Control of carbon flux through enzymes of central and intermediary metabolism during growth of Escherichia coli on acetate

Current Opinion in Microbiology

Volumn 9, Issue 2, 2006, Pages 173-179

  El Mansi, Mansi ^a   Cozzone, Alain J ^b   Shiloach, Joseph ^c   Eikmanns, Bernhard J ^d  

^a EDINBURGH NAPIER UNIVERSITY   (United Kingdom)

^b UNIVERSITÉ DE LYON   (France)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d UNIVERSITY OF ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ACETYL COENZYME A; ACETYL COENZYME A SYNTHETASE; COENZYME A; GLYOXYLIC ACID; ISOCITRIC ACID; OXOGLUTARATE DEHYDROGENASE; PHOSPHATE ACETYLTRANSFERASE;

AEROBIC METABOLISM; BACTERIAL GROWTH; BACTERIAL METABOLISM; CITRIC ACID CYCLE; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; ENZYME SYNTHESIS; ESCHERICHIA COLI; GROWTH RATE; NONHUMAN; REVIEW;

ACETATES; ACETYL COENZYME A; CARBON; CULTURE MEDIA; ENZYME INHIBITORS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GLYOXYLATES; ISOCITRATE DEHYDROGENASE; ISOCITRATE LYASE; ISOCITRATES; KETOGLUTARATE DEHYDROGENASE COMPLEX; PHOSPHATE ACETYLTRANSFERASE; PHOSPHORYLATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 33645857669     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2006.02.002     Document Type: Review

References (41)

1. McCleary W.R., Stock J.B., and Ninfa J. Is acetyl phosphate a global signal in Escherichia coli?. J Bacteriol 175 (1993) 2793-2798
2. Wanner B.L. Gene regulation by phosphate in enteric bacteria. J Cell Biochem 51 (1993) 47-54
3. Pruss B.M. Acetyl phosphate and the phosphorylation of OmpR arc involved in the regulation of the cell division rate in Escherichia coli. Arch Microbiol 170 (1998) 141-146
4. Prohinar P., Forst S.A., Reede D., Mandic-Mulec I., and Weiss J. OmpR-dependent and OMR-independent responses of Escherichia coli to sublethal attack by the neutrophil bactericidal/permeability increasing protein. Mol Microbiol 43 (2002) 1493-1504
5. Wolfe A.J., Chang D.-E., Walker J.D., Seitz-Partridge J.E., Vidaurri M.D., Lang C.F., Pruss B.M., Henk M.C., Larkin J.C., and Conway T. Evidence that acetyl phosphate functions as a global signal during biofilm development. Mol Microbiol 48 (2003) 977-988. An excellent study in which the authors provide conclusive support for the role of the global regulator acetyl phosphate in biofilm formation.
6. El-Mansi M. Flux to acetate and lactate excretions in industrial fermentations: physiological and biochemical implications. J Ind Microbiol Biotechnol 31 (2004) 295-300. This study argues that flux to acetate and to lactate excretions are not merely a reflection of metabolite overflow but, rather, serve certain biochemical and physiological functions.
7. Wolfe A.J. The acetate switch. Microbiol Mol Biol Rev 69 (2005) 12-50. This extensive, yet elegant, review of the acetate switch is a must read for all researchers interested in acetate metabolism. In addition to describing acetogenesis, acetate assimilation and the possible role of acetyl phosphate as a global regulator of cellular metabolism, it also eloquently describes the mechanism which regulates transcription from the complex promoter of acs, the structural gene encoding the AMP-forming acetyl CoA synthase.
8. El-Mansi M. Free-CoA mediated regulation of intermediary and central metabolism: an hypothesis, which accounts for the excretion of α-ketoglutarate during growth of Escherichia coli on acetate. Res Microbiol 156 (2005) 874-879. In this study the author proposed that partition of carbon flux at the level of HS-CoA between PTA and α-KGDH, and at the level of isocitrate between isocitrate dehydrogenase and isocitrate lyase, are regulated in a precise way that facilitates high intracellular levels of isocitrate and the operation of the glyoxylate bypass.
9. Cozzone A.J., and El-Mansi E.M.T. Control of isocitrate dehydrogenase catalytic activity in Escherichia coli by protein phosphorylation. J Mol Microbiol Biotechnol 9 (2005) 132-146. In this study the authors illustrated reversible phosphorylation, and its role in bringing about the reversible inactivation of ICDH in E. coli and related organisms.
10. Guest J.R., and Russell G.C. Complexes and complexities of the citric acid cycle in Escherichia coli. Curr Top Cell Regul 33 (1992) 231-247
11. Guest J.R. Oxygen regulated gene expression in Escherichia coli. J Gen Microbiol 138 (1992) 2253-2263
12. Guest J.R., Abdel-Hamid A.M., Auger G.A., Cunnigham L., Henderson R.A., Machado R.S., and Attwood M.M. Physiological effects of replacing the PDH complex of E. coli by genetically engineered variants or by pyruvate oxidase. In: Frank Gordon, Mulchand S., and Patel (Eds). Thiamine: catalytic mechanisms and role in normal and disease states (2004), Marcel Dekker Inc, New York. 0-8247-4062-9 389-407. In this excellent review the authors described the physiological consequences of replacing pyruvate dehydrogenase with genetically-modified variants or with pyruvate oxidase. Among the many findings reported is that loss of flux through pyruvate oxidase was accompanied by a 15-20% drop in growth rate, growth yield and efficiency of carbon conversion to biomass, thus enforcing the view that 'energy is not the sole criterion in defining growth efficiency'.
13. Abde-Hamid A.M., Attwood M.M., and Guest J.R. Pyruvate oxidase contributes to the aerobic growth efficiency of Escherichia coli. Microbiology 147 (2001) 1483-1498
14. Phue J.-N., and Shiloach J. Impact of dissolved oxygen concentration on acetate accumulation and physiology of E. coli BL21, evaluating transcription levels of key genes at different dissolved oxygen conditions. Metab Eng 7 (2005) 353-363. In this paper, evidence is provided that pyruvate oxidase is expressed during log phase when oxygen is limited, even though it is a stationary phase induced enzyme.
15. Brasen C., and Schonheit P. Unusual ADP-forming acetyl-coenzyme A synthetases from the mesophillic euryarchaeon Haloarcula marismortui and from the hyperthermophilic crenarchaeon Pyrobaculum aerophilum. Arch Microbiol 182 (2004) 277-287. In this study, the authors reported the discovery of novel ACSs with unique catalytic features; which might be of biotechnological interest.
16. Brasen C., and Schonheit P. Regulation of acetate and acetyl-CoA converting enzymes during growth on acetate and/or glucose in the halophilic archaeon Haloarcula marismortui. FEMS Microbiol Lett 241 (2004) 21-26. In this study the authors provided evidence that acetate excretion was catalysed through the activity of an inducible ADP-forming ACS whereas acetate utilization and its activation to acetyl CoA was achieved through the activity of the AMP-forming ACS.
17. Shin S., Song S.G., Lee D.S., Pan L.G., and Park C. Involvement of iclR and rpoS in the induction of acs, the gene for acetyl CoA synthetase of Escherichia coli K12. FEMS Microbiol Lett 146 (1997) 103-108
18. Oh M.-K., Rohlin L., Kao K.C., and Liao J.C. Global expression profiling of acetate-grown Escherichia coli. J Biol Chem 277 (2002) 13175-13183
19. Aoshima M., Ishii M., Yamagishi A., Oshima T., and Igarashi Y. Metabolic characteristics of an isocitrate dehydrogenase defective derivative of Escherichia coli BL21(DE3). Biotechnol Bioeng 84 (2003) 732-737
20. Phue J.-N., Noronha S.B., Hattacharyya R., Wolfe A.J., and Shiloach J. Glucose metabolism at high density growth of E. coli B and E. coli K: differences in metabolic pathways are responsible for efficient glucose utilization in E coli B as determined by microarrays and Northern blot analyses. Biotechnol Bioeng 90 (2005) 805-820. In this study the authors revealed that FruR, a major regulatory molecule that controls the expression of ppsA (phosphoenolpyruvate synthetase) and aceBAK in E. coli, might also regulate the expression of acs.
21. Holms W.H. Control of flux through the citric acid cycle and the glyoxylate bypass in Escherichia coli. Biochem Soc Symp 54 (1987) 17-31
22. Cozzone A.J. Regulation of acetate metabolism by protein phosphorylation in enteric bacteria. Annu Rev Microbiol 52 (1998) 127-164
23. Hofmeyr J.-H.S., Kacser H., and Merwe K.J. Metabolic control analysis of moiety-conserved cycles. Eur J Biochem 155 (1986) 631-641
24. Koshland Jr. D.E. Switches, thresholds and ultrasensitivity. Trends Biochem Sci 12 (1987) 225-229
25. Gerstmeir R., Wendisch V.F., Schnicke S., Ruan H., Farwick M., Reinscheid D., and Eikmanns B.J. Acetate metabolism and its regulation in Corynebacterium glutamicum. J Biotechnol 104 (2003) 99-122
26. Eikmanns B.J. Central metabolic pathways of Corynebacterium glutamicum: tricarboxylic cycle and anaplerotic reactions. In: Eggeling L., and Bott M. (Eds). Handbook of Corynebacterium glutamicum (2005), CRC Press, Boca Raton 241-276. This book chapter summarizes what is known about the TCA cycle, the glyoxylate cycle and the related pathways at the PEP-pyruvate-oxaloacetate node of C. glutamicum. Moreover, it highlights the characteristic features of these pathways in C. glutamicum.
27. 13C-labelled acetate and glucose using GC-MS and powerful flux calculation method. J Biotechnol 101 (2003) 101-117
28. Zhao J., Baba T., Mori H., and Shimizu K. Effect of zwf gene knockout on the metabolism of Escherichia coli grown on glucose or acetate. Metab Eng 6 (2004) 164-174. In this study, the authors showed that zwf deletion was accompanied by significant differences in the distribution of carbon flux among various enzymes of central metabolism on one hand and the efficiency of carbon conversion to biomass on the other.
29. El-Mansi E.M.T., Nimmo H.G., and Holms W.H. The role of isocitrate in control of the phosphorylation of isocitrate dehydrogenase in Escherichia coli ML308. FEBS Lett 183 (1985) 251-255
30. Holms H. Flux analysis and control of the central metabolic pathways in Escherichia coli. FEMS Microbiol Rev 19 (1996) 85-116
31. Chohnan S., Furukawa H., Fujio T., Nishihara H., and Takamura Y. Changes in the size and composition of intracellular pools of nonesterified coenzyme A thioesters in aerobic and facultatively anaerobic bacteria. Appl Environ Microbiol 63 (1997) 553-560
32. Wendisch V.F., de Graaf A.A., Sahm H., and Eikmanns B.J. Quantitative determination of metabolic fluxes during coutilization of two carbon sources: Comparative analyses with Corynebacterium glutamicum during growth on acetate and/or glucose. J Bacteriol 182 (2000) 3088-3096
33. Gerstmeir R., Cramer A., Dangel P., Schaffer S., and Eikmanns B.J. RamB, a novel transcriptional regulator of genes involved in acetate metabolism of Corynebacterium glutamicum. J Bacteriol 186 (2004) 2798-2809. This study describes the identification and characterization of a, to date unknown, repressor protein involved in the control of the acetate metabolism of C. glutamicum.
34. LaPorte D.C. The isocitrate dehydrogenase phosphorylation cycle: regulation and enzymology. J Cell Biochem 51 (1993) 14-18
35. El-Mansi E.M.T., Dawson G.C., and Bryce C.F.A. Steady-state modelling of metabolic flux between the tricarboxylic acid cycle and the glyoxylate bypass in Escherichia coli. Comput Appl Biosci 10 (1994) 295-299
36. El-Mansi E.M.T. Control of metabolic interconversion of isocitrate dehydrogenase between the catalytically active and inactive forms in Escherichia coli. FEMS Microbiol Lett 166 (1998) 333-339
37. Cortay J.C., Bleicher F., Rieul C., Reeves H.C., and Cozzone A.J. Nucleotide sequence and expression of the aceK gene coding for isocitrate dehydrogenase kinase/ phosphatase in Escherichia coli. J Bacteriol 170 (1988) 89-97
38. Ramseier T.M., Bledig S., Michotey V., Feghali R., and Saier Jr. M.H. The global regulatory protein, FruR, modulates the direction of carbon flow in Escherichia coli. Mol Microbiol 16 (1995) 1157-1169
39. Cortay J.C., Nègre D., Galinier A., Duclos B., Perrière G., and Cozzone A.J. Regulation of the acetate operon in Escherichia coli: purification and functional characterization of the IclR repressor. EMBO J 10 (1991) 675-679
40. Edlin J.D., and Sundaram T.K. Regulation of isocitrate dehydrogenase by phosphorylation in Escherichia coli K-12 and a simple method for determining the amount of inactive phosphoenzyme. J Bacteriol 171 (1989) 2634-2638
41. Neidhardt F.C., Ingraham J., and Schaechter M. Physiology of the bacterial cell: a molecular approach (1990), Sinauer Associates, Sunderland, MA