Elsevier

Biotechnology Advances

Volume 32, Issue 5, September–October 2014, Pages 905-919
Biotechnology Advances

Research review paper
The transport and mediation mechanisms of the common sugars in Escherichia coli

https://doi.org/10.1016/j.biotechadv.2014.04.009Get rights and content

Abstract

Escherichia coli can uptake and utilize many common natural sugars to form biomass or valuable target bio-products. Carbon catabolite repression (CCR) will occur and hamper the efficient production of bio-products if E. coli strains are cultivated in a mixture of sugars containing some preferred sugar, such as glucose. Understanding the transport and metabolism mechanisms of the common and inexpensive sugars in E. coli is important for further improving the efficiency of sugar bioconversion and for reducing industrial fermentation costs using the methods of metabolic engineering, synthetic biology and systems biology. In this review, the transport and mediation mechanisms of glucose, fructose, sucrose, xylose and arabinose are discussed and summarized, and the hierarchical utilization principles of these sugars are elucidated.

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.

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