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Abstract:

Bioprocesses conducted under conditions with restricted O2 supply are increasingly exploited for the synthesis of reduced biochemicals using different biocatalysts. The model facultative anaerobe Escherichia coli has elaborate sensing and signal transduction mechanisms for redox control in response to the availability of O2 and other electron acceptors. The ArcBA two-component system consists of ArcB, a membrane-associated sensor kinase, and ArcA, the cognate response regulator. The tripartite hybrid kinase ArcB possesses a transmembrane, a PAS, a primary transmitter (H1), a receiver (D1), and a phosphotransfer (H2) domain. Metabolic fluxes were compared under anoxic conditions in a wild-type E. coli strain, its ΔarcB derivative, and two partial arcB deletion mutants in which ArcB lacked either the H1 domain or the PAS-H1-D1 domains. These analyses revealed that elimination of different segments in ArcB determines a distinctive distribution of D-glucose catabolic fluxes, different from that observed in the ΔarcB background. Metabolite profiles, enzyme activity levels, and gene expression patterns were also investigated in these strains. Relevant alterations were observed at the P-enol-pyruvate/pyruvate and acetyl coenzyme A metabolic nodes, and the formation of reduced fermentation metabolites, such as succinate, D-lactate, and ethanol, was favored in the mutant strains to different extents compared to the wild-type strain. These phenotypic traits were associated with altered levels of the enzymatic activities operating at these nodes, as well as with elevated NADH/NAD+ ratios. Thus, targeted modification of global regulators to obtain different metabolic flux distributions under anoxic conditions is emerging as an attractive tool for metabolic engineering purposes. © 2012, American Society for Microbiology.

Registro:

Documento: Artículo
Título:Manipulation of the anoxic metabolism in escherichia coli by ArcB deletion variants in the ArcBA two-component system
Autor:Bidart, G.N.; Ruiz, J.A.; de Almeida, A.; Méndez, B.S.; Nikel, P.I.
Filiación:Instituto de Investigaciones Biotecnológicas Dr. Rodolfo A. Ugalde, Universidad Nacional de San Martín, Buenos Aires, Argentina
Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, IQUIBICEN-CONICET, Buenos Aires, Argentina
Instituto de Biociencias Agrícolas y Ambientales, CONICET, Buenos Aires, Argentina
Palabras clave:Acetyl coenzyme A; Anoxic conditions; Bioprocesses; D-glucose; D-lactate; Deletion mutants; Deletion variants; E. coli; Electron acceptor; Enzymatic activities; Facultative anaerobes; Gene expression patterns; Metabolic flux; Metabolic flux distribution; Metabolite profiles; Mutant strain; Phenotypic traits; Phospho-transfer; Response regulators; Sensor kinase; Signal transduction mechanism; Transmembranes; Two component systems; Wild types; Wild-type strain; Enzymes; Escherichia coli; Ethanol; Gene expression; Glucose; Metabolites; Plants (botany); Signal transduction; Metabolism; alcohol; arcA protein, E coli; arcB protein, E coli; Escherichia coli protein; glucose; lactic acid; membrane protein; nicotinamide adenine dinucleotide; outer membrane protein; protein kinase; repressor protein; succinic acid; anoxic conditions; biochemical composition; catalyst; coliform bacterium; metabolism; mutation; oxygen; redox conditions; anaerobic growth; article; enzymology; Escherichia coli; fermentation; gene deletion; genetics; metabolism; Anaerobiosis; Bacterial Outer Membrane Proteins; Escherichia coli; Escherichia coli Proteins; Ethanol; Fermentation; Glucose; Lactic Acid; Membrane Proteins; Metabolic Networks and Pathways; NAD; Protein Kinases; Repressor Proteins; Sequence Deletion; Succinic Acid; Arca; Escherichia coli
Año:2012
Volumen:78
Número:24
Página de inicio:8784
Página de fin:8794
DOI: http://dx.doi.org/10.1128/AEM.02558-12
Título revista:Applied and Environmental Microbiology
Título revista abreviado:Appl. Environ. Microbiol.
ISSN:00992240
CODEN:AEMID
CAS:alcohol, 64-17-5; glucose, 50-99-7, 84778-64-3; lactic acid, 113-21-3, 50-21-5; nicotinamide adenine dinucleotide, 53-84-9; protein kinase, 9026-43-1; succinic acid, 110-15-6; Bacterial Outer Membrane Proteins; Escherichia coli Proteins; Ethanol, 64-17-5; Glucose, 50-99-7; Lactic Acid, 50-21-5; Membrane Proteins; NAD, 53-84-9; Protein Kinases, 2.7.-; Repressor Proteins; Succinic Acid, 110-15-6; arcA protein, E coli; arcB protein, E coli, 2.7.3.-
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_00992240_v78_n24_p8784_Bidart.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00992240_v78_n24_p8784_Bidart

Referencias:

  • Alexeeva, S., de Kort, B., Sawers, G., Hellingwerf, K.J., Teixeira de Mattos, M.J., Effects of limited aeration and of the ArcAB system on intermediary pyruvate catabolism in Escherichia coli (2000) J. Bacteriol., 182, pp. 4934-4940
  • Alvarez, A.F., Georgellis, D., In vitro and in vivo analysis of the ArcB/A redox signaling pathway (2010) Methods Enzymol, 471, pp. 205-228
  • Alvarez, A.F., Malpica, R., Contreras, M., Escamilla, E., Georgellis, D., Cytochrome d but not cytochrome o rescues the toluidine blue growth sensitivity of arc mutants of Escherichia coli (2010) J. Bacteriol., 192, pp. 391-399
  • Aristidou, A.A., San, K.Y., Bennett, G.N., Metabolic flux analysis of Escherichia coli expressing the Bacillus subtilis acetolactate synthase in batch and continuous cultures (1999) Biotechnol. Bioeng., 63, pp. 737-749
  • Bekker, M., The ArcBA two-component system of Escherichia coli is regulated by the redox state of both the ubiquinone and the menaquinone pool (2010) J. Bacteriol., 192, pp. 746-754
  • Bekker, M., Teixeira de Mattos, M.J., Hellingwerf, K.J., The role of two-component regulation systems in the physiology of the bacterial cell (2006) Sci. Prog., 89, pp. 213-242
  • Bernofsky, C., Swan, M., An improved cycling assay for nicotinamide adenine dinucleotide (1973) Anal. Biochem., 53, pp. 452-458
  • Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding (1976) Anal. Biochem., 72, pp. 248-254
  • Bueno, E., Mesa, S., Bedmar, E.J., Richardson, D.J., Delgado, M.J., Bacterial adaptation of respiration from oxic to microoxic and anoxic conditions: Redox control (2012) Antioxid. Redox Signal., 16, pp. 819-852
  • Bunch, P.K., Mat-Jan, F., Lee, N., Clark, D.P., The ldhA gene encoding the fermentative lactate dehydrogenase of Escherichia coli (1997) Microbiology, 143, pp. 187-195
  • Buxton, R.S., Drury, L.S., Cloning and insertional inactivation of the dye (sfrA) gene, mutation of which affects sex factor F expression and dye sensitivity of Escherichia coli K-12 (1983) J. Bacteriol., 154, pp. 1309-1314
  • Cherepanov, P.P., Wackernagel, W., Gene disruption in Escherichia coli: Tcr and Kmr cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant (1995) Gene, 158, pp. 9-14
  • Clark, D.P., The fermentation pathways of Escherichia coli (1989) FEMS Microbiol. Rev., 5, pp. 223-234
  • Datsenko, K., Wanner, B.L., One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products (2000) Proc. Natl. Acad. Sci. U. S. A., 97, pp. 6640-6645
  • de Almeida, A., Giordano, A.M., Nikel, P.I., Pettinari, M.J., Effects of aeration on the synthesis of poly(3-hydroxybutyrate) from glycerol and glucose in recombinant Escherichia coli (2010) Appl. Environ. Microbiol., 76, pp. 2036-2040
  • Dittrich, C.R., Bennett, G.N., San, K.Y., Characterization of the acetateproducing pathways in Escherichia coli (2005) Biotechnol. Prog., 21, pp. 1062-1067
  • Dixon, G.H., Kornberg, H.L., Assay methods for key enzymes of the glyoxylate cycle (1959) Biochem. J., 73, pp. 3-10
  • Drapal, N., Sawers, G., Promoter 7 of the Escherichia coli pfl operon is a major determinant in the anaerobic regulation of expression by ArcA (1995) J. Bacteriol., 177, pp. 5338-5341
  • Ferry, J.G., Acetate kinase and phosphotransacetylase (2011) Methods Enzymol, 494, pp. 219-231
  • Fraenkel, D.G., Horecker, B.L., Pathways of D-glucose metabolism in Salmonella typhimurium. A study of a mutant lacking phosphoglucose isomerase (1964) J. Biol. Chem., 239, pp. 2765-2771
  • Georgellis, D., Kwon, O., De Wulf, P., Lin, E.C.C., Signal decay through a reverse phosphorelay in the Arc two-component signal transduction system (1998) J. Biol. Chem., 273, pp. 32864-32869
  • Georgellis, D., Kwon, O., Lin, E.C.C., Quinones as the redox signal for the arc two-component system of bacteria (2001) Science, 292, pp. 2314-2316
  • Georgellis, D., Lynch, A.S., Lin, E.C.C., In vitro phosphorylation study of the arc two-component signal transduction system of Escherichia coli (1997) J. Bacteriol., 179, pp. 5429-5435
  • Gomez, J.G.C., Making green polymers even greener: towards sustainable production of polyhydroxyalkanoates from agroindustrial byproducts (2012) Advances in applied biotechnology, pp. 41-62. , Petre M (ed), InTech, Rijeka, Croatia
  • Gottesman, S., Bacterial regulation: global regulatory networks (1984) Annu. Rev. Genet., 18, pp. 415-441
  • Green, J., Paget, M.S., Bacterial redox sensors (2004) Nat. Rev. Microbiol., 2, pp. 954-966
  • Groban, E.S., Clarke, E.J., Salis, H.M., Miller, S.M., Voigt, C.A., Kinetic buffering of cross talk between bacterial two-component sensors (2009) J. Mol. Biol., 390, pp. 380-393
  • Iuchi, S., Lin, E.C.C., Mutational analysis of signal transduction by ArcB, a membrane sensor protein responsible for anaerobic repression of operons involved in the central aerobic pathways in Escherichia coli (1992) J. Bacteriol., 174, pp. 3972-3980
  • Iuchi, S., Lin, E.C.C., Purification and phosphorylation of the Arc regulatory components of Escherichia coli (1992) J. Bacteriol., 174, pp. 5617-5623
  • Iuchi, S., Matsuda, Z., Fujiwara, T., Lin, E.C.C., The arcB gene of Escherichia coli encodes a sensor-regulator protein for anaerobic repression of the arc modulon (1990) Mol. Microbiol., 4, pp. 715-727
  • Jarboe, L.R., Metabolic engineering for production of biorenewable fuels and chemicals: contributions of synthetic biology (2010) J. Biomed. Biotechnol, 2010, p. 761042. , doi:10.1155/2010/761042
  • Kim, Y., Ingram, L.O., Shanmugam, K.T., Dihydrolipoamide dehydrogenase mutation alters the NADH sensitivity of pyruvate dehydrogenase complex of Escherichia coli K-12 (2008) J. Bacteriol., 190, pp. 3851-3858
  • Knappe, J., Blaschkowski, H.P., Gröbner, P., Schmitt, T., Pyruvate formate-lyase of Escherichia coli: the acetyl-enzyme intermediate (1974) Eur. J. Biochem., 50, pp. 253-263
  • Kwon, O., Georgellis, D., Lin, E.C.C., Phosphorelay as the sole physiological route of signal transmission by the arc two-component system of Escherichia coli (2000) J. Bacteriol., 182, pp. 3858-3862
  • Leonardo, M.R., Dailly, Y., Clark, D.P., Role of NAD in regulating the adhE gene of Escherichia coli (1996) J. Bacteriol., 178, pp. 6013-6018
  • Lynch, A.S., Lin, E.C.C., Responses to molecular oxygen (1996) Escherichia coli and Salmonella: cellular and molecular biology, 1, pp. 1526-1538. , Neidhardt FC, et al. (ed), 2nd ed. ASM Press, Washington DC
  • Malpica, R., Sandoval, G.R., Rodríguez, C., Franco, B., Georgellis, D., Signaling by the arc two-component system provides a link between the redox state of the quinone pool and gene expression (2006) Antioxid. Redox Signal., 8, pp. 781-795
  • Neidhardt, F.C., Ingraham, J.L., Schaechter, M., (1990) Physiology of the bacterial cell: a molecular approach, , Sinauer Associates, Sunderland, MA
  • Nikel, P.I., de Almeida, A., Pettinari, M.J., Méndez, B.S., The legacy of HfrH: mutations in the two-component system CreBC are responsible for the unusual phenotype of an Escherichia coli arcA mutant (2008) J. Bacteriol., 190, pp. 3404-3407
  • Nikel, P.I., Pettinari, M.J., Galvagno, M.A., Méndez, B.S., Poly(3-hydroxybutyrate) synthesis from glycerol by a recombinant Escherichia coli arcA mutant in fed-batch microaerobic cultures (2008) Appl. Microbiol. Biotechnol., 77, pp. 1337-1343
  • Nikel, P.I., Pettinari, M.J., Ramirez, M.C., Galvagno, M.A., Méndez, B.S., Escherichia coli arcA mutants: metabolic profile characterization of microaerobic cultures using glycerol as a carbon source (2008) J. Mol. Microbiol. Biotechnol., 15, pp. 48-54
  • Nikel, P.I., Zhu, J., San, K.Y., Méndez, B.S., Bennett, G.N., Metabolic flux analysis of Escherichia coli creB and arcA mutants reveals shared control of carbon catabolism under microaerobic growth conditions (2009) J. Bacteriol., 191, pp. 5538-5548
  • Nizam, S.A., Shimizu, K., Effects of arcA and arcB genes knockout on the metabolism in Escherichia coli under anaerobic and microaerobic conditions (2008) Biochem. Eng. J., 42, pp. 229-236
  • Nizam, S.A., Zhu, J., Ho, P.Y., Shimizu, K., Effects of arcA and arcB genes knockout on the metabolism in Escherichia coli under aerobic condition (2009) Biochem. Eng. J., 44, pp. 240-250
  • Okano, K., Tanaka, T., Ogino, C., Fukuda, H., Kondo, A., Biotechnological production of enantiomeric pure lactic acid from renewable resources: recent achievements, perspectives, and limits (2010) Appl. Microbiol. Biotechnol., 85, pp. 413-423
  • Overath, P., Schairer, H.U., Stoffel, W., Correlation of in vivo and in vitro phase transitions of membrane lipids in Escherichia coli (1970) Proc. Natl. Acad. Sci. U. S. A., 67, pp. 606-612
  • Park, S.J., McCabe, J., Turna, J., Gunsalus, R.P., Regulation of the citrate synthase (gltA) gene of Escherichia coli in response to anaerobiosis and carbon supply: role of the arcA gene product (1994) J. Bacteriol., 176, pp. 5086-5092
  • Patil, K.R., Bapat, P.M., Nielsen, J., Structure and flux analysis of metabolic networks (2010) The metabolic pathway engineering book: fundamentals, 1, pp. 17.11-17.18. , Smolke CD (ed), CRC Press, Boca Raton, FL
  • Peña-Sandoval, G.R., Georgellis, D., The ArcB sensor kinase of Escherichia coli autophosphorylates by an intramolecular reaction (2010) J. Bacteriol, 192, pp. 1735-1739
  • Perrenoud, A., Sauer, U., Impact of global transcriptional regulation by ArcA, ArcB, Cra, Crp, Cya, Fnr, and Mlc on glucose catabolism in Escherichia coli (2005) J. Bacteriol., 187, pp. 3171-3179
  • Rodriguez, C., Kwon, O., Georgellis, D., Effect of D-lactate on the physiological activity of the ArcB sensor kinase in Escherichia coli (2004) J. Bacteriol., 186, pp. 2085-2090
  • Rolfe, M.D., Transcript profiling and inference of Escherichia coli K-12 ArcA activity across the range of physiologically relevant oxygen concentrations (2011) J. Biol. Chem., 286, pp. 10147-10154
  • Ruiz, J.A., Fernández, R.O., Nikel, P.I., Méndez, B.S., Pettinari, M.J., dye (arc) mutants: insights into an unexplained phenotype and its suppression by the synthesis of poly(3-hydroxybutyrate) in Escherichia coli recombinants (2006) FEMS Microbiol. Lett., 258, pp. 55-60
  • Salmon, K.A., Global gene expression profiling in Escherichia coli K-12: effects of oxygen availability and ArcA (2005) J. Biol. Chem., 280, pp. 15084-15096
  • Sambrook, J., Russell, D.W., (2001) Molecular cloning: a laboratory manual 3rd ed, , Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
  • Sánchez, A.M., Bennett, G.N., San, K.Y., Batch culture characterization and metabolic flux analysis of succinate-producing Escherichia coli strains (2006) Metab. Eng., 8, pp. 209-226
  • Sawers, G., Specific transcriptional requirements for positive regulation of the anaerobically inducible pfl operon by ArcA and FNR (1993) Mol. Microbiol., 10, pp. 737-747
  • Schwalbach, M.S., Complex physiology and compound stress responses during fermentation of alkali-pretreated corn stover hydrolysate by an Escherichia coli ethanologen (2012) Appl. Environ. Microbiol., 78, pp. 3442-3457
  • Shalel-Levanon, S., San, K.Y., Bennett, G.N., Effect of oxygen on the Escherichia coli ArcA and FNR regulation systems and metabolic responses (2005) Biotechnol. Bioeng., 89, pp. 556-564
  • Shalel-Levanon, S., San, K.Y., Bennett, G.N., Effect of oxygen, and ArcA and FNR regulators on the expression of genes related to the electron transfer chain and the TCA cycle in Escherichia coli (2005) Metab. Eng., 7, pp. 364-374
  • Steiner, P., Fussenegger, M., Bailey, J.E., Sauer, U., Cloning and expression of the Zymomonas mobilis pyruvate kinase gene in Escherichia coli (1998) Gene, 220, pp. 31-38
  • Stephanopoulos, G., Metabolic fluxes and metabolic engineering (1999) Metab. Eng., 1, pp. 1-11
  • Taylor, B.L., Zhulin, I.B., PAS domains: internal sensors of oxygen, redox potential, and light (1999) Microbiol. Mol. Biol. Rev., 63, pp. 479-506
  • Thakker, C., Martínez, I., San, K.Y., Bennett, G.N., Succinate production in Escherichia coli (2012) Biotechnol. J., 7, pp. 213-224
  • Tsai, S.P., Lee, Y.H., Application of metabolic pathway stoichiometry to statistical analysis of bioreactor measurement data (1988) Biotechnol. Bioeng., 32, pp. 713-715
  • Tseng, C.P., Albrecht, J., Gunsalus, R.P., Effect of microaerophilic cell growth conditions on expression of the aerobic (cyoABCDE and cydAB) and anaerobic (narGHJI, frdABCD, and dmsABC) respiratory pathway genes in Escherichia coli (1996) J. Bacteriol., 178, pp. 1094-1098
  • Varma, A., Palsson, B.O., Stoichiometric flux balance models quantitatively predict growth and metabolic by-product secretion in wild-type Escherichia coli W3110 (1994) Appl. Environ. Microbiol., 60, pp. 3724-3731
  • Veeger, C., DerVartanian, D.V., Zeylemaker, W.P., Succinate dehydrogenase (1969) Methods Enzymol, 13, pp. 81-90
  • Vickers, C.E., Klein-Marcuschamer, D., Krömer, J.O., Examining the feasibility of bulk commodity production in Escherichia coli (2012) Biotechnol. Lett., 34, pp. 585-596
  • Wang, L., Divergence involving global regulatory gene mutations in an Escherichia coli population evolving under phosphate limitation (2010) Genome Biol. Evol., 2, pp. 478-487
  • Weitzman, P.D.J., Citrate synthase from Escherichia coli (1969) Methods Enzymol, 13, pp. 22-26
  • Yamamoto, K., Functional characterization in vitro of all twocomponent signal transduction systems from Escherichia coli (2005) J. Biol. Chem., 280, pp. 1448-1456
  • Zhu, J., Shalel-Levanon, S., Bennett, G.N., San, K.Y., Effect of the global redox sensing/regulation networks on Escherichia coli and metabolic flux distribution based on C-13 labeling experiments (2006) Metab. Eng., 8, pp. 619-627

Citas:

---------- APA ----------
Bidart, G.N., Ruiz, J.A., de Almeida, A., Méndez, B.S. & Nikel, P.I. (2012) . Manipulation of the anoxic metabolism in escherichia coli by ArcB deletion variants in the ArcBA two-component system. Applied and Environmental Microbiology, 78(24), 8784-8794.
http://dx.doi.org/10.1128/AEM.02558-12
---------- CHICAGO ----------
Bidart, G.N., Ruiz, J.A., de Almeida, A., Méndez, B.S., Nikel, P.I. "Manipulation of the anoxic metabolism in escherichia coli by ArcB deletion variants in the ArcBA two-component system" . Applied and Environmental Microbiology 78, no. 24 (2012) : 8784-8794.
http://dx.doi.org/10.1128/AEM.02558-12
---------- MLA ----------
Bidart, G.N., Ruiz, J.A., de Almeida, A., Méndez, B.S., Nikel, P.I. "Manipulation of the anoxic metabolism in escherichia coli by ArcB deletion variants in the ArcBA two-component system" . Applied and Environmental Microbiology, vol. 78, no. 24, 2012, pp. 8784-8794.
http://dx.doi.org/10.1128/AEM.02558-12
---------- VANCOUVER ----------
Bidart, G.N., Ruiz, J.A., de Almeida, A., Méndez, B.S., Nikel, P.I. Manipulation of the anoxic metabolism in escherichia coli by ArcB deletion variants in the ArcBA two-component system. Appl. Environ. Microbiol. 2012;78(24):8784-8794.
http://dx.doi.org/10.1128/AEM.02558-12