New insights into Escherichia coli metabolism: Carbon scavenging, acetate metabolism and carbon recycling responses during growth on glycerol

Microbial Cell Factories

Volumn 11, Issue , 2012, Pages

  Martínez Gómez, Karla ^a   Flores, Noemí ^a   Castañeda, Héctor M ^a   Martínez Batallar, Gabriel ^b   Hernández Chávez, Georgina ^a   Ramírez, Octavio T ^a   Gosset, Guillermo ^a   Encarnación, Sergio ^b   Bolivar, Francisco ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^b INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; CARBON; GLUCOSE; GLYCEROL;

ADAPTATION; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM CULTURE; BIOMASS; CARBON CYCLING; ESCHERICHIA COLI; GENE OVEREXPRESSION; GROWTH RATE; NONHUMAN;

ACETATES; CARBON; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GLYCEROL; PROTEOMICS;

ESCHERICHIA COLI;

EID: 84862179493     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/1475-2859-11-46     Document Type: Article

References (86)

1. Weissenborn DL, Wittekindt N, Larson TJ: Structure and regulation of the glpFK operon encoding glycerol diffusion facilitator and glycerol kinase of Escherichia coli K-12. JBiolChem 1992, 267:6122-6131.
2. Bisen P, Sanodiya B, Thakur G, Baghel R, Prasad G: Biodiesel production with special emphasis on lipase-catalyzed transesterification. Biotechnol Lett 2010, 32:1019-1030.
3. Vasudevan P, Briggs M: Biodiesel production-current state of the art and challenges. J Ind Microbiol Biotechnol 2008, 35:421-430.
4. Dharmadi Y, Murarka A, Gonzalez R: Anaerobic fermentation of glycerol by Escherichia coli: A new platform for metabolic engineering. Biotechnology & Bioengeering 2006, 94:821-829.
5. Iuchi S, Cole ST, Lin EC: Multiple regulatory elements for the glpA operon encoding anaerobic glycerol-3-phosphate dehydrogenase and the glpD operon encoding aerobic glycerol-3-phosphate dehydrogenase in Escherichia coli: further characterization of respiratory control. J Bacteriol 1990, 172:179-184.
6. Frankel D.G: Glycolysis. In: Escherichia coli and Salmonella tiphymurium: Cellular and Molecular Biology. 2nd edition. Edited by Neidhardt, F.C. ASM Press, Washington, DC; 1996:189-196.
7. Oh MK, Liao JC: Gene expression profiling by DNA microarrays and metabolic fluxes in Escherichia coli. Biotechnol Prog 2000, 16:278-286.
8. Peng L, Shimizu K: Global metabolic regulation analysis for Escherichia coli K12 based on protein expression by 2-dimensional electrophoresis and enzyme activity measurement. Appl Microbiol Biotechnol 2003, 61:163-178.
9. Notley L, Ferenci T: Induction of RpoS-dependent functions in glucose- limited continuous culture: what level of nutrient limitation induces the stationary phase of Escherichia coli? J Bacteriol 1996, 178:1465-1468.
10. Hua Q, Yang C, Oshima T, Mori H, Shimizu K: Analysis of gene expression in Escherichia coli in response to changes of growth-limiting nutrient in chemostat cultures. Appl Environ Microbiol 2004, 70:2354-2366.
11. Hardiman T, Lemuth K, Keller MA, Reuss M, Siemann-Herzberg M: Topology of the global regulatory network of carbon limitation in Escherichia coli. JBiotechnol 2007, 132:359-374.
12. Flores N, Escalante A, de Anda R, Báez-Viveros JL, Merino E, Franco BGeorgellis D, Gosset G, Bolívar F: New insights into the role of sigma factor RpoS as revealed in Escherichia coli strains lacking the phosphoenolpyruvate:carbohydrate phosphotransferase system. Journal of Molecular Microbiology and Biotechnology 2008, 14:176-192.
13. Flores N, Flores S, Escalante A, de Anda R, Leal L, Malpica R, Georgellis D, Gosset G, Bolívar F: Adaptation for fast growth on glucose by differential expression of central carbon metabolism and gal regulon genes in an Escherichia coli strain lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system. Metabolic Engineering 2005, 7:70-87.
14. Storz G, Hengge-Aronis R (Ed): Bacterial stress responses, Chapter 11, page 163. 1st edition. ASM Press, Washington, DC; 2000.
15. Teich A, Meyer S, Lin HY, Andersson L, Enfors SO, Neubauer P: Growth rate related concentration changes of the starvation response regulators RpoS and ppGpp in glucose-limited fed-batch and continuous cultures of Escherichia coli. Biotechnol Prog 1999, 15:123-129.
16. Kayser A, Weber J, Hecht V, Rinas U: Metabolic flux analysis of Escherichia coli in glucose-limited continuous culture. I. Growth-rate-dependent metabolic efficiency at steady state. Microbiology 2005, 151:693-706.
17. Lange R, Hengge-Aronis R: Identification of a central regulator of stationary- phasegeneexpressionin Escherichia coli. Mol Microbiol 1991, 5:49-59.
18. Lange R, Hengge-Aronis R: The cellular concentration of the sigma S subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability. Genes Dev 1994, 8:1600-1612.
19. Flores N, de Anda R, Flores S, Escalante A, Hernández G, Martínez A, Bolívar F: Role of pyruvate oxidase in Escherichia coli strains lacking the phosphoenolpyruvate:carbohydrate phosphotransferase system. J Mol Microbiol Biotechnol 2004, 8:209-221.
20. Olvera L, Mendoza-Vargas A, Flores N, Olvera M, Sigala JC, Gosset G, Bolívar F: Transcription analysis of central metabolism genes in Escherichia coli. Possible roles of sigma38 in their expression, as a response to carbon limitation. PLoS One 2009, 4(e(10)):7466.
21. Flores S, Flores N, de Anda R, Gonzalez A, Escalante A, Gosset G, Bolivar F: Nutrient scavenging stress response in an Escherichia coli strain lacking the phosphoenol pyruvate: carbohydrate phosphotransferase system as explored by gene expression profile. J Mol Microbiol Biotechnol 2005, 10:51-63.
22. Gaal T, Mandel MJ, Silhavy TJ, Gourse RL: Crl facilitates RNA polymerase holoenzyme formation. J Bacteriol 2006, 188:7966-7970.
23. Messing J: A multi-purpose cloning system based on a single-stranded DNA bacteriophage M13. Recombinant DNA Technical Bulletin, NIH Publ 1979, 99:43-48.
24. Sigala J, Flores SFN, Aguilar C, de Anda R, Gosset G, Bolívar F: Acetate metabolism in Escherichia coli strains lacking phosphoenolpyruvate: carbohydrate phosphotransferase system; evidence of carbon recycling strategies and futile cycles. J Mol Microbiol Biotechnol 2008, 16:224-235.
25. Hengge R: The two-component network and the general stress sigma factor RpoS in Escherichia coli. In Bacterial Signal Transduction: Networks and Drug Targets. 631 edition. Edited by Utsumi R. Springer New York; 2008:40-53.
26. Hengge AR: Regulatory gene expression during entry into stationary phase. Escherichia coli and Salmonella tiphymurium: Cellular and Molecular Biology 1996, 2:1497-1512.
27. Kwon YD, Lee SY, Kim P: A physiology study of Escherichia coli overexpressing phosphoenolpyruvate carboxykinase. Biosci Biotechnol Biochem 2008, 72:1138-1141.
28. Konrberg H: L: The role and control of the glyoxylate cycle in Escherichia coli. Biochem J 1966, 99:1-11.
29. Courtright JB, Henning U: Malate dehydrogenase mutants in Escherichia coli K-12. J Bacteriol 1970, 102:722-728.
30. Fong SS, Palsson BO: Metabolic gene-deletion strains of Escherichia coli evolve to computationally predicted growth phenotypes. Nat Genet 2004 36:1056-1058.
31. Cozzone AJ: Regulation of acetate metabolism by protein phosphorylation in enteric bacteria. Annual Reviews of Microbiology 1998, 52:127-164.
32. Boos W, Shuman H: Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiol Mol Biol Rev 1998, 62:204-229.
33. Dippel R, Bergmiller T, Bohm A, Boos W: The maltodextrin system of Escherichia coli: glycogen-derived endogenous induction and osmoregulation. J Bacteriol 2005, 187:8332-8339.
34. Ferenci T: Adaptation to life at micromolar nutrient levels: the regulation of Escherichia coli glucose transport by endoinduction and cAMP. FEMS Microbiol Rev 1996, 18:301-317.
35. Death A, Ferenci T: Between feast and famine: endogenous inducer synthesis in the adaptation of Escherichia coli to growth with limiting carbohydrates. J Bacteriol 1994, 176:5101-5107.
36. Ferenci T: Hungry bacteria. Definition and properties of a nutritional state. Environmental Microbiology 2001, 3:605-609.
37. LiuM,DurfeeT,CabreraJE,ZhaoK,JinDJ,BlattnerFR: Global Transcriptional programs reveal a carbon source foraging strategy by Escherichia coli. JBiolChem 2005, 280:15921-15927.
38. Geanacopoulos M, Adhya S: Functional characterization of roles of GalR and GalS as regulators of the gal regulon. J Bacteriol 1997, 179:228-234.
39. Horváth P, Hunziker A, Erdossy J, Krishna S, Semsey S: Timing of gene transcription in the galactose utilization system of Escherichia coli. J Biol Chem 2010, 285:38062-38068.
40. Hengge-Aronis R: Signal transduction and regulatory mechanisms involved in the control of the sigmaS (RpoS) subunit of RNA polymerase Microbiol Mol Biol Rev 2002, 66:373-395.
41. Lelong C, Aguiluz K, Luche S, Kuhn L, Garin J, Rabilloud T: The Crl-RpoS regulon of Escherichia coli. Molecular & Cellular Proteomics 2007, 6:648-659.
42. Pratt LA, Hsing W, Gibson KE, Silhavy TJ: From acids to osmZ:multiple factors influence synthesis of the OmpF and OmpC porins in Escherichia coli. Mol Microbiol 1996, 20:911-917.
43. Ferrario M, Ernsting BR, Borst DW, Wiese DE, Blumenthal RM, Matthews RG: The leucine-responsive regulatory protein of Escherichia coli negatively regulates transcription of ompC and micF and positively regulates translation of ompF. J Bacteriol 1995, 177:103-113.
44. Chen S, Zhang A, Blyn LB, Storz G: micC, a second small-RNA regulator of Omp protein expression in Escherichia coli. J Bacteriol 2004, 186:6689-6697.
45. Yoshida T, Qin L, Egger LA, Inouye M: Transcription regulation of ompF and ompC by a single transcription factor, OmpR. JBiol Chem 2006, 281:17114-17123.
46. De la Cruz CE: The complexities of porin genetic regulation. J Mol Microbiol Biotechnol 2010, 18:24-36.
47. Death A, Notley L, Ferenci T: Derepression of LamB protein facilitates outer membrane permeation of carbohydrates into Escherichia coli unde conditions of nutrient stress. J Bacteriol 1993, 175:1475-1483.
48. Gosset G: Improvement of Escherichia coli production strains by modification of the phosphoenolpyruvate:sugar phosphotransferase system. Microbial Cell Factories 2005, 4:14.
49. Romeo T, Snoep JL. Glycolysis and flux control. Edited by Bock, A., Curtiss, R., Kaper, J.B., Karp, P.D., Neidhardt,F.C., Nystrom, T., Slauch, J. M.,Squires,C.L.andUssery,D.In:EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology. American Society for Microbiology, Washington, D. C. 2005
50. Lacour S, Landini P: SigmaS-dependent gene expression at the onset of stationary phase in Escherichia coli: function of S-dependent genes and identification of their promoter sequences. J Bacteriol 2004, 186:7186-7195.
51. Mendoza-Vargas A, Olvera L, Olvera M, Grande R, Vega-Alvarado L, Taboada B, Collado-Vides J, Morett E: Genome-wide identification of transcription start sites, promoters and transcription factor binding sites in E. coli. PLoS One 2009, 4(10):e7526.
52. Raman B, Nandakumar MP, Muthuvijayan V, Marten MR: Proteome analysis to assess physiological changes in Escherichia coli grown under glucoselimited fed-batch conditions. Biotechnol Bioeng 2005, 92:384-392.
53. Bledig SA, Ramseier TM, Saier MH Jr: FruR mediates catabolite activation of pyruvate kinase (pykF) gene expression in Escherichia coli. J Bacteriol 1996, 178:280-283.
54. Weber J, Kayser A, Rinas U: Metabolic flux analysis of Escherichia coli in glucose-limited continuous culture. II. Dynamic response to famine and feast, activation of the methylglyoxal pathway and oscillatory behaviour. Microbiology 2005, 151:707-716.
55. Gimenez R, Nunez MF, Badia J, Aguilar J, Baldoma L: The gene yjcG, cotranscribed with the gene acs, encodes an acetate permease in Escherichia coli. J Bacteriol 2003, 185:6448-6455.
56. Flores S, Gosset G, Flores N, de Graaf AA, Bolívar F: Analysis of carbon metabolism in Escherichia coli strains with an inactive phosphotransferase system by 13 C labeling and NMR spectroscopy. Metab Eng 2002, 4:124-137.
57. Dong T, Schellhorn H: Control of RpoS in global gene expression of Escherichia coli in minimal media. Molecular Genetics and Genomics 2009, 281:19-33.
58. Oh MK, Rohlin L, Kao KC, Liao JC: Global expression profiling of acetate- grown Escherichia coli. J Biol Chem 2002, 277:13175-13183.
59. Cronan J, Subrahmanyam S: FadR, transcriptional co-ordination of metabolic expediency. Mol Microbiol 1998, 29:937-943.
60. Cunningham L, Gruer MJ, Guest JR: Transcriptional regulation of the aconitase genes (acnA and acnB)of Escherichia coli. Microbiology 1997, 143:3795-3805.
61. Zientz E, Bongaerts J, Unden G: Fumarate regulation of gene expression in Escherichia coli by the DcuSR (dcuSR Genes) two-component regulatory system. J Bacteriol 1998, 180:5421-5425.
62. Davies SJ, Golby P, Omrani D, Broad SA, Harrington VL, Guest JR, Kelly DJ, Andrews SC: Inactivation and regulation of the aerobic C4-dicarboxylate transport (dctA) gene of Escherichia coli. Journal of Bacteriology 1999, 181:5624-5635.
63. Hove-Jensen B: Mutation in the phosphoribosylpyrophosphate synthetase gene (prs) that results in simultaneous requirements for purine and pyrimidine nucleosides, nicotinamide nucleotide, histidine, and tryptophan in Escherichia coli. J Bacteriol 1988, 170:1148-1152.
64. Dong T, Kirchhof M, Schellhorn H: RpoS regulation of gene expression during exponential growth of Escherichia coli K12. Molecular Genetics and Genomics 2008, 279:267-277.
65. Balderas-Hernandez V, Sabido-Ramos A, Silva P, Cabrera-Valladares N, Hernandez-Chavez G, Baez-Viveros J, Gosset G: Metabolic engineering for improving anthranilate synthesis from glucose in Escherichia coli. Microbial Cell Factories 2009, 8:19.
66. Escalante A, Calderon R, Valdivia A, de Anda R, Hernandez G, Ramirez O, Bolívar F: Metabolic engineering for the production of shikimic acid in an evolved Escherichia coli strain lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system. Microbial Cell Factories 2010, 9:21.
67. Bolívar F, Rodríguez RL, Greene PJ, Betlach MC, Heynker HL, Boyer HW,CrossaJH,FalkowS: Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene 1977, 2:95-113.
68. Flores N, Leal L, Sigala JC, De Anda R, Martínez A, Escalante, Bolívar F: Growth recovery on glucose under aerobic conditions of an Escherichia coli strain carrying a phosphoenolpyruvate:carbohydrate phosphotransferase system deletion by inactivating arcA and overexpressing the genes coding for glucokinase and galactose permease. Journal of Molecular Microbiology and Biotechnology 2007, 13:105-116.
69. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H: Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Molecular Systems Biology 2006, 2. doi:10.1038/msb4100050.
70. Datsenko KA, Wanner BL: One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci 2000, 97:6640-6645.
71. Martínez K, de Anda R, Hernández G, Escalante A, Gosset G, Ramírez OT, Bolívar F: Coutilization of glucose and glycerol enhances the production of aromatic compounds in an Escherichia coli strain lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system. Microbial Cell Factories 2008, 7:1.
72. Chávez-Béjar MI, Lara AR, López H, Hernández-Chávez G, Martínez A, Ramírez OT, Bolívar F, Gosset G: Metabolic engineering of Escherichia coli for L-tyrosine production by expression of genes coding for the chorismate mutase domain of the native chorismate mutase-prephenate dehydratase and a cyclohexadienyl dehydrogenase from Zymomonas mobilis. Appl Environ Microbiol 2008, 74:3284-3290.
73. Xue Z, McCluskey M, Cantera K, Ben-Bassat A, Sariaslani FS, Huang L: Improved production of p-hydroxycinnamic acid from tyrosine using a novel thermostable phenylalanine/tyrosine ammonia lyase enzyme. Enzyme Microb Technol 2007, 42:58-64.
74. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT: The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 2009, 55:611-622.
75. Taylor S, Wakem M, Dijkman G, Alsarraj M, Nguyen M: A practical approach to RT-qPCR publishing data that conform to the MIQE guidelines. Methods 2010, 50:S1-S5.
76. Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta][Delta]CT method. Methods 2001, 25:402-408.
77. Kruger NJ: The Bradford method for protein quantitation. In: Basic Protein and Peptide Protocols. 32 edition. Edited by Walker, J.M. Humana Press Inc., Totowa, NJ; 1994:9-15
78. Sridhar J, Eiteman MA, Wiegel JW: Elucidation of enzymes in fermentation pathways used by Clostridium thermosuccinogenes growing on inulin. Appl Environ Microbiol 2000, 66:246-251.
79. der Werf MJV, Guettler MV, Jain MK, Zeikus JG: Environmental and physiological factors affecting the succinate product ratio during carbohydrate fermentation by Actinobacillus sp. 130Z. Arch Microbiol 1997, 167:332-342.
80. Ramírez-Trujillo JA, Encarnación S, Salazar E, de los Santos AG, Dunn MF, Emerich DW, Calva E, Hernández-Lucas I: Functional characterization of the Sinorhizobium meliloti acetate metabolism genes aceA, SMc00767, and glcB. Journal of Bacteriology 2007, 189:5875-5884.
81. Aoshima M, Ishii M, Yamagishi A, Oshima T, Igarashi Y: Metabolic characteristics of an isocitrate dehydrogenase defective derivative of Escherichia coli BL21(DE3). Biotechnol Bioeng 2003, 84:732-737.
82. Boctor FN, Ragher HH, Kamel MY, Hamed RR: A colorimetric method for the determination of indole, and its application to assay of tryptophanase. Anal Biochem 1978, 86:457-462.
83. Salazar E, Díaz-Mejía JJ, Moreno-Hagelsieb G, Martínez-Batallar G, Mora Y, Mora J, Encarnación S: Characterization of the NifA-RpoN regulon in Rhizobium etli in free life and in symbiosis with Phaseolus vulgaris. Applied Environmental Microbiology 2010, 76:4510-4520.
84. Higareda-Almaraz J, Enríquez-Gasca M, Hernández-Ortiz M, Resendis-Antonio O, Encarnación-Guevara S: Proteomic patterns of cervical cancer cell lines, a network perspective. BMC Syst Biol 2011, 5:96.
85. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS: Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20:3551-3567.
86. The UniProt Consortium: The universal protein resource (UniProt). Nucleic Acids Res 2008, 36:D190-D195.