Switching Clostridium acetobutylicum to an ethanol producer by disruption of the butyrate/butanol fermentative pathway

Metabolic Engineering

Volumn 13, Issue 5, 2011, Pages 464-473

  Lehmann, Dörte ^a   Lütke Eversloh, Tina ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

3 hydroxybutyryl CoA dehydrogenase; Biofuel; Butanol; Clostridium; Ethanol

Indexed keywords

3-HYDROXYBUTYRYL-COA DEHYDROGENASE; ALCOHOL DEHYDROGENASE; BATCH CULTURE; CELL EXTRACTS; CLOSTRIDIUM ACETOBUTYLICUM; ETHANOL PRODUCTION; FED-BATCH FERMENTATION; GLUCOSE YIELDS; METABOLIC PATHWAYS; MOLECULAR HYDROGEN; NEGATIVE MUTANTS; PRODUCT PATTERNS; SOLVENTOGENIC CLOSTRIDIA; WILD-TYPE STRAIN;

ACETONE; ALCOHOLS; BATCH CELL CULTURE; CLOSTRIDIUM; ETHANOL; FERMENTATION; GENETIC ENGINEERING; GLUCOSE; METABOLISM;

ORGANIC SOLVENTS;

3 HYDROXYBUTYRYL COENZYME A DEHYDROGENASE; ACETONE; ACETYL COENZYME A ACETYLTRANSFERASE; ALCOHOL; ALCOHOL DEHYDROGENASE; BUTANOL; BUTYRIC ACID; CELL EXTRACT; ENOYL COENZYME A HYDRATASE; GLUCOSE; HYDROGEN; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SUGAR; UNCLASSIFIED DRUG; XYLOSE;

ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIUM CULTURE; BIOSYNTHESIS; CLOSTRIDIA; CLOSTRIDIUM ACETOBUTYLICUM; CONTROLLED STUDY; ENZYME ACTIVITY; FERMENTATION; GENETIC ENGINEERING; NONHUMAN; PRIORITY JOURNAL; WILD TYPE;

3-HYDROXYACYL COA DEHYDROGENASES; ALCOHOL DEHYDROGENASE; BACTERIAL PROTEINS; BUTANOLS; BUTYRATES; CLOSTRIDIUM ACETOBUTYLICUM; CULTURE MEDIA; ENOYL-COA HYDRATASE; ETHANOL; FERMENTATION; GENE KNOCKDOWN TECHNIQUES; GENES, BACTERIAL; GLUCOSE; MUTATION; XYLOSE;

CLOSTRIDIA; CLOSTRIDIUM; CLOSTRIDIUM ACETOBUTYLICUM;

EID: 80052029042     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2011.04.006     Document Type: Article

References (68)

1. Alper H., Stephanopoulos G. Engineering for biofuels: exploiting innate microbial capacity or importing biosynthetic potential?. Nat. Rev. Microbiol. 2009, 7:715-723.
2. Bergmeyer H.U. Methods in Enzymatic Analysis 1983, Verlag Chemie, Weinheim, Germany.
3. Bradford M.M. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal. Biochem. 1976, 72:248-254.
4. Breznak J.A., Costilow R.N. Physicochemical factors in growth. Methods for General and Molecular Bacteriology 1994, American Society for Microbiology, Washington, DC, USA. P. Gerhardt, R.G.E. Murray, W.A. Wood, N.R. Krieg (Eds.).
5. Chen J.S. Alcohol dehydrogenase: multiplicity and relatedness in the solvent-producing clostridia. FEMS Microbiol. Rev. 1995, 17:263-273.
6. Cornillot E., Nair R.V., Papoutsakis E.T., Soucaille P. The genes for butanol and acetone formation in Clostridium acetobutylicum ATCC 824 reside on a large plasmid whose loss leads to degeneration of the strain. J. Bacteriol. 1997, 179:5442-5447.
7. Desai R.P., Harris L.M., Welker N.E., Papoutsakis E.T. Metabolic flux analysis elucidates the importance of the acid-formation pathways in regulating solvent production by Clostridium acetobutylicum. Metab. Eng. 1999, 1:206-213.
8. Desai R.P., Papoutsakis E.T. Antisense RNA strategies for metabolic engineering of Clostridium acetobutylicum. Appl. Environ. Microbiol. 1999, 65:936-945.
9. Dong H., Zhang Y., Dai Z., Li Y. Engineering Clostridium strain to accept unmethylated DNA. PLoS One 2010, 5:e9038.
10. Dürre P., Kuhn A., Gottwald M., Gottschalk G. Enzymatic investigations on butanol dehydrogenase and butyraldehyde dehydrogenase in extracts of Clostridium acetobutylicum. Appl. Microbiol. Biotechnol. 1987, 26:268-272.
11. Dürre P., Fischer R.J., Kuhn A., Lorenz K., Schreiber W., Stürzenhofecker B., Ullmann S., Winzer K., Sauer U. Solventogenic enzymes of Clostridium acetobutylicum: catalytic properties, genetic organization, and transcriptional regulation. FEMS Microbiol. Rev. 1995, 17:251-262.
12. Dürre P. Biobutanol: an attractive biofuel. Biotechnol. J 2007, 2:1525-1534.
13. Dürre P. Fermentative butanol production: bulk chemical and biofuel. Ann. NY Acad. Sci. 2008, 1125:353-362.
14. Ezeji T.C., Qureshi N., Blaschek H.P. Bioproduction of butanol from biomass: from genes to bioreactors. Curr. Opin. Biotechnol. 2007, 18:220-227.
15. Ezeji T., Milne C., Price N.D., Blaschek H.P. Achievements and perspectives to overcome the poor solvent resistance in acetone and butanol-producing microorganisms. Appl. Microbiol. Biotechnol. 2010, 85:1697-1712.
16. Fischer C.R., Klein-Marcuschamer D., Stephanopoulos G. Selection and optimization of microbial hosts for biofuels production. Metab. Eng. 2008, 10:295-304.
17. Fischer R.J., Oehmcke S., Meyer U., Mix M., Schwarz K., Fiedler T., Bahl H. Transcription of the pst operon of Clostridium acetobutylicum is dependent on phosphate concentration and pH. J. Bacteriol. 2006, 188:5469-5478.
18. Fond O., Engasser J.M., Matta-El-Amouri G., Petitdemange H. The acetone butanol fermentation on glucose and xylose. I. Regulation and kinetics in batch cultures. Biotechnol. Bioeng. 1986, 28:160-166.
19. Fond O., Engasser J.M., Matta-El-Amouri G., Petitdemange H. The acetone butanol fermentation on glucose and xylose. II. Regulation and kinetics in fed-batch cultures. Biotechnol. Bioeng. 1986, 28:167-175.
20. Fontaine L., Meynial-Salles I., Girbal L., Yang X., Croux C., Soucaille P. Molecular characterization and transcriptional analysis of adhE2, the gene encoding the NADH-dependent aldehyde/alcohol dehydrogenase responsible for butanol production in alcohologenic cultures of Clostridium acetobutylicum ATCC 824. J. Bacteriol. 2002, 184:821-830.
21. Gheshlaghi R., Scharer J.M., Moo-Young M., Chou C.P. Metabolic pathways of clostridia for producing butanol. Biotechnol. Adv. 2009, 27:764-781.
22. Girbal L., Croux C., Vasconcelos I., Soucaille P. Regulation of metabolic shifts in Clostridium acetobutylicum ATCC 824. FEMS Microbiol. Rev. 1995, 17:287-297.
23. Grant S.G., Jessee J., Bloom F.R., Hanahan D. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc. Natl. Acad. Sci. USA 1990, 87:4645-4649.
24. Green E.M., Boynton Z.L., Harris L.M., Rudolph F.B., Papoutsakis E.T., Bennett G.N. Genetic manipulation of acid formation pathways by gene inactivation in Clostridium acetobutylicum ATCC 824. Microbiology 1996, 142:2079-2086.
25. Grimmler C., Janssen H., Krauße D., Fischer R.J., Bahl H., Dürre P., Liebl W., Ehrenreich A. Genome-wide gene expression analysis of the switch between acidogenesis and solventogenesis in continuous cultures of Clostridium acetobutylicum. J. Mol. Microbiol. Biotechnol. 2011, 20:1-15.
26. Hahn-Hägerdal B., Karhumaa K., Fonseca C., Spencer-Martins I., Gorwa-Grauslund M.F. Towards industrial pentose-fermenting yeast strains. Appl. Microbiol. Biotechnol. 2007, 74:937-953.
27. Harris L.M., Desai R.P., Welker N.E., Papoutsakis E.T. Characterization of recombinant strains of the Clostridium acetobutylicum butyrate kinase inactivation mutant: need for new phenomenological models for solventogenesis and butanol inhibition?. Biotechnol. Bioeng. 2000, 67:1-11.
28. Hartmanis M.G., Gatenbeck S. Intermediary metabolism in Clostridium acetobutylicum: levels of enzymes involved in the formation of acetate and butyrate. Appl. Environ. Microbiol. 1984, 47:1277-1283.
29. Heap J.T., Pennington O.J., Cartman S.T., Carter G.P., Minton N.P. The ClosTron: a universal gene knock-out system for the genus Clostridium. J. Microbiol. Methods 2007, 70:452-464.
30. Heap J.T., Kuehne S.A., Ehsaan M., Cartman S.T., Cooksley C.M., Scott J.C., Minton N.P. The ClosTron: mutagenesis in Clostridium refined and streamlined. J. Microbiol. Methods 2010, 80:49-55.
31. Hermann M., Fayolle F., Marchal R., Podvin L., Sebald M., Vandecasteele J.P. Isolation and characterization of butanol-resistant mutants of Clostridium acetobutylicum. Appl. Environ. Microbiol. 1985, 50:1238-1243.
32. Ho S.N., Hunt H.D., Horton R.M., Pullen J.K., Pease L.R. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 1989, 77:51-59.
33. Huang K.X., Huang S., Rudolph F.B., Bennett G.N. Identification and characterization of a second butyrate kinase from Clostridium acetobutylicum ATCC 824. J. Mol. Microbiol. Biotechnol. 2000, 2:33-38.
34. Jarboe L.R., Grabar T.B., Yomano L.P., Shanmugan K.T., Ingram L.O. Development of ethanologenic bacteria. Adv. Biochem. Eng. Biotechnol. 2007, 108:237-261.
35. Jiang Y., Xu C., Dong F., Yang Y., Jiang W., Yang S. Disruption of the acetoacetate decarboxylase gene in solvent-producing Clostridium acetobutylicum increases the butanol ratio. Metab. Eng. 2009, 11:284-291.
36. Jones D.T., Woods D.R. Acetone-butanol fermentation revisited. Microbiol. Rev. 1986, 50:484-524.
37. Jones S.W., Paredes C.J., Tracy B., Cheng N., Sillers R., Senger R.S., Papoutsakis E.T. The transcriptional program underlying the physiology of clostridial sporulation. Genome Biol. 2008, 9:R114.
38. Kim B.H., Zeikus J.G. Specificity of alcohol dehydrogenase from Clostridium acetobutylicum ATCC 4259. J. Microbiol. Biotechnol. 1992, 2:268-272.
39. Kharkwal S., Karimi I.A., Chang M.W., Lee D.Y. Strain improvement and process development for biobutanol production. Rec. Pat. Biotechnol. 2009, 3:202-210.
40. la Grange D.C., den Haan R., van Zyl W.H. Engineering cellulolytic ability into bioprocessing organisms. Appl. Microbiol. Biotechnol. 2010, 87:1195-1208.
41. Lee S.Y., Park J.H., Jang S.H., Nielsen L.K., Kim J., Jung K.S. Fermentative butanol production by clostridia. Biotechnol. Bioeng. 2008, 101:209-228.
42. Lin Y., Tanaka S. Ethanol fermentation from biomass resources: current state and prospects. Appl. Microbiol. Biotechnol. 2006, 69:627-642.
43. Liu S., Qureshi N. How microbes tolerate ethanol and butanol. N. Biotechnol. 2009, 26:117-121.
44. Lütke-Eversloh, T., Bahl, H., 2011. Metabolic engineering of Clostridium acetobutylicum: recent advances to improve butanol production. Curr. Opin. Biotechnol., 10.1016/j.copbio.2011.01.011.
45. Madan V.K., Hillmer P., Gottschalk G. Purification and properties of NADP-dependent L(+)-3-hydroxybutyryl-CoA dehydrogenase from Clostridium kluyveri. Eur. J. Biochem. 1973, 32:51-56.
46. Mermelstein L.D., Papoutsakis E.T. In vivo methylation in Escherichia coli by the Bacillus subtilis phage phi3TI methyltransferase to protect plasmids from restriction upon transformation of Clostridium acetobutylicum ATCC 824. Appl. Environ. Microbiol. 1993, 59:1077-1081.
47. Monot F., Martin J.R., Petitdemange H., Gay R. Acetone and butanol production by Clostridium acetobutylicum in a synthetic medium. Appl. Environ. Microbiol. 1982, 44:1318-1324.
48. Mussatto S.I., Dragone G., Guimarães P.M., Silva J.P., Carneiro L.M., Roberto I.C., Vicente A., Domingues L., Teixeira J.A. Technological trends, global market, and challenges of bio-ethanol production. Biotechnol. Adv. 2010, 28:817-830.
49. Nicolaou S.A., Gaida S.M., Papoutsakis E.T. A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: from biofuels and chemicals, to biocatalysis and bioremediation. Metab. Eng. 2010, 12:307-331.
50. Nölling J., Breton G., Omelchenko M.V., Makarova K.S., Zeng Q., Gibson R., Lee H.M., Dubois J., Qiu D., Hitti J., et al. Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J. Bacteriol. 2001, 183:4823-4838.
51. Papoutsakis E.T. Engineering solventogenic clostridia. Curr. Opin. Biotechnol. 2008, 19:420-429.
52. Petitdemange H., Cherrier C., Raval R., Gay R. Regulation of the NADH and NADPH-ferredoxin oxidoreductases in clostridia of the butyric group. Biochim. Biophys. Acta 1976, 421:334-347.
53. Ren C., Gu Y., Hu S., Wu Y., Wang P., Yang Y., Yang C., Yang S., Jiang W. Identification and inactivation of pleiotropic regulator CcpA to eliminate glucose repression of xylose utilization in Clostridium acetobutylicum. Metab. Eng. 2010, 12:446-454.
54. 2 detoxification in Clostridium acetobutylicum. Microbiology 2009, 155:16-24.
55. Roos J.W., McLaughlin J.K., Papoutsakis E.T. The effect of pH on nitrogen supply, cell lysis, and solvent production in fermentations of Clostridium acetobutylicum. Biotechnol. Bioeng. 1985, 27:681-694.
56. Saerens S.M., Duong C.T., Nevoigt E. Genetic improvement of brewer's yeast: current state, perspectives and limits. Appl. Microbiol. Biotechnol. 2010, 86:1195-1212.
57. Sambrock J., Russell D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, NY, USA. 3rd Ed.
58. Sauer U., Dürre P. Differential induction of genes related to solvent formation during the shift from acidogenesis to solventogenesis in continuous culture of Clostridium acetobutylicum. FEMS Microbiol. Lett. 1995, 125:115-120.
59. Servinsky M.D., Kiel J.T., Dupuy N.F., Sund C.J. Transcriptional analysis of differential carbohydrate utilization by Clostridium acetobutylicum. Microbiology 2010, 156:3478-3491.
60. Sillers R., Chow A., Tracy B., Papoutsakis E.T. Metabolic engineering of the non-sporulating, non-solventogenic Clostridium acetobutylicum strain M5 to produce butanol without acetone demonstrate the robustness of the acid-formation pathways and the importance of the electron balance. Metab. Eng. 2008, 10:321-332.
61. Sillers R., Al-Hinai M.A., Papoutsakis E.T. Aldehyde-alcohol dehydrogenase and/or thiolase overexpression coupled with CoA transferase downregulation lead to higher alcohol titers and selectivity in Clostridium acetobutylicum fermentations. Biotechnol. Bioeng. 2008, 102:38-49.
62. Solomon B.D. Biofuels and sustainability. Ann. NY Acad. Sci. 2010, 1185:119-134.
63. Stim-Herndon K.P., Nair R.V., Papoutsakis E.T., Bennett G.N. Analysis of degenerate variants of Clostridium acetobutylicum ATCC 824. Anaerobe 1996, 2:11-18.
64. Thormann K., Feustel L., Lorenz K., Nakotte S., Dürre P. Control of butanol formation in Clostridium acetobutylicum by transcriptional activation. J. Bacteriol. 2002, 184:1966-1973.
65. Tummala S.B., Junne S.G., Papoutsakis E.T. Antisense RNA downregulation of coenzyme A transferase combined with alcohol-aldehyde dehydrogenase overexpression leads to predominantly alcohologenic Clostridium acetobutylicum fermentations. J. Bacteriol. 2003, 185:3644-3653.
66. Weber C., Farwick A., Benisch F., Brat D., Dietz H., Subtil T., Boles E. Trends and challenges in the microbial production of lignocellulosic bioalcohol fuels. Appl. Microbiol. Biotechnol. 2010, 87:1303-1315.
67. Youngleson J.S., Jones D.T., Woods D.R. Homology between hydroxybutyryl and hydroxyacyl coenzyme A dehydrogenase enzymes from Clostridium acetobutylicum fermentation and vertebrate fatty acid beta-oxidation pathways. J. Bacteriol. 1989, 171:6800-6807.
68. Zhao Y., Tomas C.A., Rudolph F.B., Papoutsakis E.T., Bennett G.N. Intracellular butyryl phosphate and acetyl phosphate concentrations in Clostridium acetobutylicum and their implications for solvent formation. Appl. Environ. Microbiol. 2005, 71:530-537.