Transcriptional regulation of main metabolic pathways of cyoA, cydB, fnr, and fur gene knockout Escherichia coli in C-limited and N-limited aerobic continuous cultures

Microbial Cell Factories

Volumn 10, Issue , 2011, Pages

  Kumar, Rahul ^a,c   Shimizu, Kazuyuki ^a,b  

^a KYUSHU INSTITUTE OF TECHNOLOGY   (Japan)

^b KEIO UNIVERSITY   (Japan)

^c CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE; QUINOLINE; BACTERIAL PROTEIN; CARBON; CYOA PROTEIN, E COLI; CYTOCHROME; CYTOCHROME BD TERMINAL OXIDASE COMPLEX, E COLI; CYTOCHROME C OXIDASE; ESCHERICHIA COLI PROTEIN; FERRIC UPTAKE REGULATING PROTEINS, BACTERIAL; FNR PROTEIN, E COLI; IRON SULFUR PROTEIN; MULTIENZYME COMPLEX; NITROGEN; OXIDOREDUCTASE; REPRESSOR PROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIUM CULTURE; CONTROLLED STUDY; CRP GENE; CYDB GENE; CYOA GENE; ESCHERICHIA COLI; FNR GENE; FUR GENE; GENE CONTROL; GENE DELETION; GENE MUTATION; GENETIC TRANSCRIPTION; GLNA GENE; GLNB GENE; GLNE GENE; GLNG GENE; GLNK GENE; GLNL GENE; GLTB GENE; GLTD GENE; GLUCOSE INTAKE; MIC GENE; NONHUMAN; PTSG GENE; PTSH GENE; SODA GENE; SORS GENE; SOXR GENE; AEROBIC METABOLISM; CULTURE MEDIUM; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; METABOLISM; UPREGULATION;

ARCA; ESCHERICHIA COLI;

AEROBIOSIS; BACTERIAL PROTEINS; CARBON; CULTURE MEDIA; CYTOCHROMES; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; ELECTRON TRANSPORT COMPLEX IV; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKOUT TECHNIQUES; IRON-SULFUR PROTEINS; METABOLIC NETWORKS AND PATHWAYS; NITROGEN; OXIDOREDUCTASES; REPRESSOR PROTEINS; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 79251538647     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/1475-2859-10-3     Document Type: Article

References (69)

1. Fuhrer T, Sauer U. Different biochemical mechanisms ensure network-wide balancing of reducing equivalents in microbial metabolism. J Bacteriol 2009, 191:2112-2121. 10.1128/JB.01523-08, 2655529, 19181802.
2. Yuan J, Doucette CD, Fowler WU, Feng XJ, Piazza M, Rabitz HA, Wingreen NS, Rabinowitz JD. Metabolomics-driven quantitative analysis of ammonia assimilation in E. coli. Mol Syst Biol 2009, 5:302. 10.1038/msb.2009.60, 2736657, 19690571.
3. 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. 10.1128/AEM.70.4.2354-2366.2004, 383082, 15066832.
4. Magasanik B. Global regulation of gene expression. Proc Natl Acad Sci USA 2000, 97:14044-14045. 10.1073/pnas.97.26.14044, 34095, 11121014.
5. Zimmer DP, Soupene E, Lee HL, Khodursky AB, Peter BJ, Bender RA, Kustu S. Nitrogen regulatory protein C-controlled genes of Escherichia coli: Scavenging as a defense against nitrogen limitation. Proc Natl Acad Sci USA 2000, 97:14674-14679. 10.1073/pnas.97.26.14674, 18977, 11121068.
6. Peterson CN, Mandel MJ, Silhavy TJ. Escherichia coli starvation diets: essential nutrients weigh in distinctly. J Bacteriol 2005, 187:7549-7553. 10.1128/JB.187.22.7549-7553.2005, 1280323, 16267278.
7. Ferenci T. Hungry Bacteria-definition and properties of a nutritional state. Environ Microbiol 2001, 3:605-611. 10.1046/j.1462-2920.2001.00238.x, 11722540.
8. Harder W, Dijkhuizen L. Physiological responses to nutrient limitation. Annu Rev Microbiol 1983, 37:1-24. 10.1146/annurev.mi.37.100183.000245, 6357049.
9. Molenaar D, van Berlo R, de Ridder D, Teusink B. Shifts in growth strategies reflect tradeoffs in cellular economics. Mol Syst Biol 2009, 5:323. 10.1038/msb.2009.82, 2795476, 19888218.
10. De Mattos MJT, Neijssel OM. Bioenergetic consequences of microbial adaptation to lownutrient environments. J Biotechnol 1997, 59:117-126. 10.1016/S0168-1656(97)00174-0, 9487720.
11. Yuan J, Fowler WU, Kimball E, Lu W, Rabinowitz JD. Kinetic flux profiling of nitrogen assimilation in Escherichia coli. Nat Chem Biol 2006, 2:529-530. 10.1038/nchembio816, 16936719.
12. Reitzer L. Nitrogen assimilation and global regulation in Escherichia coli. Annu Rev Microbiol 2003, 57:155-176. 10.1146/annurev.micro.57.030502.090820, 12730324.
13. Pramanik J, Keasling JD. Stoichiometric model of Escherichia coli metabolism: Incorporation of growth-rate dependent biomass composition and mechanistic energy requirements. Biotechnol Bioeng 1997, 56:398-421. 10.1002/(SICI)1097-0290(19971120)56:4<398::AID-BIT6>3.0.CO;2-J, 18642243.
14. Neijssel OM, De Mattos MJT, Tempest DW. Growth yield and energy distribution. Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology 1996, Chapter 107. American Society for Microbiology, Washington, DC, Neidhardt FC.
15. Varma A, Boesch BW, Palsson BO. Biochemical production capabilities of Escherichia coli. Biotechnol Bioeng 1993, 42:59-73. 10.1002/bit.260420109, 18609648.
16. Bekker M, De Vries D, Beek AT, Hellingwerf KJ, De Mattos MJT. Respiration of Escherichia coli can be fully uncoupled via the nonelectrogenic terminal cytochrome bd- II oxidase. J Bacteriol 2009, 191:5510-5517. 10.1128/JB.00562-09, 2725625, 19542282.
17. Vemuri GN, Altman E, Sangurdekar DP, Khodursky AB, Eiteman MA. Overflow metabolism in Escherichia coli during steady-state growth: transcriptional regulation and effect of the redox ratio. Appl Environ Microbiol 2006, 72:3653-3661. 10.1128/AEM.72.5.3653-3661.2006, 1472329, 16672514.
18. Kumar R, Shimizu K. Metabolic regulation of Escherichia coli and its gdhA, glnL, gltB, D mutants under different carbon and nitrogen limitations in the continuous culture. Microbial Cell Factories 2010, 9:8. 10.1186/1475-2859-9-8, 2827463, 20105320.
19. Puustinen A, Finel M, Haltia T, Gennis RB, Wikstrom M. Properties of the two terminal oxidases of Escherichia coli. Biochemistry 1991, 30:3936-3942. 10.1021/bi00230a019, 1850294.
20. Kang Y, Weber KD, Qiu Y, Kiley PJ, Blattner FR. Genome-wide expression analysis indicates that FNR of Escherichia coli K-12 regulates a large number of genes of unknown function. J Bacteriol 2005, 187:1135-1160. 10.1128/JB.187.3.1135-1160.2005, 545700, 15659690.
21. Salmon K, Hung SP, Mekjian K, Baldi P, Hatfield GW, Gunsalus RP. Global gene expression profiling in Escherichia coli K12. The effects of oxygen availability and FNR. J Biol Chem 2003, 278:29837-29855. 10.1074/jbc.M213060200, 12754220.
22. Iuchi S, Lin EC. Adaptation of Escherichia coli to redox environments by gene expression. Mol Microbiol 1993, 9:9-15. 10.1111/j.1365-2958.1993.tb01664.x, 8412675.
23. Chen Z, Lewis KA, Shultzaberger RK, Lyakhov IG, Zheng M, Doan B, Storz G, Schneider TD. Discovery of Fur binding site clusters in Escherichia coli by information theory models. Nucleic Acids Res 2007, 35:6762-6777. 10.1093/nar/gkm631, 2189734, 17921503.
24. Hantke K. Iron and metal regulation in bacteria. Curr Opin Microbiol 2001, 4:172-177. 10.1016/S1369-5274(00)00184-3, 11282473.
25. Zhang Z, Gosset G, Barabote R, Gonzalez CS, Cuevas WA, Saier MH. Functional interactions between the carbon and iron utilization regulators, Crp and Fur, in Escherichia coli. J Bacteriol 2005, 187:980-990. 10.1128/JB.187.3.980-990.2005, 545712, 15659676.
26. Vassinova N, Kozyrev D. A method for direct cloning of fur-regulated genes: identification of seven new fur-regulated loci in Escherichia coli. Microbiology 2000, 146:3171-3182.
27. Tseng CP. Regulation of fumarase (fumB) gene expression in Escherichia coli in response to oxygen, iron and heme availability: role of the arcA, fur, and hemA gene products. FEMS Microbiol Lett 1997, 157:67-72. 10.1111/j.1574-6968.1997.tb12754.x, 9418241.
28. Brickman TJ, Ozenberger BA, McIntosh MA. Regulation of divergent transcription from the iron-responsive fepB-entC promoter-operator regions in Escherichia coli. J Mol Biol 1990, 212:669-682. 10.1016/0022-2836(90)90229-F, 2139473.
29. Steen EJ, Kang Y, Bokinsky G, Hu Z, Schirmer A, McClure A, del Cardayre SB, Keasling JD. Microbial production of fatty-acid-derived fuels and chemicals from plant biomass. Nature 2010, 463:559-562. 10.1038/nature08721, 20111002.
30. Brynildsen MP, Liao JC. An integrated network approach indentifies the isobutanol response network of Escherichia coli. Mol Syst Biol 2009, 5:34.
31. Keasling JD, Chou H. Metabolic engineering delivers next generation biofuels. Nature Biotechnol 2008, 26:298-299.
32. Frederick RE, Mayfield JA, DuBois JL. Iron trafficking as an antimicrobial target. Biometals 2009, 22:583-593. 10.1007/s10534-009-9236-1, 19350396.
33. Azpiroz MF, Lavińa M. Involvement of enterobactin synthesis pathway in production of Microcin H47. Antimicrob Agents Chemother 2004, 48:1235-1241. 10.1128/AAC.48.4.1235-1241.2004, 375329, 15047525.
34. Clarke TE. Structural characterization of Escherichia coli periplasmic ferric siderophores binding proteins 2001, Dissertation, University of Calgary, Alberta.
35. Georgellis D, Kwon O, Lin ECC. Quinones as the Redox Signal for the Arc Two-Component System of Bacteria. Science 2001, 292:2314-2316. 10.1126/science.1059361, 11423658.
36. Shalel-Levanon S, San KY, Bennett GN. Effect of oxygen on the Escherichia coli ArcA and FNR regulation systems and metabolic responses. Biotechnol Bioeng 2005, 89:556-564. 10.1002/bit.20381, 15669087.
37. Portnoy VA, Herrgard MJ, Palsson BO. Aerobic fermentation of D-glucose by an evolved cytochrome oxidase-deficient Escherichia coli strain. Appl Environ Micorobiol 2008, 74:7561-7569.
38. Sauer U, Canonaco F, Heri S, Perrenoud A, Fischer E. The soluble and membrane-bound transhydrogenases UdhA and PntAB have divergent functions in NADPH metabolism of Escherichia coli. J Biol Chem 2004, 279:6613-6619. 10.1074/jbc.M311657200, 14660605.
39. Unden G, Achebach S, Holighaus G, Tran HG, Wackwitz B, Zeuner Y. Control of Fnr function of Escherichia coli by O2 and reducing conditions. J Mol Microbiol Biotechnol 2002, 4:263-268.
40. Reinhart F, Achebach S, Koch T, Unden G. Reduced Apo-Fumarate Nitrate Reductase Regulator (ApoFNR) as the major form of FNR in aerobically growing Escherichia coli. J Bacteriol 2008, 190:879-886. 10.1128/JB.01374-07, 2223584, 18055593.
41. Shin D, Lim S, Seok YJ, Ryu S. Heat shock RNA polymerase (Eσ32) is involved in the transcription of mlc and crucial for induction of the Mlc regulon by glucose in Escherichia coli. J Biol Chem 2001, 276:25871-25875. 10.1074/jbc.M101757200, 11340070.
42. Mao XJ, Huo YX, Buck M, Kolb A, Wang YP. Interplay between CRP-cAMP and PII-Ntr systems forms novel regulatory network between carbon metabolism and nitrogen assimilation in Escherichia coli. Nucleic Acids Res 2007, 35:1432-1440. 10.1093/nar/gkl1142, 1865078, 17284458.
43. Ferenci T. Hungry bacteria-definition and properties of a nutritional state. Environ Microbiol 2001, 3:605-611. 10.1046/j.1462-2920.2001.00238.x, 11722540.
44. Javalle A, Severi E, Thorton J, Merrick M. Ammonium sensing in Escherichia coli. J Biol Chem 2004, 279:8530-853. 10.1074/jbc.M312399200, 14668330.
45. Constantinidou C, Hobman JL, Griffiths L, Patel MD, Penn CW, Cole JA, Overton TW. A renassessment of the Fnr regulon and transcriptomic analysis of the effects of nitrate, nitrite, narXL, and narQP as Escherichia coli K12 adapts from aerobic to anaerobic growth. J Biol Chem 2006, 281:4802-4815. 10.1074/jbc.M512312200, 16377617.
46. Ogasawara H, Ishida Y, Yamada K, Yamamoto K, Ishihama A. PdhR (Pyruvate Dehydrogenase Complex Regulator) Controls the Respiratory Electron Transport System in Escherichia coli. J Bacteriol 2007, 189:5534-5541. 10.1128/JB.00229-07, 1951801, 17513468.
47. Wagner AFV, Schultz S, Bomke J, Pils T, Lehmann WD, Knappe J. YfiD of Escherichia coli and Y061 of bacteriophage T4 as autonomous glycyl radical cofactors reconstituting the catalytic center of oxygen-fragmented pyruvate formate-lyase. Biochem Biophys Res Commun 2001, 285:456-462. 10.1006/bbrc.2001.5186, 11444864.
48. Moreau PL. The lysine decarboxylase CadA protects Escherichia coli starved of phosphate against fermentation acids. J Bacteriol 2007, 189:2249-61. 10.1128/JB.01306-06, 1899392, 17209032.
49. Fotheringham IG, Dacey SA, Taylor PP, Smith TJ, Hunter MG, Finlay ME, Primrose SB, Parker DM, Edwards RM. The cloning and sequence analysis of the aspC and tyrB genes from Escherichia coli K12. J Biochem 1986, 234:593-604.
50. Cotter PA, Melville SB, Albrecht JA, Gunsalus RP. Aerobic regulation of cytochrome d oxidase (cydAB) operon expression in Escherichia coli: roles of Fnr and ArcA in repression and activation. Mol Microbiol 1997, 25:605-615. 10.1046/j.1365-2958.1997.5031860.x, 9302022.
51. Mason MG, Shepherd M, Nicholls P, Dobbin PS, Dodsworth KS, Poole RK, Cooper CE. Cytochrome bd confers nitric oxide resistance to Escherichia coli. Nat Chem Biol 2009, 5:94-96. 10.1038/nchembio.135, 19109594.
52. Verkhovsky MI, Morgan JE, Puustein A, Wikström M. Kinetic trapping of oxygen in cell respiration. Nature 1996, 380:268-270. 10.1038/380268a0, 8637579.
53. Govantes F, Orjalo AV, Gunsalus RP. Interplay between three global regulatory proteins mediates oxygen regulation of the Escherichia coli cytochrome d oxidase (cydAB) operon. Mol Microbiol 2000, 38:1061-1073. 10.1046/j.1365-2958.2000.02215.x, 11123679.
54. Zheng M, Doan B, Schneider TD, Storz G. OxyR and SoxRS regulation of fur. J Biotechnol 1999, 181:4639-4643.
55. Storz G, Imlay JA. Oxidative stress. Curr Opin Microbiol 1999, 2:188-194. 10.1016/S1369-5274(99)80033-2, 10322176.
56. Braun V. Regulation of iron uptake minimizes iron-mediated oxidative stress. J Biosci 1998, 23:483-489.
57. McHugh JP, Rodríguez-Quiñones F, Abdul-Tehrani H, Svistunenko DA, Poole RK, Cooper CE, Andrews SC. Global iron-dependent gene regulation in Escherichia coli. J Biol Chem 2003, 278:29478-29486. 10.1074/jbc.M303381200, 12746439.
58. Dann CE, Wakeman CA, Sieling CL, Baker SC, Irnov I, Winker WC. Structure and mechanism of a metal-sensing regulatory RNA. Cell 2007, 130:878-892. 10.1016/j.cell.2007.06.051, 17803910.
59. Helmann JD. Measuring metals with RNA. Mol Cell 2007, 27:859-860. 10.1016/j.molcel.2007.09.002, 3022019, 17889657.
60. Gennis RB, Stewart V. Respiration in Escherichia coli and Salmonella: Cellular and Molecular Biology. 1996, Washington, DC: ASM press, Bock A, Curtiss R III, Kaper JB, Neidhardt FC, Nystrom T, Rudd KE, Squires CL.
61. Jovanovic G, Lloyde LJ, Stumpf MP, Mayhew AJ, Buck M. Induction and function of the phase shock protein extracytoplasmic stress response in Escherichia coli. J Biol Chem 2006, 281:21147-21161. 10.1074/jbc.M602323200, 16709570.
62. Blanchard JR, Wholey WY, Conlon EM, Pomposiello PJ. Rapid changes in gene expression dynamics in response to superoxide reveal SoxRS-dependent and independent transcriptional network. PLoS One 2007, 2:e1186. 10.1371/journal.pone.0001186, 2064960, 18000553.
63. Semsey S, Andersson AM, Krishna S, Jensen MH, Masse E, Sneppen K. Genetic regulation of fluxes: iron homeostasis of Escherichia coli. Nucleic Acids Res 2006, 34:4960-4967. 10.1093/nar/gkl627, 1635276, 16982641.
64. Hantash FM, Ammerlaan M, Earhart CF. Enterobactin synthase polypeptides of Escherichia coli are present in an osmotic-shock-sensitive cytoplasmic locality. Microbiology 1997, 143:147-156. 10.1099/00221287-143-1-147, 9025288.
65. 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. Mol Syst Biol 2006, 2. 2006.0008.
66. Rahman M, Hassan MR, Shimizu K. Growth phase-dependent changes in the expression of global regulatory genes and associated metabolic pathways in Escherichia coli. Biotechnol Lett 2008, 30:853-860. 10.1007/s10529-007-9621-1, 18175070.
67. Peng L, Shimizu K. Effect of fadR gene knockout on the metabolism of Escherichia coli based on analyses of protein expressions, enzyme activities and intracellular metabolite concentrations. Enzyme Microbiol Technol 2006, 38:512-520.
68. Kabir MM, Shimizu K. Gene expression patterns for metabolic pathway in pgi knockout Escherichia coli with and without phb genes based on RT-PCR. J Biotechnol 2003, 105:11-31. 10.1016/S0168-1656(03)00170-6, 14511906.
69. Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 3.