron DC (2001) Accumulation of methylglyoxal in anaerobically grown Escherichia coli and its detoxification by expression of the Pseudomonas putida glyoxalase I gene. Metab Eng 3: 218-225.
• Zhu MM, Lawman PD, Cameron DC (2002) Improving 1,3-propanediol production from glycerol in a metabolically engineered Escherichia coli by reducing accumulation of sn-Glycerol-3-phosphate. Biotechnol Prog 18: 694-699.
• Zhuge B, Zhang C, Fang H, Zhuge J, Permaul K (2010) Expression of 1,3-propanediol oxidoreductase and its isoenzyme in Klebsiella pneumoniae for bioconversion of glycerol into 1,3-propanediol. Appl Microbiol Biotechnol 87: 2177-2184.
• Zhuge J, Fang HY, Wang ZX, Chen DZ, Jin HR, Gu HL (2001) Glycerol production by a novel osmotolerant yeast Candida glycerinogenes. Appl Microbiol Biotechnol 55: 686-692.