A shift in the dominant phenotype governs the pH-induced metabolic switch of Clostridium acetobutylicumin phosphate-limited continuous cultures

Applied Microbiology and Biotechnology

Volumn 97, Issue 14, 2013, Pages 6451-6466

  Millat, Thomas ^a   Janssen, Holger ^a,d   Thorn, Graeme J ^b   King, John R ^b   Bahl, Hubert ^a   Fischer, Ralf Jörg ^a   Wolkenhauer, Olaf ^a,c  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c STELLENBOSCH UNIVERSITY   (South Africa)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Acetone butanol ethanol fermentation; Clostridium acetobutylicum; Continuous culture; Mathematical modelling; pH induced metabolic shift; Phenotypic switch

Indexed keywords

ACETONE-BUTANOL-ETHANOL FERMENTATION; CLOSTRIDIUM ACETOBUTYLICUM; CONTINUOUS CULTURE; ENZYMATIC ACTIVITIES; EXPERIMENTAL CONDITIONS; EXPRESSION PATTERNS; METABOLIC SHIFT; THEORETICAL STUDY;

ACETONE; ENZYME ACTIVITY; ETHANOL; FERMENTATION; MATHEMATICAL MODELS; POPULATION DYNAMICS;

METABOLISM;

ACETONE; ALCOHOL; ALCOHOL DEHYDROGENASE; BUTANOL; PHOSPHATE;

ACETONE; BACTERIUM; ENZYME ACTIVITY; ETHANOL; FERMENTATION; METABOLISM; NUMERICAL MODEL; PH; PHENOTYPE; PHOSPHATE; POPULATION DYNAMICS; PROTEOMICS; SOLVENT;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIUM CULTURE; CLOSTRIDIUM ACETOBUTYLICUM; CONTINUOUS CULTURE; ENZYME ACTIVITY; FERMENTATION; INTRACELLULAR SPACE; METABOLOMICS; NONHUMAN; OPTICAL DENSITY; PH; PHENOTYPE; PROTEIN EXPRESSION; PROTEOMICS; TRANSCRIPTOMICS;

ACETONE; ACIDS; BUTANOLS; CLOSTRIDIUM ACETOBUTYLICUM; CULTURE MEDIA; ETHANOL; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN-ION CONCENTRATION; PHENOTYPE; PHOSPHATES;

CLOSTRIDIUM; CLOSTRIDIUM ACETOBUTYLICUM;

EID: 84879840909     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-4860-7     Document Type: Article

References (66)

1. Aguilar C, Vlamakis H, Losick R, Kolter R (2007) Thinking about Bacillus subtilis as a multicellular organism. Curr Opin Microbiol 10(6):638-643
2. Al-Hinai M, Fast A, Papoutsakis E (2012) A novel system for efficient isolation of double-crossover allelic exchange mutants in Clostridium enabling markerless chromosomal gene deletions and DNA integration. Appl Environ Microbiol 78(22):8112-8121
3. Andersch W, Bahl H, Gottschalk G (1983) Level of enzymes involved in acetate, butyrate, acetone and butanol formation by Clostridium acetobutylicum. Appl Microbiol Biotechnol 18(6):327-332
4. Atkinson S, Williams P (2009) Quorum sensing and social networking in the microbial world. J Soc Roy Interf 6(40):959-978
5. Bahl H, Andersch W, Gottschalk G (1982) Continuous production of acetone and butanol by Clostridium acetobutylicum in a two-stage phosphate limited chemostat. Appl Microbiol Biotechnol 15(4):201-205
6. Balaban N, Merrin J, Chait R, Kowalik L, Leibler S (2004) Bacterial persistence as a phenotypic switch. Science 305(5690):1622-1625
7. Boynton Z, Bennett G, Rudolph F (1996) Cloning, sequencing, and expression of genes encoding phosphotransacetylase and acetate kinase from Clostridium acetobutylicum ATCC 824. Appl Environ Microbiol 62(8):2758-2766
8. Cardoso M, Salcedo R, Feyo de Azevedo S (1996) The simplex-simulated annealing approach to continuous non-linear optimization. Comput Chem Eng 20(9):1065-1080
9. Clarke K, Hansford G, Jones D (1988) Nature and significance of oscillatory behavior during solvent production by Clostridium acetobutylicum in continuous culture. Biotechnol Bioeng 32(4):538-544
10. Cooksley C, Zhang Y, Wang H, Redl S, Winzer K, Minton N (2012) Targeted mutagenesis of the Clostridium acetobutylicum acetone-butanol-ethanol fermentation pathway. Metab Eng 14(6):630-641
11. de Jong I, Veening JW, Kuipers O (2010) Heterochronic phosphorelay gene expression as a source of heterogeneity in Bacillus subtilis spore formation. J Bacteriol 192(8):2053-2067
12. Desai R, Harris L, Welker N, Papoutsakis E (1999) Metabolic flux analysis elucidates the importance of the acid-formation pathways in regulating solvent production by Clostridium acetobutylicum. Metab Eng 1(3):206-213
13. Dürre P (2005) Formation of solvents in Clostridia. In: Handbook on Costridia, pp 671-693
14. Dürre P, Fischer RJ, Kuhn A, Lorenz K, Schreiber W, Stürzenhofecker B, Ullmann S, Winzer K, Sauer U (1995) Solventogenic enzymes of Clostridium acetobutylicum: catalytic properties, genetic organization, and transcriptional regulation. FEMS Microbiol Rev 17(3):251-262
15. Fiedler T, Mix M, Meyer U, Mikkat S, Glocker M, Bahl H, Fischer RJ (2008) The two-component system PhoPR of Clostridium acetobutylicum is involved in phosphate-dependent gene regulation. J Bacteriol 190(20):6559-6567
16. Fischer RJ, Oehmcke S, Meyer U, Mix M, Schwarz K, Fiedler T, Bahl H (2006) Transcription of the pst Operon of Clostridium acetobutylicum is dependent on phosphate concentration and pH. J Bacteriol 188(15):5469-5478
17. Fontaine L, Meynial-Salles I, Girbal L, Yang X, Croux C, Soucaille P (2002) 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 184(3):821-830
18. Gottwald M, Gottschalk G (1985) The internal pH of Clostridium acetobutylicum and its effect on the shift from acid to solvent formation. Arch Microbiol 143(1):42-46
19. Green E (2011) Fermentative production of butanol - the industrial perspective. Curr Opin Biotechnol 22(3):337-343
20. Grimmler C, Janssen H, Krauße D, Fischer R J, Bahl H, Dürre P, Liebl W, Ehrenreich A (2011) Genome-wide gene expression analysis of the switch between acidogenesis and solventogenesis in continuous cultures of Clostridium acetobutylicum. J Mol Microbiol Biotechnol 20(1):1-15
21. Grupe H, Gottschalk G (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(12):3896-3902
22. Hartmanis M, Gatenbeck S (1984) Intermediary metabolism in Clostridium acetobutylicum: levels of enzymes involved in the formation of acetate and butyrate. Appl Environ Microbiol 47(6):1277-1283
23. Hartmanis M, Klason T, Gatenbeck S (1984) Uptake and activation of acetate and butyrate in Clostridium acetobutylicum. Appl Microbiol Biotechnol 20(1):66-71
24. Haus S, Jabbari S, Millat T, Janssen H, Fischer RJ, Bahl H, King J, Wolkenhauer O (2011) A systems biology approach to investigate the effect of pH-induced gene regulation on solvent production by Clostridium acetobutylicum in continuous culture. BMC Syst Biol 5(1):10
25. Ho MC, Menetret JF, Tsuruta H, Allen K (2009) The origin of the electrostatic perturbation in acetoacetate decarboxylase. Nature 459(7245):393-397
26. Hooshangi S, Bentley W (2008) From unicellular properties to multicellular behavior: bacteria quorum sensing circuitry and applications. Curr Opin Biotechnol 19(6):550-555
27. Hoskisson P, Hobbs G (2005) Continuous culture - making a comeback. Microbiol 151(10):3153-3159
28. Jang YS, Lee J, Malaviya A, Seung DY, Cho JH, Lee SY (2012) Butanol production from renewable biomass: rediscovery of metabolic pathways and metabolic engineering. Biotechnol J 7:186-198
29. Janssen H, Döring C, Ehrenreich A, Voigt B, Hecker M, Bahl H, Fischer RJ (2010) Appl Microbiol Biotechnol 87(6):2209-2226
30. Janssen H, Grimmler C, Ehrenreich A, Bahl H, Fischer RJ (2012) A transcriptional study of acidogenic chemostat cells of Clostridium acetobutylicum - solvent stress caused by a transient n-butanol pulse. J Biotechnol 161(3):354-365
31. Janssen H, Fiedler T, Schwarz K, Bahl H, Fischer RJ (2013) Supporting systems biology of Clostridium acetobutylicum by proteome analysis. In: Systems biology of Clostridium, pp 49-74
32. Jeon S, Lee J, Kim S, Kim S, Han S (2012) Analysis of selective, high protein-protein binding interaction of cohesin-dockerin complex using biosensing methods. Biosens Bioelectron 35(1):382-389
33. Jones D, Woods D (1986) Acetone-butanol fermentation revisited. Microbiol Rev 50(4):484-524
34. Keene J (2010) The global dynamics of RNA stability orchestrates responses to cellular activation. BMC Biol 8(1):95
35. Kuehne S, Minton N (2012) ClosTron-mediated engineering of Clostridium. Bioengineered 3(4):247-254
36. Kussell E, Kishony R, Balaban N, Leibler S (2005) Bacterial persistence a model of survival in changing environments. Genetics 169(4):1807-1814
37. Lee J, Yun H, Feist A, Palsson B, Lee S (2008) Genome-scale reconstruction and in silico analysis of the Clostridium acetobutylicum ATCC 824 metabolic network. Appl Microbiol Biotechnol 80(5):849-862
38. Lehmann D (2011) Lütke-Eversloh, T. Switching Clostridium acetobutylicum to an ethanol producer by disruption of the butyrate/butanol fermentative pathway. Metab Eng 13(5):464-473
39. Lehmann D, Hönicke D, Ehrenreich A, Schmidt M, Weuster-Botz D, Bahl H, Lütke-Eversloh T (2012) Modifying the product pattern of Clostridium acetobutylicum. Appl Microbiol Biotechnol 93(1):1-12
40. Linhova M, Branska B, Patakova P, Lipovsky J, Fribert P, Rychtera M, Melzoch K (2012) Rapid flow cytometric method for viability determination of solventogenic Clostridia. Folia Microbiol 57(4):307-311
41. Lütke-Eversloh T, Bahl H (2011) Metabolic engineering of Clostridium acetobutylicum: recent advances to improve butanol production. Curr Opin Biotechnol 22(5):634-647
42. Maier T, Schmidt A, Güell M, Kühner S, Gavin AC, Aebersold R, Serrano L (2011) Quantification of mRNA and protein and integration with protein turnover in a bacterium. Mol Syst Biol 7:511
43. McAnulty M, Yen J, Freedman B, Senger R (2012) Genome-scale modeling using flux ratio constraints to enable metabolic engineering of clostridial metabolism in silico. BMC Syst Biol 6(1):42
44. Millat T, Janssen H, Bahl H, Fischer RJ, Wolkenhauer O (2013) Integrative modelling of pH-dependent enzyme activity and transcriptomic regulation of the acetone-butanol-ethanol fermentation of Clostridium acetobutylicum in continuous culture. Microbial Biotechnol. 10.1111/1751-7915.12033
45. Milne C, Eddy J, Raju R, Ardekani S, Kim PJ, Senger R, Jin YS, Blaschek H, Price N (2011) Metabolic network reconstruction and genome-scale model of butanol-producing strain Clostridium beijerinckii NCIMB 8052. BMC Syst Biol 5(1):130
46. Mitchell W (1997) Physiology of carbohydrate to solvent conversion by Clostridia. Adv Microb Physiol 39:31-130
47. Papoutsakis E (1984) Equations and calculations for fermentations of butyric acid bacteria. Biotechnol Bioeng 26(2):174-187
48. Petersen D, Bennett G (1990) Purification of acetoacetate decarboxylase from Clostridium acetobutylicum ATCC 824 and cloning of the acetoacetate decarboxylase gene in Escherichia coli. Appl Environ Microbiol 56(11):3491-3498
49. Petersen D, Welch R, Rudolph F, Bennett G (1991) Molecular cloning of an alcohol (butanol) dehydrogenase gene cluster from Clostridium acetobutylicum ATCC 824. J Bacteriol 173(5):1831-1834
50. Press W, Teukolsky S, Vetterling W, Flannery B (2007) Numerical recipes in C - the art of scientific computing, 3rd edn. Cambridge University Press, Cambridge
51. Sauer U, Dürre P (1995) Differential induction of genes related to solvent formation during the shift from acidogenesis to solventogenesis in continuous culture of Clostridium acetobutylicum. FEMS Microbiol Lett 125(1):115-120
52. Schaffer S, Isci N, Zickner B, Dürre P (2002) Changes in protein synthesis and identification of proteins specifically induced during solventogenesis in Clostridium acetobutylicum. Electrophoresis 23(1):110-121
53. Schertzer J, Boulette M, Whiteley M (2009) More than a signal: non-signaling properties of quorum sensing molecules. Trends Microbiol 17(5):189-195
54. Senger R, Papoutsakis E (2008) Genome-scale model for Clostridium acetobutylicum. Part I: metabolic network resolution and analysis. Biotechnol Bioeng 101(5):1036-1052
55. Shapiro J (1988) Bacteria as multicellular organisms. Sci Am 258:82-89
56. Shapiro J (1998) Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52(1):81-104
57. Shinto H, Tashiro Y, Yamashita M, Kobayashi G, Sekiguchi T, Hanai T, Kuriya Y, Okamoto M, Sonomoto K (2007) Kinetic modeling and sensitivity analysis of acetone-butanol-ethanol production. J Biotechnol 131(1):45-56
58. Straub L (2011) Beyond the transcripts: what controls protein variation? PLoS Biol 9(9):e1001146
59. Tangney M, Mitchell W (2007) Characterisation of a glucose phosphotransferase system in Clostridium acetobutylicum ATCC 824. Appl Microbiol Biotechnol 74(2):398-405
60. Tracy B, Gaida S, Papoutsakis E (2008) Development and application of flow-cytometric techniques for analyzing and sorting endospore-forming Clostridia. Appl Environ Microbiol 74(24):7497-7506
61. Veening JW, Stewart E, Berngruber T, Taddei F, Kuipers O, Hamoen L (2008) Bet-hedging and epigenetic inheritance in bacterial cell development. Proc Natl Acad Sci USA 105(11):4393-4398
62. Verhamme D, Kiley T, Stanley-Wall N (2007) DegU co-ordinates multicellular behaviour exhibited by Bacillus subtilis. Mol Microbiol 65(2):554-568
63. Walter K, Bennett G, Papoutsakis E (1992) Molecular characterization of two Clostridium acetobutylicum ATCC 824 butanol dehydrogenase isozyme genes. J Bacteriol 174(22):7149-7158
64. Welch R, Rudolph F, Papoutsakis E (1989) Purification and characterization of the NADH-dependent butanol dehydrogenase from Clostridium acetobutylicum (ATCC 824). Arch Biochem Biophys 273(2):309-318
65. Wiesenborn D, Rudolph F, Papoutsakis E (1989a) Coenzyme A transferase from Clostridium acetobutylicum ATCC 824 and its role in the uptake of acids. Appl Environ Microbiol 55(2):323-329
66. Wiesenborn D, Rudolph F, Papoutsakis E (1989b) Phosphotransbutyrylase from Clostridium acetobutylicum ATCC 824 and its role in acidogenesis. Appl Environ Microbiol 55(2):317-322