Deletion of genes encoding cytochrome oxidases and quinol monooxygenase blocks the aerobic anaerobic shift in escherichia coli K-12 MG1655

Applied and Environmental Microbiology

Volumn 76, Issue 19, 2010, Pages 6529-6540

  Portnoy, Vasiliy A ^a   Scott, David A ^b   Lewis, Nathan E ^a   Tarasova, Yekaterina ^b   Osterman, Andrei L ^b   Palsson, Bernhard Ø ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AEROBIC GROWTH; AEROBIC-ANAEROBIC; ANAEROBIC RESPIRATION; ANOXIC CONDITIONS; CENTRAL METABOLISMS; CYTOCHROME OXIDASE; D-LACTATE; E. COLI; FLUX ANALYSIS; GENES ENCODING; HIGHLY-CORRELATED; KNOCKOUT STRAINS; MENAQUINONES; METABOLIC FLUX DISTRIBUTION; MONOOXYGENASES; MUTANT STRAIN; OXIC CONDITIONS; OXYGEN UPTAKE RATES; REGULATORY SYSTEMS; SIMILAR PATTERN; TRANSCRIPTIONAL REGULATOR; TRANSCRIPTOME ANALYSIS; TRICARBOXYLIC ACIDS;

ACIDS; ESCHERICHIA COLI; GENES; LAKES; METABOLISM; OXYGEN; PHYSIOLOGY; PIGMENTS;

ACTIVATION ANALYSIS;

ARCA PROTEIN, E COLI; CARBON; CYTOCHROME C OXIDASE; ESCHERICHIA COLI PROTEIN; FARNOQUINONE; LACTIC ACID; MIXED FUNCTION OXIDASE; OUTER MEMBRANE PROTEIN; OXYGEN; REPRESSOR PROTEIN; UBIQUINONE; YGIN PROTEIN, E COLI;

ANOXIC CONDITIONS; CARBON ISOTOPE; COLIFORM BACTERIUM; CYTOCHROME; ENZYME ACTIVITY; GENE EXPRESSION; METABOLISM; MUTATION; PHENOTYPE; REDOX CONDITIONS;

AEROBIC METABOLISM; ANAEROBIC GROWTH; ARTICLE; BIOSYNTHESIS; CITRIC ACID CYCLE; ESCHERICHIA COLI K 12; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; GLYCOLYSIS; METABOLISM; METHODOLOGY; STAINING;

AEROBIOSIS; ANAEROBIOSIS; BACTERIAL OUTER MEMBRANE PROTEINS; CARBON ISOTOPES; CITRIC ACID CYCLE; ELECTRON TRANSPORT COMPLEX IV; ESCHERICHIA COLI K12; ESCHERICHIA COLI PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GLYCOLYSIS; LACTIC ACID; MIXED FUNCTION OXYGENASES; OXYGEN; REPRESSOR PROTEINS; STAINING AND LABELING; UBIQUINONE; VITAMIN K 2;

ARCA; ESCHERICHIA COLI; ESCHERICHIA COLI K12;

EID: 78049253925     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01178-10     Document Type: Article

References (53)

1. Adams, M. A., and Z. Jia. 2005. Structural and biochemical evidence for an enzymatic quinone redox cycle in Escherichia coli: identification of a novel quinol monooxygenase. J. Biol. Chem. 280:8358-8363.
2. Alexeeva, S., K. J. Hellingwerf, and M. J. Teixeira de Mattos. 2003. Requirement of ArcA for redox regulation in Escherichia coli under microaerobic but not anaerobic or aerobic conditions. J. Bacteriol. 185:204-209.
3. Barrett, T., D. B. Troup, S. E. Wilhite, P. Ledoux, D. Rudnev, C. Evangelista, I. F. Kim, A. Soboleva, M. Tomashevsky, K. A. Marshall, K. H. Phillippy, P. M. Sherman, R. N. Muertter, and R. Edgar. 2009. NCBI GEO: archive for high-throughput functional genomic data. Nucleic Acids Res. 37:D885-D890.
4. Bekker, M., S. Alexeeva, W. Laan, G. Sawers, J. Teixeira de Mattos, and K. Hellingwerf. 2010. The ArcBA two-component system of Escherichia coli is regulated by the redox state of both the ubiquinone and the menaquinone pool. J. Bacteriol. 192:746-754.
5. Bekker, M., G. Kramer, A. F. Hartog, M. J. Wagner, C. G. de Koster, K. J. Hellingwerf, and M. J. de Mattos. 2007. Changes in the redox state and composition of the quinone pool of Escherichia coli during aerobic batchculture growth. Microbiology 153:1974-1980.
6. Brondsted, L., and T. Atlung. 1994. Anaerobic regulation of the hydrogenase 1 (hya) operon of Escherichia coli. J. Bacteriol. 176:5423-5428.
7. Cho, B. K., E. M. Knight, and B. O. Palsson. 2006. PCR-based tandem epitope tagging system for Escherichia coli genome engineering. Biotechniques 40:67-72.
8. Compan, I., and D. Touati. 1994. Anaerobic activation of arcA transcription in Escherichia coli: roles of Fnr and ArcA. Mol. Microbiol. 11:955-964.
9. Covert, M. W., E. M. Knight, J. L. Reed, M. J. Herrgard, and B. O. Palsson. 2004. Integrating high-throughput and computational data elucidates bacterial networks. Nature 429:92-96.
10. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
11. Dellomonaco, C., C. Rivera, P. Campbell, and R. Gonzalez. 2010. Engineered respiro-fermentative metabolism for the production of biofuels and biochemicals from fatty acid-rich feedstocks. Appl. Environ. Microbiol. 76: 5067-5078.
12. Edgar, R., M. Domrachev, and A. E. Lash. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30:207-210.
13. Feist, A. M., C. S. Henry, J. L. Reed, M. Krummenacker, A. R. Joyce, P. D. Karp, L. J. Broadbelt, V. Hatzimanikatis, and B. O. Palsson. 2007. A genome- scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information. Mol. Syst. Biol. 3:121.
14. Fischer, E., and U. Sauer. 2003. Metabolic flux profiling of Escherichia coli mutants in central carbon metabolism using GC-MS. Eur. J. Biochem. 270: 880-891.
15. Fong, S. S., A. P. Burgard, C. D. Herring, E. M. Knight, F. R. Blattner, C. D. Maranas, and B. O. Palsson. 2005. In silico design and adaptive evolution of Escherichia coli for production of lactic acid. Biotechnol. Bioeng. 91:643-648.
16. Gama-Castro, S., V. Jimenez-Jacinto, M. Peralta-Gil, A. Santos-Zavaleta, M. I. Penaloza-Spinola, B. Contreras-Moreira, J. Segura-Salazar, L. Muniz- Rascado, I. Martinez-Flores, H. Salgado, C. Bonavides-Martinez, C. Abreu- Goodger, C. Rodriguez-Penagos, J. Miranda-Rios, E. Morett, E. Merino, A. M. Huerta, L. Trevino-Quintanilla, and J. Collado-Vides. 2008. RegulonDB (version 6.0): gene regulation model of Escherichia coli K-12 beyond transcription, active (experimental) annotated promoters and Textpresso navigation. Nucleic Acids Res. 36:D120-D124.
17. Georgellis, D., O. Kwon, and E. C. Lin. 2001. Quinones as the redox signal for the arc two-component system of bacteria. Science 292:2314-2316.
18. Gonzalez, R., P. Campbell, and M. Wong. 2010. Production of ethanol from thin stillage by metabolically engineered Escherichia coli. Biotechnol. Lett. 32:405-411.
19. Gunsalus, R. P., and S. J. Park. 1994. Aerobic-anaerobic gene regulation in Escherichia coli: control by the ArcAB and Fnr regulons. Res. Microbiol. 145:437-450.
20. Herring, C. D., A. Raghunathan, C. Honisch, T. Patel, M. K. Applebee, A. R. Joyce, T. J. Albert, F. R. Blattner, D. van den Boom, C. R. Cantor, and B. O. Palsson. 2006. Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nat. Genet. 38:1406-1412.
21. Iuchi, S., and E. C. Lin. 1993. Adaptation of Escherichia coli to redox environments by gene expression. Mol. Microbiol. 9:9-15.
22. Iuchi, S., and E. C. Lin. 1988. arcA (dye), a global regulatory gene in Escherichia coli mediating repression of enzymes in aerobic pathways. Proc. Natl. Acad. Sci. U. S. A. 85:1888-1892.
23. Iverson, T. M., C. Luna-Chavez, G. Cecchini, and D. C. Rees. 1999. Structure of the Escherichia coli fumarate reductase respiratory complex. Science 284: 1961-1966.
24. Jarboe, L. R., X. Zhang, X. Wang, J. C. Moore, K. T. Shanmugam, and L. O. Ingram. 2010. Metabolic engineering for production of biorenewable fuels and chemicals: contributions of synthetic biology. J. Biomed. Biotechnol. 2010:761042.
25. Jervis, A. J., J. C. Crack, G. White, P. J. Artymiuk, M. R. Cheesman, A. J. Thomson, N. E. Le Brun, and J. Green. 2009. The O2 sensitivity of the transcription factor FNR is controlled by Ser24 modulating the kinetics of [4Fe-4S] to [2Fe-2S] conversion. Proc. Natl. Acad. Sci. U. S. A. 106:4659-4664.
26. Kanehisa, M., S. Goto, M. Furumichi, M. Tanabe, and M. Hirakawa. 2010. KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res. 38:D355-D360.
27. Kang, Y., K. D. Weber, Y. Qiu, P. J. Kiley, and F. R. Blattner. 2005. Genome-wide expression analysis indicates that FNR of Escherichia coli K-12 regulates a large number of genes of unknown function. J. Bacteriol. 187:1135-1160.
28. Karp, P. D., I. M. Keseler, A. Shearer, M. Latendresse, M. Krummenacker, S. M. Paley, I. Paulsen, J. Collado-Vides, S. Gama-Castro, M. Peralta-Gil, A. Santos-Zavaleta, M. I. Penaloza-Spinola, C. Bonavides-Martinez, and J. Ingraham. 2007. Multidimensional annotation of the Escherichia coli K-12 genome. Nucleic Acids Res. 35:7577-7590.
29. Keseler, I. M., C. Bonavides-Martinez, J. Collado-Vides, S. Gama-Castro, R. P. Gunsalus, D. A. Johnson, M. Krummenacker, L. M. Nolan, S. Paley, I. T. Paulsen, M. Peralta-Gil, A. Santos-Zavaleta, A. G. Shearer, and P. D. Karp. 2009. EcoCyc: a comprehensive view of Escherichia coli biology. Nucleic Acids Res. 37:D464-D470.
30. Lee, K. H., J. H. Park, T. Y. Kim, H. U. Kim, and S. Y. Lee. 2007. Systems metabolic engineering of Escherichia coli for L-threonine production. Mol. Syst. Biol. 3:149.
31. Lee, S. J., D. Y. Lee, T. Y. Kim, B. H. Kim, J. Lee, and S. Y. Lee. 2005. Metabolic engineering of Escherichia coli for enhanced production of succinic acid, based on genome comparison and in silico gene knockout simulation. Appl. Environ. Microbiol. 71:7880-7887.
32. Li, Z. J., J. Jian, X. X. Wei, X. W. Shen, and G. Q. Chen. 2010. Microbial production of meso-2,3-butanediol by metabolically engineered Escherichia coli under low oxygen condition. Appl. Microbiol. Biotechnol. 87:2001-2009.
33. Lynch, A. S., and E. C. Lin. 1996. Transcriptional control mediated by the ArcA two-component response regulator protein of Escherichia coli: characterization of DNA binding at target promoters. J. Bacteriol. 178:6238-6249.
34. Ma, J. F., M. Jiang, K. Q. Chen, B. Xu, S. W. Liu, P. Wei, and H. J. Ying. 22 May 2010, posting date. Succinic acid production with metabolically engineered Escherichia coli recovered from two-stage fermentation. Biotechnol. Lett. [Epub ahead of print.] doi:10.1007/s10529-010-0313-x.
35. Mazumdar, S., J. M. Clomburg, and R. Gonzalez. 2010. Escherichia coli strains engineered for homofermentative production of D-lactic acid from glycerol. Appl. Environ. Microbiol. 76:4327-4336.
36. Murray, E. L., and T. Conway. 2005. Multiple regulators control expression of the Entner-Doudoroff aldolase (Eda) of Escherichia coli. J. Bacteriol. 187:991-1000.
37. Nanchen, A., T. Fuhrer, and U. Sauer. 2007. Determination of metabolic flux ratios from 13C-experiments and gas chromatography-mass spectrometry data: protocol and principles. Methods Mol. Biol. 358:177-197.
38. Neidhardt, F. (ed.). 1996. Escherichia coli and Salmonella, 2nd ed., vol. 1. ASM Press, Washington, DC.
39. Portnoy, V. A., M. J. Herrgard, and B. O. Palsson. 2008. Aerobic fermentation of D-glucose by an evolved cytochrome oxidase-deficient Escherichia coli strain. Appl. Environ. Microbiol. 74:7561-7569.
40. Salmon, K., S. P. Hung, K. Mekjian, P. Baldi, G. W. Hatfield, and R. P. Gunsalus. 2003. Global gene expression profiling in Escherichia coli K12. The effects of oxygen availability and FNR. J. Biol. Chem. 278:29837-29855.
41. Scott, C., J. D. Partridge, J. R. Stephenson, and J. Green. 2003. DNA target sequence and FNR-dependent gene expression. FEBS Lett. 541:97-101.
42. Shestopalov, A. I., A. V. Bogachev, R. A. Murtazina, M. B. Viryasov, and V. P. Skulachev. 1997. Aeration-dependent changes in composition of the quinone pool in Escherichia coli. Evidence of post-transcriptional regulation of the quinone biosynthesis. FEBS Lett. 404:272-284.
43. Shukla, V. B., S. Zhou, L. P. Yomano, K. T. Shanmugam, J. F. Preston, and L. O. Ingram. 2004. Production of D(-)-lactate from sucrose and molasses. Biotechnol. Lett. 26:689-693.
44. Spiro, S., and J. R. Guest. 1991. Adaptive responses to oxygen limitation in Escherichia coli. Trends Biochem. Sci. 16:310-314.
45. Spiro, S., and J. R. Guest. 1990. FNR and its role in oxygen-regulated gene expression in Escherichia coli. FEMS Microbiol. Rev. 6:399-428.
46. Storey, J. D., and R. Tibshirani. 2003. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. U. S. A. 100:9440-9445.
47. Sutton, V. R., E. L. Mettert, H. Beinert, and P. J. Kiley. 2004. Kinetic analysis of the oxidative conversion of the [4Fe-4S]2'cluster of FNR to a [2Fe- 2S]2'cluster. J. Bacteriol. 186:8018-8025.
48. Szyperski, T. 1995. Biosynthetically directed fractional 13C-labeling of proteinogenic amino acids. An efficient analytical tool to investigate intermediary metabolism. Eur. J. Biochem. 232:433-448.
49. van Winden, W. A., C. Wittmann, E. Heinzle, and J. J. Heijnen. 2002. Correcting mass isotopomer distributions for naturally occurring isotopes. Biotechnol. Bioeng. 80:477-479.
50. Yagi, T., and A. Matsuno-Yagi. 2003. The proton-translocating NADHquinone oxidoreductase in the respiratory chain: the secret unlocked. Biochemistry 42:2266-2274.
51. Zhou, S., T. B. Causey, A. Hasona, K. T. Shanmugam, and L. O. Ingram. 2003. Production of optically pure D-lactic acid in mineral salts medium by metabolically engineered Escherichia coli W3110. Appl. Environ. Microbiol. 69:399-407.
52. Zhu, Y., M. A. Eiteman, R. Altman, and E. Altman. 2008. High glycolytic flux improves pyruvate production by a metabolically engineered Escherichia coli strain. Appl. Environ. Microbiol. 74:6649-6655.
53. Zhu, Y., M. A. Eiteman, K. DeWitt, and E. Altman. 2007. Homolactate fermentation by metabolically engineered Escherichia coli strains. Appl. Environ. Microbiol. 73:456-464.