Research review paperThe transport and mediation mechanisms of the common sugars in Escherichia coli
Introduction
Glucose, together with fructose, sucrose, maltose, mannose, xylose etc., is abundant in nature and serves as an important carbon source frequently used by microorganisms. The utilization of different carbon sources requires a different set of genes that encode the specific transporters, regulators and functional enzymes for metabolism. Interestingly, there is a specific hierarchy for the utilization of carbon sources in nearly all microorganisms, and glucose is usually at the top of these sugars (Görke and Stülke, 2008, Postma et al., 1993). If there is sufficient glucose called preferred sugars in the growth media, then the synthesis of the enzymes necessary for the transport and metabolism of less favorable carbon sources will be repressed. The phenomenon is called carbon catabolite repression (CCR) (Stülke and Hillen, 1999). Additionally, it is well known that CCR is involved in the phosphoenolpyruvate-dependent carbohydrate phosphotransferase system (PTS) (Deutscher et al., 2006, Görke and Stülke, 2008, Postma et al., 1993).
Currently, glucose is the main carbon source used in the fermentation industry; however, glucose is an expensive raw material for producing many bulk chemicals due to its production cost (Dale, 1999, Lugar and Woolsey, 1999, Sheehan and Himmel, 1999). Hence, less expensive and easily available carbon sources or mixtures are highly desired. Sucrose and lignocelullosic hydrolysates containing glucose, xylose, arabinose and small amounts of galactose and mannose (Aristidou and Penttilä, 2000, Asghari et al., 1996, Bothast et al., 1999, Li et al., 2007, Sheehan and Himmel, 1999) may be possible substitutes, and many novel biotechnologies, particularly metabolic engineering, synthetic biology and systems biology, have been applied to modify transport systems to enhance the utilization efficiency of these carbon sources in bacteria (Stephanopoulos, 2007). Escherichia coli have been chosen to be a microbial cell factory for the production of many valuable chemicals due to its clear gene background, fast propagation, easy cultivation and utilization of multiple carbon substrates. In many previous reported works, the transport and metabolism mechanisms of some sugars in E. coli have been investigated and focused on modifying the sugar import capacity of the cell, particularly on the PTS of glucose (Chatterjee et al., 2001, Chen et al., 1997b, Chou et al., 1994, Hernández-Montalvo et al., 2001, Hernández-Montalvo et al., 2003, Lindsay et al., 1995, Snoep et al., 1994, Yao et al., 2011). Meanwhile, research attention is also focused on the PTS and on CCR in enteric bacteria and in low-G + C Gram-positive bacteria (Deutscher et al., 2006, Görke and Stülke, 2008, Kotrba et al., 2001, Park et al., 2012, Postma et al., 1993, Siebold et al., 2001, Stülke and Hillen, 1999). Furthermore, increasing attention has been given to the utilization of cheap sugars in E. coli, such as sucrose and xylose. In this review, the transport and mediation metabolisms of most common sugars that can be utilized by E. coli, such as glucose, fructose, sucrose, xylose and arabinose, are summarized, and some interactions among the utilizations of these sugars are elucidated. Strategies of strain manipulation based on the greater understanding of these regulation mechanisms will further improve the yield and efficiency of large-scale industrial processes and increase their economic feasibility.
Section snippets
The mechanisms of glucose transport and metabolism in E. coli
Glucose, which is one of the main products and fuels of photosynthesis, exists in several different molecular structures; however, all of these structures can be divided into two families of mirror images. Correspondingly, glucose has two stereoisomers of d-glucose and l-glucose. d-glucose exists in nature, whereas l-glucose is rarely found in nature. Additionally, d-glucose is now used as the main carbon source for some microorganisms and for biotechnology products.
Fructose transport pathways in E. coli
E. coli can grow in medium with fructose serving as the sole carbon source (Fraenkel, 1968, Kornberg, 1990, Kornberg, 2001, Aristidou et al., 1999). Approximately 57% of fructose is in the β-d-pyranose form in solution (Kornberg and Lourenco, 2006). Identical to other sugars possessing the 3,4,5-d-arabino-hexose configuration of d-glucose, d-mannose, d-mannitol and d-glucitol (Kornberg, 2001, Kornberg and Lourenco, 2006), d-fructose can be taken up by E. coli via FruAB and ManXYZ carriers of
The transport pathways of sucrose in E. coli
Due to the low price and availability of various carbon feedstocks, sucrose is used as a carbon source for cell growth and metabolism to reduce production costs (Wang et al., 2011). Sucrose transport pathways have been described in Enterobacteriaceae. Initially, strains of Klebsiella pneumoniae were found to take up and phosphorylate the disaccharide sucrose; now, it has been confirmed that more than 90% of wild-type strains of Klebsiella spp., but less than 50% of E. coli and less than 10% of
The transport and metabolism mechanisms of xylose and arabinose in E. coli
Arabinose and xylose account for more than 30% of the total sugars in agricultural residues and in hardwoods (Olofsson et al., 2008). Xylose is the second most abundant sugar in nature besides glucose (Jeffries, 1983) and primarily exists in d-xylose (Badia et al., 1991). In hydrolytes of lignocellulosic materials, xylose accounts for 5 to 20% (Aristidou and Penttilä, 2000, Li et al., 2007). Arabinose is the second major pentose sugar following xylose, and most arabinose is l-arabinose in
Conclusions and prospects
To enhance the bioconversion of sugars, it is necessary to understand the sugar import and mediation mechanisms during cross-membrane transport and the relations among sugar uptake rate, metabolic flux distributions and metabolic products, including the target products and byproducts. More key information concerning these interactions will lead to more effective metabolism mediations and, finally, to a higher yield of target products. The common sugars, particularly sucrose and monosaccharoses
Acknowledgments
This work was supported by grant no. 21176200 from the National Natural Science Foundation of China and by grant no. 2010JC21 from the Scientific Research Program of Shaanxi Provincial Department of Education, China.
References (215)
- et al.
Purification and properties of a periplasmic d-xylose-binding protein from Escherichia coli K-12
J Biol Chem
(1982) - et al.
Metabolic engineering applications to renewable resource utilization
Curr Opin Biotechnol
(2000) - et al.
A quantitative approach to catabolite repression in Escherichia coli
J Biol Chem
(2006) - et al.
A transferable sucrose utilization approach for non-sucrose-utilizing Escherichia coli strains
Biotechnol Adv
(2012) - et al.
Carbon catabolite repression in bacteria: choice of the carbon source and autoregulatory limitation of sugar utilization
FEMS Microbiol Lett
(2002) - et al.
Transcription activation by catabolite activator protein (CAP)
J Mol Biol
(1999) - et al.
EnvZ–OmpR interaction and osmoregulation in Escherichia coli
J Biol Chem
(2002) Regulation of the regulatory gene for the arabinose pathway, araC
J Mol Biol
(1976)- et al.
Enzyme I: the first protein and potential regulator of the bacterial phosphoenolpyruvate: glycose phosphotransferase system
Res Microbiol
(1996) - et al.
The localization of the phosphorylation site of BglG, the response regulator of the Escherichia coli bgl sensory system
J Biol Chem
(1997)
Replacement of the glucose phosphotransferase transport system by galactose permease reduces acetate accumulation and improves process performance of Escherichia coli for recombinant protein production without impairment of growth rate
Metab Eng
The mechanisms of carbon catabolite repression in bacteria
Curr Opin Microbiol
Group translocation of glucose and other carbohydrates by the bacterial phosphotransferase system
Int Rev Cytol
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
Phosphate transfer between acetate kinase and enzyme I of the bacterial phosphotransferase system
J Biol Chem
The phosphoenolpyruvate-initiated pathway of fructose metabolism in Escherichia coli
J Biol Chem
Membrane transport proteins: implications of sequence comparisons
Curr Opin Cell Biol
Deletion analysis of sucrose metabolic genes from a Salmonella plasmid cloned in Escherichia coli K12
Plasmid
Allosteric regulation of the cAMP receptor protein
BBA-Protein Struct Mol Enzymol
Regulation of the Escherichia coli l-arabinose operon studied by gel electrophoresis DNA binding assay
J Mol Biol
High-affinity l-arabinose transport operon. Gene product expression and mRNAs
J Mol Biol
Relief of catabolite repression in a cAMP-independent catabolite gene activator mutant of Escherichia coli
Res Microbiol
Role of xylose transporters in xylitol production from engineered Escherichia coli
J Biotechnol
Regulation of the l-arabinose transport operons in Escherichia coli
J Mol Biol
The roles of HPr and FPr in the utilization of fructose by Escherichia coli
FEBS Lett
Regulation of fructose uptake by glucose in Escherichia coli
J Gen Microbiol
The genome sequence of E. coli W (ATCC 9637): comparative genome analysis and an improved genome-scale reconstruction of E. coli
BMC Genomics
Improvement of biomass yield and recombinant gene expression in Escherichia coli by using fructose as the primary carbon source
Biotechnol Prog
Ethanol production from hemicellulose hydrolysates of agricultural residues using genetically engineered Escherichia coli strain KO11
J Ind Microbiol
Molecular analysis of two fructokinases involved in sucrose metabolism of enteric bacteria
Mol Microbiol
l-lyxose metabolism employs the l-rhamnose pathway in mutant cells of Escherichia coli adapted to grow on l-lyxose
J Bacteriol
Correlation between growth rates, EIIACrr phosphorylation, and intracellular cyclic AMP levels in Escherichia coli K-12
J Bacteriol
Characterization of a chromosomally encoded, non-PTS metabolic pathway for sucrose utilization in Escherichia coli EC3132
Mol Gen Genet
Molecular analysis of sucrose metabolism of Erwinia amylovora and influence on bacterial virulence
J Bacteriol
Trehalose transport and metabolism in Escherichia coli
J Bacteriol
Fermentations with new recombinant organisms
Biotechnol Prog
Cyclic AMP in prokaryotes
Microbiol Mol Biol Rev
Properties of d-arabinose isomerase purified from two strains of Escherichia coli
J Bacteriol
Metabolism of d-arabinose by Escherichia coli B/r
J Bacteriol
Signal transduction pathways involving protein phosphorylation in prokaryotes
Annu Rev Biochem
A second transport system for l-arabinose in Escherichia coli B/r controlled by the araC gene
J Bacteriol
Sequence of the lactose permease gene
Nature
Transport of d-xylose in Lactobacillus pentosus, Lactobacillus casei, and Lactobacillus plantarum: evidence for a mechanism of facilitated diffusion via the phosphoenolpyruvate: mannose phosphotransferase system
J Bacteriol
Function of the duplicated IIB domain and oligomeric structure of the fructose permease of Escherichia coli
J Biol Chem
Mutation of the ptsG gene results in increased production of succinate in fermentation of glucose by Escherichia coli
Appl Environ Microbiol
The different functions of BglF, the E. coli β-glucoside permease and sensor of the bgl system, have different structural requirements
Biochemistry
Comparative studies of Escherichia coli strains using different glucose uptake systems: metabolism and energetics
Biotechnol Bioeng
Effect of modulated glucose uptake on high-level recombinant protein production in a dense Escherichia coli culture
Biotechnol Prog
Engineering Escherichia coli for xylitol production from glucose–xylose mixtures
Biotechnol Bioeng
Control of the sequential utilization of glucose and fructose by Escherichia coli
Microbiology
Cited by (72)
Recent advances in the metabolic engineering and physiological opportunities for microbial synthesis of L-aspartic acid family amino acids: A review
2023, International Journal of Biological MacromoleculesHigh-level itaconic acid (IA) production using engineered Escherichia coli Lemo21(DE3) toward sustainable biorefinery
2023, Enzyme and Microbial TechnologyBiosynthesis of value-added bioproducts from hemicellulose of biomass through microbial metabolic engineering
2022, Metabolic Engineering CommunicationsCronobacter species
2021, Foodborne Infections and IntoxicationsThe mannose phosphotransferase system (Man-PTS) - Mannose transporter and receptor for bacteriocins and bacteriophages
2020, Biochimica et Biophysica Acta - Biomembranes