Metabolome remodeling during the acidogenic-solventogenic transition in clostridium acetobutylicum

Applied and Environmental Microbiology

Volumn 77, Issue 22, 2011, Pages 7984-7997

  Amador Noguez, Daniel ^a   Brasg, Ian A ^a   Feng, Xiao Jiang ^a   Roquet, Nathaniel ^a   Rabinowitz, Joshua D ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A; ACIDOGENESIS; BIOMASS PRODUCTIONS; CARBON FLUXES; CLOSTRIDIUM ACETOBUTYLICUM; EXPONENTIAL GROWTH; GLYCOLYTIC INTERMEDIATE; INTRACELLULAR LEVELS; ISOTOPE TRACERS; LOW ENERGIES; METABOLIC CHANGES; METABOLIC FLUX; METABOLITE CONCENTRATIONS; METABOLOMES; METABOLOMICS; NAD(P)H; NUCLEOTIDE TRIPHOSPHATES; PYRUVATES; QUANTITATIVE FLUX; REDUCING POWER; SOLVENT PRODUCTION; SOLVENTOGENESIS; TCA CYCLE; TRICARBOXYLIC ACIDS;

ACETONE; AMINO ACIDS; CARBON; CLOSTRIDIUM; ETHANOL; FERMENTATION; FORESTRY; ISOTOPES; METABOLITES; NUCLEOTIDES; ORGANIC SOLVENTS; VOLATILE FATTY ACIDS;

METABOLISM;

ACETIC ACID DERIVATIVE; ACETONE; ALCOHOL; BUTANOL; BUTYRIC ACID DERIVATIVE;

AMINO ACID; BACTERIUM; BIOFUEL; BIOMASS POWER; CARBON FLUX; CARBOXYLIC ACID; FERMENTATION; METABOLISM; METABOLITE; NUMERICAL MODEL; RENEWABLE RESOURCE; TRACER;

ARTICLE; CHEMISTRY; CLOSTRIDIUM ACETOBUTYLICUM; CYTOSOL; ENERGY METABOLISM; FERMENTATION; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METABOLOME;

ACETATES; ACETONE; BUTANOLS; BUTYRATES; CLOSTRIDIUM ACETOBUTYLICUM; CYTOSOL; ENERGY METABOLISM; ETHANOL; FERMENTATION; GENE EXPRESSION REGULATION, BACTERIAL; METABOLOME;

EID: 83055188821     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.05374-11     Document Type: Article

References (44)

1. Alsaker, K. V., and E. T. Papoutsakis. 2005. Transcriptional program of early sporulation and stationary-phase events in Clostridium acetobutylicum. J. Bacteriol. 187:7103-7118.
2. Amador-Noguez, D., et al. Systems-level metabolic flux profiling elucidates a complete, bifurcated tricarboxylic acid cycle in Clostridium acetobutylicum. J. Bacteriol. 192:4452-4461.
3. Baer, S. H., H. P. Blaschek, and T. L. Smith. 1987. Effect of butanol challenge and temperature on lipid composition and membrane fluidity of butanol-tolerant Clostridium acetobutylicum. Appl. Environ. Microbiol. 53: 2854-2861.
4. Baer, S. H., D. L. Bryant, and H. P. Blaschek. 1989. Electron spin resonance analysis of the effect of butanol on the membrane fluidity of intact cells of Clostridium acetobutylicum. Appl. Environ. Microbiol. 55:2729-2731.
5. Bajad, S. U., et al. 2006. Separation and quantitation of water soluble cellular metabolites by hydrophilic interaction chromatography-tandem mass spectrometry. J. Chromatogr. A 1125:76-88.
6. Bennett, B. D., et al. 2009. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol. 5:593-599.
7. Bennett, B. D., J. Yuan, E. H. Kimball, and J. D. Rabinowitz. 2008. Absolute quantitation of intracellular metabolite concentrations by an isotope ratiobased approach. Nat. Protoc. 3:1299-1311.
8. Boer, V. M., C. A. Crutchfield, P. H. Bradley, D. Botstein, and J. D. Rabinowitz. Growth-limiting intracellular metabolites in yeast growing under diverse nutrient limitations. Mol. Biol. Cell 21:198-211.
9. Boynton, Z. L., G. N. Bennett, and F. B. Rudolph. 1994. Intracellular concentrations of coenzyme A and its derivatives from Clostridium acetobutylicum ATCC 824 and their roles in enzyme regulation. Appl. Environ. Microbiol. 60:39-44.
10. Carrieri, D., et al. 2009. Identification and quantification of water-soluble metabolites by cryoprobe-assisted nuclear magnetic resonance spectroscopy applied to microbial fermentation. Magn. Reson. Chem. 47(Suppl. 1):S138- S146.
11. Crown, S. B., et al. Resolving the TCA cycle and pentose-phosphate pathway of Clostridium acetobutylicum ATCC 824: isotopomer analysis, in vitro activities and expression analysis. Biotechnol. J. 6:300-305.
12. Dürre, P. 2005. Handbook on clostridia. Taylor & Francis, Boca Raton, FL.
13. Durre, P., et al. 2002. Transcriptional regulation of solventogenesis in Clostridium acetobutylicum. J. Mol. Microbiol. Biotechnol. 4:295-300.
14. Eisen, M. B., P. T. Spellman, P. O. Brown, and D. Botstein. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 95:14863-14868.
15. Feng, X. J., et al. 2004. Optimizing genetic circuits by global sensitivity analysis. Biophys. J. 87:2195-2202.
16. Feng, X. J., and H. Rabitz. 2004. Optimal identification of biochemical reaction networks. Biophys. J. 86:1270-1281.
17. Girbal, L., and P. Soucaille. 1994. Regulation of Clostridium acetobutylicum metabolism as revealed by mixed-substrate steady-state continuous cultures: role of NADH/NAD ratio and ATP pool. J. Bacteriol. 176:6433-6438.
18. Green, E. M., et al. 1996. Genetic manipulation of acid formation pathways by gene inactivation in Clostridium acetobutylicum ATCC 824. Microbiology 142(Pt. 8):2079-2086.
19. Grupe, H., and G. Gottschalk. 1992. Physiological events in Clostridium acetobutylicum during the shift from acidogenesis to solventogenesis in continuous culture and presentation of a model for shift induction. Appl. Environ. Microbiol. 58:3896-3902.
20. Harris, L. M., R. P. Desai, N. E. Welker, and E. T. Papoutsakis. 2000. Characterization of recombinant strains of the Clostridium acetobutylicum butyrate kinase inactivation mutant: need for new phenomenological models for solventogenesis and butanol inhibition? Biotechnol. Bioeng. 67:1-11.
21. Huang, H., H. Liu, and Y. R. Gan. Genetic modification of critical enzymes and involved genes in butanol biosynthesis from biomass. Biotechnol. Adv. 28:651-657.
22. Hutkins, R. W., and E. R. Kashket. 1986. Phosphotransferase activity in Clostridium acetobutylicum from acidogenic and solventogenic phases of growth. Appl. Environ. Microbiol. 51:1121-1123.
23. Hwang, T. L., and A. J. Shaka. 1995. Water suppression that works: excitation sculpting using arbitrary wave-forms and pulsed-field gradients. J. Magn. Reson. 112:275-279.
24. Janssen, H., et al. A proteomic and transcriptional view of acidogenic and solventogenic steady-state cells of Clostridium acetobutylicum in a chemostat culture. Appl. Microbiol. Biotechnol. 87:2209-2226.
25. Jiang, Y., et al. 2009. Disruption of the acetoacetate decarboxylase gene in solvent-producing Clostridium acetobutylicum increases the butanol ratio. Metab. Eng. 11:284-291.
26. Jones, S. W., et al. 2008. The transcriptional program underlying the physiology of clostridial sporulation. Genome Biol. 9:R114.
27. Kimball, E., and J. D. Rabinowitz. 2006. Identifying decomposition products in extracts of cellular metabolites. Anal. Biochem. 358:273-280.
28. Kraml, C. M., D. Zhou, N. Byrne, and O. McConnell. 2005. Enhanced chromatographic resolution of amine enantiomers as carbobenzyloxy derivatives in high-performance liquid chromatography and supercritical fluid chromatography. J. Chromatogr. A 1100:108-115.
29. LePage, C., M. Fayolle, M. Hermann, and J. P. Vandecasteele. 1987. Changes in membrane-lipid composition of Clostridium acetobutylicum during acetone butanol fermentation: effects of solvents, growth temperature and pH. J. Gen. Microbiol. 133:103-110.
30. Lu, W., B. D. Bennett, and J. D. Rabinowitz. 2008. Analytical strategies for LC-MS-based targeted metabolomics. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 871:236-242.
31. Lu, W., et al. Metabolomic analysis via reversed-phase ion-pairing liquid chromatography coupled to a stand alone OrbiTrap mass spectrometer. Anal. Chem. 82:3212-3221.
32. Mansilla, M. C., L. E. Cybulski, D. Albanesi, and D. de Mendoza. 2004. Control of membrane lipid fluidity by molecular thermosensors. J. Bacteriol. 186:6681-6688.
33. Monot, F., J. Engasser, and H. Petitdemange. 1984. Influence of pH and undissociated butyric acid on the production of acetone and butanol in batch cultures of Clostridium acetobutylicum. Appl. Microbiol. Biotechnol. 19:422-426.
34. Monot, F., J. R. Martin, H. Petitdemange, and R. Gay. 1982. Acetone and butanol production by Clostridium acetobutylicum in a synthetic medium. Appl. Environ. Microbiol. 44:1318-1324.
35. Munger, J., et al. 2008. Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat. Biotechnol. 26:1179-1186.
36. Rabinowitz, J. D., and E. Kimball. 2007. Acidic acetonitrile for cellular metabolome extraction from Escherichia coli. Anal. Chem. 79:6167-6173.
37. Rao, G., and R. Mutharasan. 1989. NADH levels and solventogenesis in Clostridium acetobutylicum: new insights through culture fluorescence. Appl. Biochem. Biotechnol. 30:59-66.
38. Saldanha, A. J. 2004. Java Treeview: extensible visualization of microarray data. Bioinformatics 20:3246-3248.
39. Schaffer, S., N. Isci, B. Zickner, and P. Durre. 2002. Changes in protein synthesis and identification of proteins specifically induced during solventogenesis in Clostridium acetobutylicum. Electrophoresis 23:110-121.
40. Terracciano, J. S., and E. R. Kashket. 1986. Intracellular conditions required for initiation of solvent production by Clostridium acetobutylicum. Appl. Environ. Microbiol. 52:86-91.
41. Vollherbst-Schneck, K., J. A. Sands, and B. S. Montenecourt. 1984. Effect of butanol on lipid composition and fluidity of Clostridium acetobutylicum ATCC 824. Appl. Environ. Microbiol. 47:193-194.
42. Yuan, J., B. D. Bennett, and J. D. Rabinowitz. 2008. Kinetic flux profiling for quantitation of cellular metabolic fluxes. Nat. Protoc. 3:1328-1340.
43. Yuan, J., et al. 2009. Metabolomics-driven quantitative analysis of ammonia assimilation in Escherichia coli. Mol. Syst. Biol. 5:302.
44. Zhao, Y., C. A. Tomas, F. B. Rudolph, E. T. Papoutsakis, and G. N. Bennett. 2005. Intracellular butyryl phosphate and acetyl phosphate concentrations in Clostridium acetobutylicum and their implications for solvent formation. Appl. Environ. Microbiol. 71:530-537.