Artículo

Godoy, M.S.; Nikel, P.I.; Cabrera Gomez, J.G.; Julia Pettinari, M. "The CreC regulator of Escherichia coli, a new target for metabolic manipulations" (2016) Applied and Environmental Microbiology. 82(1):244-254
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Abstract:

The CreBC (carbon source-responsive) two-component regulation system of Escherichia coli affects a number of functions, including intermediary carbon catabolism. The impacts of different creC mutations (a ΔcreC mutant and a mutant carrying the constitutive creC510 allele) on bacterial physiology were analyzed in glucose cultures under three oxygen availability conditions. Differences in the amounts of extracellular metabolites produced were observed in the null mutant compared to the wild-type strain and the mutant carrying creC510 and shown to be affected by oxygen availability. The ΔcreC strain secreted more formate, succinate, and acetate but less lactate under low aeration. These metabolic changes were associated with differences in AckA and LdhA activities, both of which were affected by CreC. Measurement of the NAD(P)H/NAD(P)+ ratios showed that the creC510 strain had a more reduced intracellular redox state, while the opposite was observed for the ΔcreC mutant, particularly under intermediate oxygen availability conditions, indicating that CreC affects redox balance. The null mutant formed more succinate than the wild-type strain under both low aeration and no aeration. Overexpression of the genes encoding phosphoenolpyruvate carboxylase from E. coli and a NADH-forming formate dehydrogenase from Candida boidinii in the ΔcreC mutant further increased the yield of succinate on glucose. Interestingly, the elimination of ackA and adhE did not significantly improve the production of succinate. The diverse metabolic effects of this regulator on the central biochemical network of E. coli make it a good candidate for metabolic-engineering manipulations to enhance the formation of bioproducts, such as succinate. © 2015, American Society for Microbiology.

Registro:

Documento: Artículo
Título:The CreC regulator of Escherichia coli, a new target for metabolic manipulations
Autor:Godoy, M.S.; Nikel, P.I.; Cabrera Gomez, J.G.; Julia Pettinari, M.
Filiación:Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires (IQUIBICEN-CONICET), Buenos Aires, Argentina
Spanish National Centre for Biotechnology (CNB-CSIC), Madrid, Spain
Departamento de Microbiologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, Brazil
Palabras clave:Enzyme activity; Escherichia coli; Glucose; Metabolism; Oxygen; Biochemical network; Engineering manipulations; Extracellular metabolites; Formate dehydrogenase; Metabolic changes; Metabolic effects; Phosphoenolpyruvate carboxylase; Wild-type strain; Metabolic engineering; acetate; aeration; catabolism; coliform bacterium; metabolism; microbial community; physiology; Bacteria (microorganisms); Candida boidinii; Escherichia coli; CreC protein, E coli; Escherichia coli protein; glucose; nicotinamide adenine dinucleotide; oxygen; protein kinase; reduced nicotinamide adenine dinucleotide dehydrogenase; succinic acid; anaerobic growth; Escherichia coli; gene expression regulation; genetics; metabolic engineering; metabolism; mutation; oxidation reduction reaction; protein engineering; Anaerobiosis; Escherichia coli; Escherichia coli Proteins; Gene Expression Regulation, Bacterial; Glucose; Metabolic Engineering; Mutation; NAD; NADH Dehydrogenase; Oxidation-Reduction; Oxygen; Protein Engineering; Protein Kinases; Succinic Acid
Año:2016
Volumen:82
Número:1
Página de inicio:244
Página de fin:254
DOI: http://dx.doi.org/10.1128/AEM.02984-15
Título revista:Applied and Environmental Microbiology
Título revista abreviado:Appl. Environ. Microbiol.
ISSN:00992240
CODEN:AEMID
CAS:glucose, 50-99-7, 84778-64-3; nicotinamide adenine dinucleotide, 53-84-9; oxygen, 7782-44-7; protein kinase, 9026-43-1; reduced nicotinamide adenine dinucleotide dehydrogenase, 9027-14-9, 9032-21-7, 9079-67-8; succinic acid, 110-15-6; CreC protein, E coli; Escherichia coli Proteins; Glucose; NAD; NADH Dehydrogenase; Oxygen; Protein Kinases; Succinic Acid
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00992240_v82_n1_p244_Godoy

Referencias:

  • Martínez-Antonio, A., Collado-Vides, J., Identifying global regulators in transcriptional regulatory networks in bacteria (2003) Curr Opin Microbiol, 6, pp. 482-489. , http://dx.doi.org/10.1016/j.mib.2003.09.002
  • Bettenbrock, K., Bai, H., Ederer, M., Green, J., Hellingwerf, K.J., Holcombe, M., Kunz, S., Poole, R.K., Towards a systems level understanding of the oxygen response of Escherichia coli (2014) Adv Microb Physiol, 64, pp. 65-114. , http://dx.doi.org/10.1016/B978-0-12-800143-1.00002-6
  • Rolfe, M.D., Ter Beek, A., Graham, A.I., Trotter, E.W., Asif, H.M.S., Sanguinetti, G., Teixeira de Mattos, M.J., Green, J., 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. , http://dx.doi.org/10.1074/jbc.M110.211144
  • 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. , http://dx.doi.org/10.1016/j.ymben.2006.07.002
  • Nikel, P.I., de Almeida, A., Giordano, A.M., Pettinari, M.J., Redox driven metabolic tuning: carbon source and aeration affect synthesis of poly(3-hydroxybutyrate) in Escherichia coli (2010) Bioeng Bugs, 1, pp. 291-295. , http://dx.doi.org/10.4161/bbug.1.4.12103
  • Cariss, S.J., Tayler, A.E., Avison, M.B., Defining the growth conditions and promoter-proximal DNA sequences required for activation of gene expression by CreBC in Escherichia coli (2008) J Bacteriol, 190, pp. 3930-3939. , http://dx.doi.org/10.1128/JB.00108-08
  • Avison, M.B., Horton, R.E., Walsh, T.R., Bennett, P.M., Escherichia coli CreBC is a global regulator of gene expression that responds to growth in minimal media (2001) J Biol Chem, 276, pp. 26955-26961. , http://dx.doi.org/10.1074/jbc.M011186200
  • Hsieh, Y.J., Wanner, B.L., Global regulation by the seven-component Pi signaling system (2010) Curr Opin Microbiol, 13, pp. 198-203. , http://dx.doi.org/10.1016/j.mib.2010.01.014
  • Wanner, B.L., Signal transduction in the control of phosphateregulated genes of Escherichia coli (1996) Kidney Int, 49, pp. 964-967. , http://dx.doi.org/10.1038/ki.1996.136
  • Wanner, B.L., Wilmes, M.R., Young, D.C., Control of bacterial alkaline phosphatase synthesis and variation in an Escherichia coli K-12 phoR mutant by adenyl cyclase, the cyclic AMP receptor protein, and the phoM operon (1988) J Bacteriol, 170, pp. 1092-1102
  • Zhou, L., Lei, X.H., Bochner, B.R., Wanner, B.L., Phenotype microarray analysis of Escherichia coli K-12 mutants with deletions of all twocomponent systems (2003) J Bacteriol, 185, pp. 4956-4972. , http://dx.doi.org/10.1128/JB.185.16.4956-4972.2003
  • Cariss, S.J., Constantinidou, C., Patel, M.D., Takebayashi, Y., Hobman, J.L., Penn, C.W., Avison, M.B., YieJ (CbrC) mediates CreBC-dependent colicin E2 tolerance in Escherichia coli (2010) J Bacteriol, 192, pp. 3329-3336. , http://dx.doi.org/10.1128/JB.01352-09
  • 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 (2012) Appl Environ Microbiol, 78, pp. 8784-8794. , http://dx.doi.org/10.1128/AEM.02558-12
  • Carlson, R., Wlaschin, A., Srienc, F., Kinetic studies and biochemical pathway analysis of anaerobic poly-(R)-3-hydroxybutyric acid synthesis in Escherichia coli (2005) Appl Environ Microbiol, 71, pp. 713-720. , http://dx.doi.org/10.1128/AEM.71.2.713-720.2005
  • Pettinari, M.J., Nikel, P.I., Ruiz, J.A., Méndez, B.S., ArcA redox mutants as a source of reduced bioproducts (2008) J Mol Microbiol Biotechnol, 15, pp. 41-47. , http://dx.doi.org/10.1159/000111991
  • Ruiz, J.A., de Almeida, A., Godoy, M.S., Mezzina, M.P., Bidart, G.N., Méndez, B.S., Pettinari, M.J., Nikel, P.I., Escherichia coli redox mutants as microbial cell factories for the synthesis of reduced biochemicals (2012) Comput Struct Biotechnol J, 3. , http://dx.doi.org/10.5936/csbj.201210019
  • 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. , http://dx.doi.org/10.1111/j.1574-6968.2006.00196.x
  • 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. , http://dx.doi.org/10.1128/JB.00040-08
  • Nikel, P.I., Pettinari, M.J., Galvagno, M.A., Méndez, B.S., Poly(3-hydroxybutyrate) synthesis by recombinant Escherichia coli arcA mutants in microaerobiosis (2006) Appl Environ Microbiol, 72, pp. 2614-2620. , http://dx.doi.org/10.1128/AEM.72.4.2614-2620.2006
  • 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. , http://dx.doi.org/10.1007/s00253-007-1255-7
  • López, N.I., Pettinari, M.J., Nikel, P.I., Méndez, B.S., Polyhydroxyalkanoates: much more than biodegradable plastics (2015) Adv Appl Microbiol, 93, pp. 73-106. , http://dx.doi.org/10.1016/bs.aambs.2015.06.001
  • Nikel, P.I., Pettinari, M.J., Galvagno, M.A., Méndez, B.S., Metabolic selective pressure stabilizes plasmids carrying biosynthetic genes for reduced biochemicals in Escherichia coli redox mutants (2010) Appl Microbiol Biotechnol, 88, pp. 563-573. , http://dx.doi.org/10.1007/s00253-010-2774-1
  • Nikel, P.I., Ramírez, M.C., Pettinari, M.J., Méndez, B.S., Galvagno, M.A., Ethanol synthesis from glycerol by Escherichia coli redox mutants expressing adhE from Leuconostoc mesenteroides (2010) J Appl Microbiol, 109, pp. 492-504. , http://dx.doi.org/10.1111/j.1365-2672.2010.04668.x
  • Datsenko, K.A., 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. , http://dx.doi.org/10.1073/pnas.120163297
  • Cherepanov, P.P., Wackernagel, W., Gene disruption in Escherichia coli: TcR andKmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant (1995) Gene, 158, pp. 9-14. , http://dx.doi.org/10.1016/0378-1119(95)00193-A
  • Bernofsky, C., Swan, M., An improved cycling assay for nicotinamide adenine dinucleotide (1973) Anal Biochem, 53, pp. 452-458. , http://dx.doi.org/10.1016/0003-2697(73)90094-8
  • Nikel, P.I., Pérez-Pantoja, D., de Lorenzo, V., Why are chlorinated pollutants so difficult to degrade aerobically? Redox stress limits 1,3-dichloroprop-1-ene metabolism by Pseudomonas pavonaceae (2013) Philos Trans R Soc Lond B Biol Sci, 368. , http://dx.doi.org/10.1098/rstb.2012.0377
  • Nikel, P.I., Chavarría, M., Fuhrer, T., Sauer, U., de Lorenzo, V., Pseudomonas putida KT2440 strain metabolizes glucose through a cycle formed by enzymes of the Entner-Doudoroff, Embden-Meyerhof-Parnas, and pentose phosphate pathways (2015) J Biol Chem, 290, pp. 25920-25932. , http://dx.doi.org/10.1074/jbc.M115.687749
  • Nikel, P.I., Chavarría, M., Quantitative physiology approaches to understand and optimize reducing power availability in environmental bacteria (2015) Hydrocarbon and lipid microbiology protocols, , http://dx.doi.org/10.1007/8623_2015_84, McGenity TJ (ed), in press. Humana Press, New York, NY
  • Dittrich, C.R., Bennett, G.N., San, K.Y., Characterization of the acetateproducing pathways in Escherichia coli (2005) Biotechnol Prog, 21, pp. 1062-1067
  • Lipmann, F., Tuttle, L.C., The detection of activated carboxyl groups with hydroxylamine as interceptor (1945) J Biol Chem, 161, p. 415
  • Tarmy, E.M., Kaplan, N.O., Chemical characterization of D-lactate dehydrogenase from Escherichia coli B (1968) J Biol Chem, 243, pp. 2579-2586
  • Jiang, G.R., Nikolova, S., Clark, D.P., Regulation of the ldhA gene, encoding the fermentative lactate dehydrogenase of Escherichia coli (2001) Microbiology, 147, pp. 2437-2446. , http://dx.doi.org/10.1099/00221287-147-9-2437
  • McKinlay, J.B., Vieille, C., Zeikus, J.G., Prospects for a bio-based succinate industry (2007) Appl Microbiol Biotechnol, 76, pp. 727-740. , http://dx.doi.org/10.1007/s00253-007-1057-y
  • Thakker, C., Martínez, I., San, K.Y., Bennett, G.N., Succinate production in Escherichia coli (2012) Biotechnol J, 7, pp. 213-224. , http://dx.doi.org/10.1002/biot.201100061
  • Chao, Y.P., Liao, J.C., Alteration of growth yield by overexpression of phosphoenolpyruvate carboxylase and phosphoenolpyruvate carboxykinase in Escherichia coli (1993) Appl Environ Microbiol, 59, pp. 4261-4265
  • Gokarn, R.R., Eiteman, M.A., Altman, E., Metabolic analysis of Escherichia coli in the presence and absence of the carboxylating enzymes phosphoenolpyruvate carboxylase and pyruvate carboxylase (2000) Appl Environ Microbiol, 66, pp. 1844-1850. , http://dx.doi.org/10.1128/AEM.66.5.1844-1850.2000
  • Wang, D., Li, Q., Mao, Y., Xing, J., Su, Z., High-level succinic acid production and yield by lactose-induced expression of phosphoenolpyruvate carboxylase in ptsG mutant Escherichia coli (2010) Appl Microbiol Biotechnol, 87, pp. 2025-2035. , http://dx.doi.org/10.1007/s00253-010-2689-x
  • Wang, W., Li, Z., Xie, J., Ye, Q., Production of succinate by a pflB ldhA double mutant of Escherichia coli overexpressing malate dehydrogenase (2009) Bioprocess Biosyst Eng, 32, pp. 737-745. , http://dx.doi.org/10.1007/s00449-009-0298-9
  • Jantama, K., Haupt, M.J., Svoronos, S.A., Zhang, X., Moore, J.C., Shanmugam, K.T., Ingram, L.O., Combining metabolic engineering and metabolic evolution to develop nonrecombinant strains of Escherichia coli C that produce succinate and malate (2008) Biotechnol Bioeng, 99, pp. 1140-1153. , http://dx.doi.org/10.1002/bit.21694
  • Samuelov, N.S., Lamed, R., Lowe, S., Zeikus, J.G., Influence of CO2-HCO3 - levels and pH on growth, succinate production, and enzyme activities of Anaerobiospirillum succiniciproducens (1991) Appl Environ Microbiol, 57, pp. 3013-3019
  • Kwon, Y.D., Kwon, O.H., Lee, H.S., Kim, P., The effect of NADP-dependent malic enzyme expression and anaerobic C4 metabolism in Escherichia coli compared with other anaplerotic enzymes (2007) J Appl Microbiol, 103, pp. 2340-2345. , http://dx.doi.org/10.1111/j.1365-2672.2007.03485.x
  • Berríos-Rivera, S.J., Bennett, G.N., San, K.Y., The effect of increasing NADH availability on the redistribution of metabolic fluxes in Escherichia coli chemostat cultures (2002) Metab Eng, 4, pp. 230-237. , http://dx.doi.org/10.1006/mben.2002.0228
  • Sakai, Y., Murdanoto, A.P., Konishi, T., Iwamatsu, A., Kato, N., Regulation of the formate dehydrogenase gene, FDH1, in the methylotrophic yeast Candida boidinii and growth characteristics of an FDH1-disrupted strain on methanol, methylamine, and choline (1997) J Bacteriol, 179, pp. 4480-4485
  • Balzer, G.J., Thakker, C., Bennett, G.N., San, K.Y., Metabolic engineering of E. coli to minimize byproduct formate and improving succinate productivity through increasing NADH availability by heterologous expression of NAD+-dependent formate dehydrogenase (2013) Metab Eng, 20, pp. 1-8. , http://dx.doi.org/10.1016/j.ymben.2013.07.005
  • Sánchez, A.M., Bennett, G.N., San, K.Y., Novel pathway engineering design of the anaerobic central metabolic pathway in Escherichia coli to increase succinate yield and productivity (2005) Metab Eng, 7, pp. 229-239. , http://dx.doi.org/10.1016/j.ymben.2005.03.001
  • 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. , http://dx.doi.org/10.1128/JB.00174-09
  • Amemura, M., Makino, K., Shinagawa, H., Nakata, A., Cross talk to the phosphate regulon of Escherichia coli by PhoM protein: PhoM is a histidine protein kinase and catalyzes phosphorylation of PhoB and PhoMopen reading frame 2 (1990) J Bacteriol, 172, pp. 6300-6307
  • Holm, A.K., Blank, L.M., Oldiges, M., Schmid, A., Solem, C., Jensen, P.R., Vemuri, G.N., Metabolic and transcriptional response to cofactor perturbations in Escherichia coli (2010) J Biol Chem, 285, pp. 17498-17506. , http://dx.doi.org/10.1074/jbc.M109.095570
  • Zhou, Y., Wang, L., Yang, F., Lin, X., Zhang, S., Zhao, Z.K., Determining the extremes of the cellular NAD(H) level by using an Escherichia coli NAD+-auxotrophic mutant (2011) Appl Environ Microbiol, 77, pp. 6133-6140. , http://dx.doi.org/10.1128/AEM.00630-11
  • Vemuri, G.N., Altman, E., Sangurdekar, D.P., Khodursky, A.B., Eiteman, M.A., Overflow metabolism in Escherichia coli during steady-state growth: transcriptional regulation and effect of the redox ratio (2006) Appl Environ Microbiol, 72, pp. 3653-3661. , http://dx.doi.org/10.1128/AEM.72.5.3653-3661.2006
  • Bühler, B., Park, J.B., Blank, L.M., Schmid, A., NADH availability limits asymmetric biocatalytic epoxidation in a growing recombinant Escherichia coli strain (2008) Appl Environ Microbiol, 74, pp. 1436-1446. , http://dx.doi.org/10.1128/AEM.02234-07
  • Nikel, P.I., Pettinari, M.J., Ramírez, 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. , http://dx.doi.org/10.1159/000111992
  • 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. , http://dx.doi.org/10.1002/bit.20381
  • Alexeeva, S., Hellingwerf, K.J., Teixeira de Mattos, M.J., Requirement of ArcA for redox regulation in Escherichia coli under microaerobic but not anaerobic or aerobic conditions (2003) J Bacteriol, 185, pp. 204-209. , http://dx.doi.org/10.1128/JB.185.1.204-209.2003
  • Unden, G., Achebach, S., Holighaus, G., Tran, H.Q., Wackwitz, B., Zeuner, Y., Control of FNR function of Escherichia coli by O2 and reducing conditions (2002) J Mol Microbiol Biotechnol, 4, pp. 263-268
  • Liu, X., De Wulf, P., Probing the ArcA-P modulon of Escherichia coli by whole genome transcriptional analysis and sequence recognition profiling (2004) J Biol Chem, 279, pp. 12588-12597. , http://dx.doi.org/10.1074/jbc.M313454200
  • Salmon, K.A., Hung, S.P., Steffen, N.R., Krupp, R., Baldi, P., Hatfield, G.W., Gunsalus, R.P., Global gene expression profiling in Escherichia coli K-12: effects of oxygen availability and ArcA (2005) J Biol Chem, 280, pp. 15084-15096. , http://dx.doi.org/10.1074/jbc.M414030200
  • 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. , http://dx.doi.org/10.1128/JB.187.9.3171-3179.2005
  • Green, J., Paget, M.S., Bacterial redox sensors (2004) Nat Rev Microbiol, 2, pp. 954-966. , http://dx.doi.org/10.1038/nrmicro1022
  • Plumbridge, J., Regulation of gene expression in the PTS in Escherichia coli: the role and interactions of Mlc (2002) Curr Opin Microbiol, 5, pp. 187-193. , http://dx.doi.org/10.1016/S1369-5274(02)00296-5
  • Sabnis, N.A., Yang, H., Romeo, T., Pleiotropic regulation of central carbohydrate metabolism in Escherichia coli via the gene csrA (1995) J Biol Chem, 270, pp. 29096-29104. , http://dx.doi.org/10.1074/jbc.270.49.29096
  • Yang, H., Liu, M.Y., Romeo, T., Coordinate genetic regulation of glycogen catabolism and biosynthesis in Escherichia coli via the CsrA gene product (1996) J Bacteriol, 178, pp. 1012-1017
  • Baker, C.S., Morozov, I., Suzuki, K., Romeo, T., Babitzke, P., CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli (2002) Mol Microbiol, 44, pp. 1599-1610. , http://dx.doi.org/10.1046/j.1365-2958.2002.02982.x
  • Chang, Y.Y., Wang, A.Y., Cronan, J.E., Expression of Escherichia coli pyruvate oxidase (PoxB) depends on the sigma factor encoded by the rpoS (katF) gene (1994) Mol Microbiol, 11, pp. 1019-1028. , http://dx.doi.org/10.1111/j.1365-2958.1994.tb00380.x
  • Berríos-Rivera, S.J., Sánchez, A.M., Bennett, G.N., San, K.Y., Effect of different levels of NADH availability on metabolite distribution in Escherichia coli fermentation in minimal and complex media (2004) Appl Microbiol Biotechnol, 65, pp. 426-432. , http://dx.doi.org/10.1007/s00253-004-1609-3
  • Kim, T.Y., Park, J.M., Kim, H.U., Cho, K.M., Lee, S.Y., Design of homoorganic acid producing strains using multi-objective optimization (2015) Metab Eng, 28, pp. 63-73. , http://dx.doi.org/10.1016/j.ymben.2014.11.012
  • 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. , http://dx.doi.org/10.1016/j.ymben.2005.11.004
  • 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. , http://dx.doi.org/10.1073/pnas.67.2.606
  • Hayes, W., Observations on a transmissible agent determining sexual differentiation in Bacterium coli (1953) J Gen Microbiol, 8, pp. 72-88. , http://dx.doi.org/10.1099/00221287-8-1-72
  • Phillips, G.J., Park, S.K., Huber, D., High copy number plasmids compatible with commonly used cloning vectors (2000) Biotechniques, 28, pp. 400-402
  • Amann, E., Ochs, B., Abel, K.J., Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli (1988) Gene, 69, pp. 301-315. , http://dx.doi.org/10.1016/0378-1119(88)90440-4

Citas:

---------- APA ----------
Godoy, M.S., Nikel, P.I., Cabrera Gomez, J.G. & Julia Pettinari, M. (2016) . The CreC regulator of Escherichia coli, a new target for metabolic manipulations. Applied and Environmental Microbiology, 82(1), 244-254.
http://dx.doi.org/10.1128/AEM.02984-15
---------- CHICAGO ----------
Godoy, M.S., Nikel, P.I., Cabrera Gomez, J.G., Julia Pettinari, M. "The CreC regulator of Escherichia coli, a new target for metabolic manipulations" . Applied and Environmental Microbiology 82, no. 1 (2016) : 244-254.
http://dx.doi.org/10.1128/AEM.02984-15
---------- MLA ----------
Godoy, M.S., Nikel, P.I., Cabrera Gomez, J.G., Julia Pettinari, M. "The CreC regulator of Escherichia coli, a new target for metabolic manipulations" . Applied and Environmental Microbiology, vol. 82, no. 1, 2016, pp. 244-254.
http://dx.doi.org/10.1128/AEM.02984-15
---------- VANCOUVER ----------
Godoy, M.S., Nikel, P.I., Cabrera Gomez, J.G., Julia Pettinari, M. The CreC regulator of Escherichia coli, a new target for metabolic manipulations. Appl. Environ. Microbiol. 2016;82(1):244-254.
http://dx.doi.org/10.1128/AEM.02984-15