Adaptive laboratory evolution resolves energy depletion to maintain high aromatic metabolite phenotypes in Escherichia coli strains lacking the Phosphotransferase System

Metabolic Engineering

Volumn 48, Issue , 2018, Pages 233-242

  McCloskey, Douglas ^a,b   Xu, Sibei ^a   Sandberg, Troy E ^a   Brunk, Elizabeth ^a   Hefner, Ying ^a   Szubin, Richard ^a   Feist, Adam M ^a,b   Palsson, Bernhard O ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b Chalmers University of Technology   (Denmark)

Author keywords

Adaptive laboratory evolution; crr gene knockouts; E. coli; Multi omics analysis; Mutation analysis; ptsH; ptsI; Systems biology

Indexed keywords

AROMATIC COMPOUNDS; BIOMOLECULES; ESCHERICHIA COLI; METABOLITES;

ADAPTIVE LABORATORY EVOLUTION; E. COLI; GENE KNOCKOUT; MULTI-OMICS ANALYSIS; MUTATION ANALYSIS; PTSH; PTSI; SYSTEMS BIOLOGY;

AROMATIZATION;

AROMATIC AMINO ACID; AROMATIC COMPOUND; GLUCOSE; PHOSPHOENOLPYRUVATE; PHOSPHOTRANSFERASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

AMINO ACID SYNTHESIS; ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIAL MUTATION; BACTERIAL STRAIN; CATABOLITE REPRESSION; CELL DIVISION; CLADISTICS; CONTROLLED STUDY; ENERGY BALANCE; ESCHERICHIA COLI; EVOLUTIONARY ADAPTATION; FERMENTATION; GENE DUPLICATION; GLUCOSE TRANSPORT; GLYCOLYSIS; HOST; LABORATORY TECHNIQUE; METABOLITE; MICROBIAL RESPIRATION; NONHUMAN; OMICS; PHENOTYPE; PHOSPHORYLATION; PRECURSOR; PRIORITY JOURNAL; RCS GENE; SOS RESPONSE (GENETICS); YRFF GENE;

EID: 85048761909     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2018.06.005     Document Type: Article

References (66)

1. Aguilar, C., et al. Genetic changes during a laboratory adaptive evolution process that allowed fast growth in glucose to an Escherichia coli strain lacking the major glucose transport system. BMC Genom., 13, 2012, 385.
2. Aiba, H., Transcription of the Escherichia coli adenylate cyclase gene is negatively regulated by cAMP-cAMP receptor protein. J. Biol. Chem. 260 (1985), 3063–3070.
3. Báez, J.L., Bolívar, F., Gosset, G., Determination of 3-deoxy-D-arabino-heptulosonate 7-phosphate productivity and yield from glucose in Escherichia coli devoid of the glucose phosphotransferase transport system. Biotechnol. Bioeng. 73 (2001), 530–535.
4. Baharoglu, Z., Petranovic, M., Flores, M.-J., Michel, B., RuvAB is essential for replication forks reversal in certain replication mutants. EMBO J. 25 (2006), 596–604.
5. Balderas-Hernández, V.E., et al. Metabolic engineering for improving anthranilate synthesis from glucose in Escherichia coli. Microb. Cell Fact., 8, 2009, 19.
6. Balderas-Hernández, V.E., Hernández-Montalvo, V., Bolívar, F., Gosset, G., Martínez, A., Adaptive evolution of Escherichia coli inactivated in the phosphotransferase system operon improves co-utilization of xylose and glucose under anaerobic conditions. Appl. Biochem. Biotechnol. 163 (2011), 485–496.
7. Basan, M., et al. Overflow metabolism in Escherichia coli results from efficient proteome allocation. Nature 528 (2015), 99–104.
8. Berry, A., Improving production of aromatic compounds in Escherichia coli by metabolic engineering. Trends Biotechnol. 14 (1996), 250–256.
9. Bi, E.F., Lutkenhaus, J., FtsZ ring structure associated with division in Escherichia coli. Nature 354 (1991), 161–164.
10. Chávez-Béjar, M.I., et al. Metabolic engineering of Escherichia coli to optimize melanin synthesis from glucose. Microb. Cell Fact., 12, 2013, 108.
11. Chávez-Béjar, M.I., Báez-Viveros, J.L., Martínez, A., Bolívar, F., Gosset, G., Biotechnological production of L-tyrosine and derived compounds. Process Biochem. 47 (2012/7), 1017–1026.
12. Cho, S.-H., et al. Detecting envelope stress by monitoring β-barrel assembly. Cell 159 (2014), 1652–1664.
13. Cortés-Tolalpa, L., et al. Global transcriptomic analysis of an engineered Escherichia coli strain lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system during shikimic acid production in rich culture medium. Microb. Cell Fact., 13, 2014, 28.
14. Erni, B., The bacterial phosphoenolpyruvate: sugar phosphotransferase system (PTS): an interface between energy and signal transduction. J. Iran. Chem. Soc. 10 (2013), 593–630.
15. Escalante, A., et al. Metabolic engineering for the production of shikimic acid in an evolved Escherichia coli strain lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system. Microb. Cell Fact., 9, 2010, 21.
16. Escalante, A., Salinas Cervantes, A., Gosset, G., Bolívar, F., Current knowledge of the Escherichia coli phosphoenolpyruvate-carbohydrate phosphotransferase system: peculiarities of regulation and impact on growth and product formation. Appl. Microbiol. Biotechnol. 94 (2012), 1483–1494.
17. Evans, K.L., Kannan, S., Li, G., de Pedro, M.A., Young, K.D., Eliminating a set of four penicillin binding proteins triggers the Rcs phosphorelay and Cpx stress responses in Escherichia coli. J. Bacteriol. 195 (2013), 4415–4424.
18. Farris, C., Sanowar, S., Bader, M.W., Pfuetzner, R., Miller, S.I., Antimicrobial peptides activate the Rcs regulon through the outer membrane lipoprotein RcsF. J. Bacteriol. 192 (2010), 4894–4903.
19. Flores, N., et al. Role of pyruvate oxidase in Escherichia coli strains lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system. J. Mol. Microbiol. Biotechnol. 8 (2004), 209–221.
20. Flores, N., et al. 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. Metab. Eng. 7 (2005), 70–87.
21. Flores, N., et al. 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. J. Mol. Microbiol. Biotechnol. 13 (2007), 105–116.
22. Flores, N., et al. New insights into the role of sigma factor RpoS as revealed in Escherichia coli strains lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system. J. Mol. Microbiol. Biotechnol. 14 (2008), 176–192.
23. Flores, N., Xiao, J., Berry, A., Bolivar, F., Valle, F., Pathway engineering for the production of aromatic compounds in Escherichia coli. Nat. Biotechnol. 14 (1996), 620–623.
24. Flores, S., et al. Nutrient-scavenging stress response in an Escherichia coli strain lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system, as explored by gene expression profile analysis. J. Mol. Microbiol. Biotechnol. 10 (2005), 51–63.
25. Flores, S., Gosset, G., Flores, N., de Graaf, A.A., Bolívar, F., Analysis of carbon metabolism in Escherichia coli strains with an inactive phosphotransferase system by (13)C labeling and NMR spectroscopy. Metab. Eng. 4 (2002), 124–137.
26. Franchini, A.G., Ihssen, J., Egli, T., Effect of global regulators RpoS and cyclic-AMP/CRP on the catabolome and transcriptome of Escherichia coli K12 during carbon- and energy-limited growth. PLoS One, 10, 2015, e0133793.
27. Fuentes, L.G., et al. Modification of glucose import capacity in Escherichia coli: physiologic consequences and utility for improving DNA vaccine production. Microb. Cell Fact., 12, 2013, 42.
28. Godoy, V.G., Jarosz, D.F., Walker, F.L., Simmons, L.A., Walker, G.C., Y-family DNA polymerases respond to DNA damage-independent inhibition of replication fork progression. EMBO J. 25 (2006), 868–879.
29. Hernández-Montalvo, V., et al. Expression of galP and glk in a Escherichia coli PTS mutant restores glucose transport and increases glycolytic flux to fermentation products. Biotechnol. Bioeng. 83 (2003), 687–694.
30. Ikeda, M., Towards bacterial strains overproducing L-tryptophan and other aromatics by metabolic engineering. Appl. Microbiol. Biotechnol. 69 (2006), 615–626.
31. Kim, S.H., Schneider, B.L., Reitzer, L., Genetics and regulation of the major enzymes of alanine synthesis in Escherichia coli. J. Bacteriol. 192 (2010), 5304–5311.
32. Kreuzer, K.N., DNA damage responses in prokaryotes: regulating gene expression, modulating growth patterns, and manipulating replication forks. Cold Spring Harb. Perspect. Biol., 5, 2013, a012674.
33. Krin, E., Sismeiro, O., Danchin, A., Bertin, P.N., The regulation of Enzyme IIA(Glc) expression controls adenylate cyclase activity in Escherichia coli. Microbiology 148 (2002), 1553–1559.
34. LaCroix, R.A., et al. Use of adaptive laboratory evolution to discover key mutations enabling rapid growth of Escherichia coli K-12 MG1655 on glucose minimal medium. Appl. Environ. Microbiol. 81 (2015), 17–30.
35. Laubacher, M.E., Ades, S.E., The Rcs phosphorelay is a cell envelope stress response activated by peptidoglycan stress and contributes to intrinsic antibiotic resistance. J. Bacteriol. 190 (2008), 2065–2074.
36. Lévy, S., Zeng, G.Q., Danchin, A., Cyclic AMP synthesis in Escherichia coli strains bearing known deletions in the pts phosphotransferase operon. Gene 86 (1990), 27–33.
37. Licona-Cassani, C., et al. Inactivation of pyruvate kinase or the phosphoenolpyruvate: sugar phosphotransferase system increases shikimic and dehydroshikimic acid yields from glucose in Bacillus subtilis. J. Mol. Microbiol. Biotechnol. 24 (2014), 37–45.
38. Majdalani, N., Gottesman, S., The Rcs phosphorelay: a complex signal transduction system. Annu. Rev. Microbiol. 59 (2005), 379–405.
39. Majdalani, N., Gottesman, S., Genetic dissection of signaling through the Rcs phosphorelay. Methods Enzymol. 423 (2007), 349–362.
40. Martínez, K., et al. Coutilization of glucose and glycerol enhances the production of aromatic compounds in an Escherichia coli strain lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system. Microb. Cell Fact., 7, 2008, 1.
41. McCloskey, D., Utrilla, J., Naviaux, R.K., Palsson, B.O., Feist, A.M., Fast Swinnex filtration (FSF): a fast and robust sampling and extraction method suitable for metabolomics analysis of cultures grown in complex media. Metabolomics 11 (2014), 198–209.
42. McCloskey, D., Gangoiti, J.A., Palsson, B.O., Feist, A.M., A pH and solvent optimized reverse-phase ion-paring-LC–MS/MS method that leverages multiple scan-types for targeted absolute quantification of intracellular metabolites. Metabolomics 11 (2015), 1338–1350.
43. McCloskey, D., Young, J.D., Xu, S., Palsson, B.O., Feist, A.M., MID Max: LC-MS/MS method for measuring the precursor and product mass isotopomer distributions of metabolic intermediates and cofactors for metabolic flux analysis applications. Anal. Chem. 88 (2016), 1362–1370.
44. McCloskey, D., Young, J.D., Xu, S., Palsson, B.O., Feist, A.M., Modeling method for increased precision and scope of directly measurable fluxes at a genome-scale. Anal. Chem. 88 (2016), 3844–3852.
45. McKenzie, G.J., Lee, P.L., Lombardo, M.J., Hastings, P.J., Rosenberg, S.M., SOS mutator DNA polymerase IV functions in adaptive mutation and not adaptive amplification. Mol. Cell 7 (2001), 571–579.
46. Muñoz, A.J., et al. Metabolic engineering of Escherichia coli for improving L-3,4-dihydroxyphenylalanine (L-DOPA) synthesis from glucose. J. Ind. Microbiol. Biotechnol. 38 (2011), 1845–1852.
47. Nobelmann, B., Lengeler, J.W., Molecular analysis of the gat genes from Escherichia coli and of their roles in galactitol transport and metabolism. J. Bacteriol. 178 (1996), 6790–6795.
48. Ohara, M., Wu, H.C., Sankaran, K., Rick, P.D., Identification and characterization of a new lipoprotein, NlpI, in Escherichia coli K-12. J. Bacteriol. 181 (1999), 4318–4325.
49. Olvera, L., et al. Transcription analysis of central metabolism genes in Escherichia coli. Possible roles of sigma38 in their expression, as a response to carbon limitation. PLoS One, 4, 2009, e7466.
50. Pannen, D., Fabisch, M., Gausling, L., Schnetz, K., Interaction of the RcsB response regulator with auxiliary transcription regulators in Escherichia coli. J. Biol. Chem. 291 (2016), 2357–2370.
51. Park, Y.-H., Lee, B.R., Seok, Y.-J., Peterkofsky, A., In vitro reconstitution of catabolite repression in Escherichia coli. J. Biol. Chem. 281 (2006), 6448–6454.
52. Pastan, I., Perlman, R., Cyclic adenosine monophosphate in bacteria. Science 169 (1970), 339–344.
53. Pristovšek, P., et al. Structural Analysis of the DNA-binding domain of theErwinia amylovora RcsB protein and its interaction with the RcsAB box. J. Biol. Chem. 278 (2003), 17752–17759.
54. Reddy, P., Kamireddi, M., Modulation of Escherichia coli adenylyl cyclase activity by catalytic-site mutants of protein IIA(Glc) of the phosphoenolpyruvate:sugar phosphotransferase system. J. Bacteriol. 180 (1998), 732–736.
55. Sabido, A., et al. Physiological and transcriptional characterization of Escherichia coli strains lacking interconversion of phosphoenolpyruvate and pyruvate when glucose and acetate are coutilized. Biotechnol. Bioeng. 111 (2014), 1150–1160.
56. Sandberg, T.E., et al. Evolution of Escherichia coli to 42 °C and subsequent genetic engineering reveals adaptive mechanisms and novel mutations. Mol. Biol. Evol. 31 (2014), 2647–2662.
57. Seigneur, M., Bidnenko, V., Ehrlich, S.D., Michel, B., RuvAB acts at arrested replication forks. Cell 95 (1998), 419–430.
58. Sigala, J.C., et al. Acetate metabolism in Escherichia coli strains lacking phosphoenolpyruvate: carbohydrate phosphotransferase system; evidence of carbon recycling strategies and futile cycles. J. Mol. Microbiol. Biotechnol. 16 (2009), 224–235.
59. Singh, S.K., SaiSree, L., Amrutha, R.N., Reddy, M., Three redundant murein endopeptidases catalyse an essential cleavage step in peptidoglycan synthesis of Escherichia coli K12. Mol. Microbiol. 86 (2012), 1036–1051.
60. Singh, S.K., Parveen, S., SaiSree, L., Reddy, M., Regulated proteolysis of a cross-link-specific peptidoglycan hydrolase contributes to bacterial morphogenesis. Proc. Natl. Acad. Sci. USA 112 (2015), 10956–10961.
61. Stülke, J., Hillen, W., Carbon catabolite repression in bacteria. Curr. Opin. Microbiol. 2 (1999), 195–201.
62. Tao, J., et al. Heat shock proteins IbpA and IbpB are required for NlpI-participated cell division in Escherichia coli. Front. Microbiol., 6, 2015, 51.
63. Ueguchi, C., Misonou, N., Mizuno, T., Negative control of rpoS expression by phosphoenolpyruvate: carbohydrate phosphotransferase system in Escherichia coli. J. Bacteriol. 183 (2001), 520–527.
64. Valgepea, K., Adamberg, K., Vilu, R., Decrease of energy spilling in Escherichia coli continuous cultures with rising specific growth rate and carbon wasting. BMC Syst. Biol., 5, 2011, 106.
65. Vargas-Tah, A., et al. Production of cinnamic and p-hydroxycinnamic acid from sugar mixtures with engineered Escherichia coli. Microb. Cell Fact., 14, 2015, 6.
66. Yong, H.T., et al. Development of a system for discovery of genetic interactions for essential genes in Escherichia coli K-12. Genes Genet. Syst. 88 (2013), 233–240.