1887

Abstract

lacking the glucose phosphotransferase system (PTS), mannose PTS and glucokinase are supposedly unable to grow on glucose as the sole carbon source (Curtis SJ, Epstein W. 1975;122:1189–1199). We report that W (ALS1406) grows slowly on glucose in media containing glucose with a second carbon source: ALS1406 metabolizes glucose after that other carbon source, including arabinose, fructose, glycerol, succinate or xylose, is exhausted. Galactose is an exception to this rule, as ALS1406 simultaneously consumes both galactose and glucose. The ability of ALS1406 to metabolize glucose in a xylose–glucose mixture was unchanged by an additional knockout in any single gene involved in carbohydrate transport and utilization, including (periplasmic glucose-1-phosphatase), (galactose permease), (xylose isomerase), (allose kinase), (glucose PTS enzyme IIA), (galactose kinase), (mannokinase), (maltose transporter), (maltose PTS enzyme IIBC), (methyl-galactose transporter subunit), (N-acetyl glucosamine PTS enzyme IICBA), (N-acetyl mannosamine kinase) or (phosphoglucose mutase). Glucose metabolism was only blocked by the deletion of two metabolic genes, (phosphoglucose isomerase) and (glucose-6-phosphate 1-dehydrogenase), which prevents the entry of glucose-6-phosphate into the pentose phosphate and Embden–Meyerhof–Parnas pathways. Carbon-limited steady-state studies demonstrated that xylose must be sub-saturating for glucose to be metabolized, while nitrogen-limited studies showed that xylose is partly converted to glucose when xylose is in excess. Under transient conditions, ALS1406 converts almost 25 % (mass) xylose into glucose as a result of reversible transketolase and transaldolase and the re-entry of carbon into the pentose phosphate pathway via glucose-6-phosphate 1-dehydrogenase.

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2017-06-01
2024-03-29
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References

  1. Curtis SJ, Epstein W. Phosphorylation of D-glucose in Escherichia coli mutants defective in glucosephosphotransferase, mannosephosphotransferase, and glucokinase. J Bacteriol 1975; 122:1189–1199[PubMed]
    [Google Scholar]
  2. Postma PW, Lengeler JW, Jacobson GR. Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 1993; 57:543–594[PubMed]
    [Google Scholar]
  3. Huber F, Erni B. Membrane topology of the mannose transporter of Escherichia coli K12. Eur J Biochem 1996; 239:810–817 [View Article][PubMed]
    [Google Scholar]
  4. Flores N, Xiao J, Berry A, Bolivar F, Valle F. Pathway engineering for the production of aromatic compounds in Escherichia coli. Nat Biotechnol 1996; 14:620–623 [View Article][PubMed]
    [Google Scholar]
  5. Eiteman MA, Lee SA, Altman E. A co-fermentation strategy to consume sugar mixtures effectively. J Biol Eng 2008; 2:3 [View Article][PubMed]
    [Google Scholar]
  6. Eiteman MA, Lee SA, Altman R, Altman E. A substrate-selective co-fermentation strategy with Escherichia coli produces lactate by simultaneously consuming xylose and glucose. Biotechnol Bioeng 2009; 102:822–827 [View Article][PubMed]
    [Google Scholar]
  7. Olsson L, Hahn-Hägerdal B. Fermentation of lignocellulosic hydrolysates for ethanol production. Enzyme Microb Technol 1996; 18:312–331 [View Article]
    [Google Scholar]
  8. Xia T, Altman E, Eiteman MA. Succinate production from xylose-glucose mixtures using a consortium of engineered Escherichia coli. Eng Life Sci 2015; 15:65–72 [View Article]
    [Google Scholar]
  9. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2006; 2:1–11 [View Article][PubMed]
    [Google Scholar]
  10. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 2000; 97:6640–6645 [View Article][PubMed]
    [Google Scholar]
  11. Yu D, Ellis HM, Lee EC, Jenkins NA, Copeland NG et al. An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci USA 2000; 97:5978–5983 [View Article][PubMed]
    [Google Scholar]
  12. Higgins NP, Yang X, Fu Q, Roth JR. Surveying a supercoil domain by using the gamma delta resolution system in Salmonella typhimurium. J Bacteriol 1996; 178:2825–2835 [View Article][PubMed]
    [Google Scholar]
  13. Chang AC, Cohen SN. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 1978; 134:1141–1156[PubMed]
    [Google Scholar]
  14. Eiteman MA, Chastain MJ. Optimization of the ion-exchange analysis of organic acids from fermentation. Anal Chim Acta 1997; 338:69–75 [View Article]
    [Google Scholar]
  15. Lahtvee PJ, Valgepea K, Nahku R, Abner K, Adamberg K et al. Steady state growth space study of Lactococcus lactis in D-stat cultures. Antonie Van Leeuwenhoek 2009; 96:487–496 [View Article][PubMed]
    [Google Scholar]
  16. Bagno A, Rastrelli F, Saielli G. Prediction of the 1H and 13C NMR spectra of α-D-glucose in water by DFT methods and MD simulations. J Org Chem 2007; 72:7373–7381 [View Article][PubMed]
    [Google Scholar]
  17. Curatolo W, Neuringer LJ, Ruben D, Haberkorn R. Two-dimensional J-resolved 1H-nuclear magnetic resonance spectroscopy of α,β-D-glucose at 500 MHz. Carbohydr Res 1983; 112:297–300 [View Article]
    [Google Scholar]
  18. Peng F, Ren JL, Xu F, Bian J, Peng P et al. Fractionation of alkali-solubilized hemicelluloses from delignified Populus gansuensis: structure and properties. J Agric Food Chem 2010; 58:5743–5750 [View Article][PubMed]
    [Google Scholar]
  19. Pfeffer PE, Valentine KM, Parrish FW. Deuterium-induced differential isotope shift 13C NMR. 1. Resonance reassignments of mono- and disaccharides. J Am Chem Soc 1979; 101:1265–1274 [View Article]
    [Google Scholar]
  20. Rossi C, Marchettini N, Donati A, Medaglini D, Valassina M et al. 13C-NMR determination of simultaneous xylose and glucose fermentation by a newly isolated strain (G11) of Klebsiella planticola. Biomass and Bioenergy 1995; 8:197–202 [View Article]
    [Google Scholar]
  21. Ulrich EL, Akutsu H, Doreleijers JF, Harano Y, Ioannidis YE et al. BioMagResBank. Nucleic Acids Res 2008; 36:D402–D408 [View Article][PubMed]
    [Google Scholar]
  22. Wishart DS, Bigam CG, Yao J, Abildgaard F, Dyson HJ et al. 1H, 13C and 15N chemical shift referencing in biomolecular NMR. J Biomol NMR 1995; 6:135–140 [View Article][PubMed]
    [Google Scholar]
  23. Lendenmann U, Egli T. Is Escherichia coli growing in glucose-limited chemostat culture able to utilize other sugars without lag?. Microbiology 1995; 141:71–78 [View Article][PubMed]
    [Google Scholar]
  24. Miller BG, Raines RT. Reconstitution of a defunct glycolytic pathway via recruitment of ambiguous sugar kinases. Biochemistry 2005; 44:10776–10783 [View Article][PubMed]
    [Google Scholar]
  25. Wovcha MG, Steuerwald DL, Brooks KE. Amplification of D-xylose and D-glucose isomerase activities in Escherichia coli by gene cloning. Appl Environ Microbiol 1983; 45:1402–1404[PubMed]
    [Google Scholar]
  26. Lee DC, Cottrill MA, Forsberg CW, Jia Z. Functional insights revealed by the crystal structures of Escherichia coli glucose-1-phosphatase. J Biol Chem 2003; 278:31412–31418 [View Article]
    [Google Scholar]
  27. Yang J, Fu X, Jia Q, Shen J, Biggins JB et al. Studies on the substrate specificity of Escherichia coli galactokinase. Org Lett 2003; 5:2223–2226 [View Article][PubMed]
    [Google Scholar]
  28. Begley GS, Hansen DE, Jacobson GR, Knowles JR. Stereochemical course of the reactions catalyzed by the bacterial phosphoenolpyruvate:glucose phosphotransferase system. Biochemistry 1982; 21:5552–5556 [View Article][PubMed]
    [Google Scholar]
  29. Erni B. Glucose-specific permease of the bacterial phosphotransferase system: phosphorylation and oligomeric structure of the glucose-specific IIGlc-IIIGlc complex of Salmonella typhimurium. Biochemistry 1986; 25:305–312 [View Article][PubMed]
    [Google Scholar]
  30. Death A, Notley L, Ferenci T. Derepression of LamB protein facilitates outer membrane permeation of carbohydrates into Escherichia coli under conditions of nutrient stress. J Bacteriol 1993; 175:1475–1483 [View Article][PubMed]
    [Google Scholar]
  31. Flores S, Flores N, de Anda R, González A, Escalante A 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 2005; 10:51–63 [View Article][PubMed]
    [Google Scholar]
  32. Flores S, Gosset G, Flores N, de Graaf AA, Bolívar F. Analysis of carbon metabolism in Escherichia coli strains with an inactive phosphotransferase system by 13C labeling and NMR spectroscopy. Metab Eng 2002; 4:124–137 [View Article][PubMed]
    [Google Scholar]
  33. Ganesan AK, Rotman B. Transport systems for galactose and galactosides in Escherichia coli. Genetic determination and regulation of the methylgalactoside permease. J. Mol Biol 1965; 16:42–50 [CrossRef]
    [Google Scholar]
  34. Kalckar HM. The periplasmic galactose binding protein of Escherichia coli. Science 1971; 174:557–565 [View Article][PubMed]
    [Google Scholar]
  35. Boos W, Lengeler J, Hermann KO, Unsöld HJ. The regulation of the β-methylgalactoside transport system and of the galactose binding protein of Escherichia coli K12. Eur J Biochem 1971; 19:457–470[PubMed] [CrossRef]
    [Google Scholar]
  36. Vyas NK, Vyas MN, Quiocho FA. Comparison of the periplasmic receptors for L-arabinose, D-glucose/D-galactose, and D-ribose. structural and functional similarity. J Biol Chem 1991; 266:5226–5237[PubMed]
    [Google Scholar]
  37. Benz R, Schmid A, Vos-Scheperkeuter GH. Mechanism of sugar transport through the sugar-specific LamB channel of Escherichia coli outer membrane. J Membr Biol 1987; 100:21–29 [View Article][PubMed]
    [Google Scholar]
  38. Hernández-Montalvo V, Valle F, Bolivar F, Gosset G. Characterization of sugar mixtures utilization by an Escherichia coli mutant devoid of the phosphotransferase system. Appl Microbiol Biotechnol 2001; 57:186–191[PubMed] [CrossRef]
    [Google Scholar]
  39. Flores N, Leal L, Sigala JC, de Anda R, Escalante A 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 2007; 13:105–116 [View Article][PubMed]
    [Google Scholar]
  40. Busby S, Kolb A. The CAP modulon. In ECC Lin. (editor) Regulation of Gene Expression in Escherichia Coli New York: Landes; 1996 pp. 255–279 [CrossRef]
    [Google Scholar]
  41. Gosset G, Zhang Z, Nayyar S, Cuevas WA, Saier MH Jr. Transcriptome analysis of Crp-dependent catabolite control of gene expression in Escherichia coli. J Bacteriol 2004; 186:3516–3524 [View Article][PubMed]
    [Google Scholar]
  42. Krin E, Sismeiro O, Danchin A, Bertin PN. The regulation of Enzyme IIAGlc expression controls adenylate cyclase activity in Escherichia coli. Microbiology 2002; 148:1553–1559 [View Article][PubMed]
    [Google Scholar]
  43. Scholte BJ, Postma PW. Mutation in the crp gene of Salmonella typhimurium which interferes with inducer exclusion. J Bacteriol 1980; 141:751–757[PubMed]
    [Google Scholar]
  44. Peterkofsky A, Gazdar C. Glucose inhibition of adenylate cyclase in intact cells of Escherichia coli B. Proc Natl Acad Sci USA 1974; 71:2324–2328 [View Article][PubMed]
    [Google Scholar]
  45. Senior PJ. Regulation of nitrogen metabolism in Escherichia coli and Klebsiella aerogenes: studies with the continuous-culture technique. J Bacteriol 1975; 123:407–418[PubMed]
    [Google Scholar]
  46. Reitzer L. Nitrogen assimilation and global regulation in Escherichia coli. Annu Rev Microbiol 2003; 57:155–176 [View Article][PubMed]
    [Google Scholar]
  47. Guyer MS, Reed RR, Steitz JA, Low KB. Identification of a sex-factor-affinity site in E. coli as γδ. Cold Spring Harb Symp Quant Biol 1981; 45:135–140[PubMed] [CrossRef]
    [Google Scholar]
  48. Waksman SA, Reilly HC. Agar-Streak Method for assaying antibiotic substances. Ind Eng Chem Anal Ed 1945; 17:556–558 [View Article]
    [Google Scholar]
  49. Casadaban MJ. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and mu. J Mol Biol 1976; 104:541–555 [View Article][PubMed]
    [Google Scholar]
  50. Reyes-Lamothe R, Possoz C, Danilova O, Sherratt DJ. Independent positioning and action of Escherichia coli replisomes in live cells. Cell 2008; 133:90–102 [View Article][PubMed]
    [Google Scholar]
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