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Use the link below to share a full-text version of this article with your friends and colleagues. Learn more. Wheldon 1N. Iqbal 2C.

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Learn More. We present a comprehensive overview of the hierarchical network of intracellular processes revolving around central nitrogen metabolism in Escherichia coli. The hierarchy intertwines transport, metabolism, aling leading to posttranslational modification, and transcription.

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First, the structural and molecular knowledge on these proteins is reviewed. Thereafter, the activities of the components as they engage together in transport, metabolism, al transduction, and transcription and their regulation are discussed.

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Next, old and new molecular data and physiological data are put into a common perspective on integral cellular functioning, especially with the aim of resolving counterintuitive or paradoxical processes featured in nitrogen assimilation. Finally, we articulate what still remains to be discovered and what general lessons can be learned from the vast amounts of data that are available now. A fact of life that many microorganisms are confronted with is the unreliable environmental availability of nutrients, including N-containing compounds.

Some microorganisms have to deal with virtually every possible nutritional state between feast and famine; periods of nutrient excess may well be followed by periods of extreme starvation, or they may not be or not always be. As they can grow fast and often exponentially, many microorganisms readily deplete their own environment of the nutrient that is least in excess and thereby have to endure nutrient limitation of some sort much more frequently than they can enjoy full nutritional affluence.

Adaptive physiological responses to feast or famine conditions are the result of a highly regulated system consisting of al transduction coupled to transport, metabolism, and genetic circuits.

Online publication

A general challenge for every microorganism is how to choose to respond to changing environmental conditions if it has more than one possibility to react at its disposal. This challenge is well illustrated by Escherichia coli when it is confronted with a change in the nitrogen supply in its surroundings. Since it possesses two central nitrogen-assimilatory routes, it has to make a decision as to what extent either pathway or both pathways should be adapted most. The ammonium assimilation network of E.

At the protein level, the network includes an ammonium transporter, two ammonium assimilation pathways, two bifunctional protein modification enzymes, two trimeric al transduction proteins, and a two-component regulatory system composed of a histidine protein kinase and the corresponding response regulator 1.

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After uptake, ammonium is incorporated directly only into the amino acids glutamate and glutamine, which subsequently function as nitrogen donors in transamination and transamidation reactions. These lead to other amino acids and to precursors for the biosynthesis of purines and pyrimidines 45. Ammonium assimilation by the glutamine synthetase GS -glutamate synthase glutamine 2-oxoglutarate amidotransferase [GOGAT] pathway may for a substantial percentage of the cell's ATP requirement when it is growing on glucose minimal medium 6even though the alternative of ammonium assimilation through glutamate dehydrogenase GDH alone accomplishes the same chemistry at the cost of less ATP.

The former pathway appears to be used, even though expression of the operons encoding the proteins GS and GOGAT, as well as the activity of GS, can be regulated in multiple ways 6— 9.

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On the other hand, for many other carbon and energy sources used for growth of E. Accordingly, our research should be dedicated not only to characterizing the properties of the components in isolation but also to a full systemic understanding of the role that each and every component plays in bringing about the behavior and function of the network.

The science that studies how interactions and networks contribute to biological function has been called systems biology 1011and this systems biology is needed to understand ammonium assimilation. Studying just any single molecule, such as GS, in the network will not suffice, as the properties of that molecule will be affected by the redox state, the energy state, al transduction, gene expression, and the intracellular levels of ammonium, glutamine, and glutamate, which are also determined by the other macromolecules in the network.

An understanding of the network without understanding the molecules will not suffice either, as it is the dynamic response of the macromolecules through the levels of the micromolecules that determines network functioning One needs to study the molecules and their networking to understand biological function In this review, we focus on the assimilatory response of E. Our strategy is to first describe all the components of this network one by one, paying attention to their interactive properties.

We then discuss the different sub networks that involve these components, with the aim of showing what their functional roles are in nitrogen assimilation in E. Finally, we distill some general biology lessons from this particular subject. This review will thereby focus on i the molecular data regarding the structures and functions of the proteins involved in the central nitrogen assimilation network, most notably on the GS regulatory cascade and ii the systemic view that puts the molecular data in a systems biological perspective.

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This review focuses on E. The genus Shigellawhich also belongs to the highly diverse species E. Other enterobacteria, proteobacteria, and even archaea are discussed only when important for an understanding of E.

Nitrogen is an essential element for all organisms. Like other enteric bacteria, E. Ammonium is considered the preferred nitrogen source, as it supports the highest growth rate 7. In batch culture, E. The assimilation of ammonium into glutamate is the process where the element nitrogen is assimilated by carbon metabolism.

For this incorporation of ammonium into 2-oxoglutarate, E. GDH catalyzes the reductive amination of 2-oxoglutarate to glutamate. GS catalyzes the amidation of glutamate to glutamine at the cost of the hydrolysis of one molecule of ATP. Both enzymes use ammonium as the nitrogen source.

The reductive transfer of the glutamine amide group to the 2-position of 2-oxoglutarate, thereby forming two molecules of glutamate, is catalyzed by GOGAT.

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The latter process expends one ATP. Two pathways for glutamate synthesis. The basic characteristics of the two pathways are shown in the box below the scheme. One net glutamate is produced from the reductive amination of 2-oxoglutarate; no ATP is involved, and GDH had a relatively low affinity for ammonium. However, one ATP is invested for every amino group assimilated, and GS has a relatively high affinity for ammonium.

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However, DNA and RNA make up a smaller fraction of biomass than protein, and consequently, the flux into glutamate is much higher than the flux into glutamine other than for the purpose of producing glutamate. We shall therefore focus on the process of synthesis of glutamate from ammonium and 2-oxoglutarate. A salient feature of the two central nitrogen-assimilating enzymes of E. GS activity is regulated in multiple ways. Already metabolically, flow through GS is regulated 4-fold, i. The catalytic rate is also regulated through al transduction, which determines the reversible covalent modification state of the enzyme.

The latter mode of regulation is connected to transcription regulation by a common sensor and al transduction system 1625— Generally, in the absence of ammonium, the global nitrogen response regulator I NRI is phosphorylated by its cognate sensor NRII at a low-ammonium assimilation state of the cell. One such gene codes for the nitrogen assimilation control Nac protein. Metabolic, al transduction, and gene expression regulations each involve entire pathways, e. In addition, the three types of pathways are intertwined, already around GS itself.

The functioning of this hierarchical network depends on the interaction of its components. Below, we therefore discuss molecules, interactions, networks, and function in more detail, with a focus on the dynamic integration of the former into the latter. In addition, six enzymes NAD synthetase, carbamoyl phosphate synthetase, asparagine synthetases A and B, and glutaminases A and B and the nitrogen-phosphotransferase system N-PTS are possibly involved and are reviewed below. The first four of the latter enzymes are discussed because they have the ability to assimilate ammonium, although they normally engage in other reactions.

The glutaminases are potentially important as they may be involved in controlling the glutamine pool. The N-PTS is a recently discovered system that may or may not turn out to be relevant for nitrogen assimilation. All genes, proteins abbreviations and full namesand activities discussed in this review are shown in Table 2. GS lies at the heart of the nitrogen assimilation network. GS is a dodecamer of identical monomers of 52 kDa encoded by the glnA gene 33 Electron microscopic 35 and X-ray crystallographic analyses of completely unadenylylated GS of S.

Typhimurium have shown that the 12 subunits in each complex are arranged in two rings of six subunits each, with the second hexagon inverted on top of the first. The two layers of subunits are held together largely by the apolar carboxyl terminus of each subunit inserting into a hydrophobic pocket formed by two neighboring subunits on the opposite ring 36 Within each layer, each of the six active sites is located at the interface of a pair of subunits.

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The substrate binding sites of glutamate, ATP, and ammonium are located within this active site 3638— GS has 12 active sites that may well act cooperatively see below. The various steps in the synthesis of glutamine by fully unadenylylated GS have been visualized beautifully as a series of molecular interactions in time and space by X-ray crystallography of crystal structures of enzyme-substrate complexes 38 The affinity constants are as follows: K ATP is 0.

The two different subunits are encoded by the gltB and gltD genes, respectively. The GltB protein comprises an amidotransferase domain coupled to a synthase domain through an intramolecular ammonium tunnel. In general, glutamine-dependent amidotransferases generate NH 3 by glutamine hydrolysis, followed by NH 3 transport via an intramolecular tunnel and further reaction by an enzyme-specific synthase activity Under some conditions, these enzymes use cytosolic ammonium instead of glutamine and, by doing so, function as ammonium-assimilating enzymes.

On the basis of data obtained with a polar gltF mutant, GltF was ased a regulatory role in nitrogen catabolism and ammonium transport 5051but this observation could not be confirmed when a nonpolar mutant was used GltF may be translocated to the periplasmic space, which may make a direct regulatory function in GOGAT activity unlikely Thus, until now, its precise function remains unclear 50— The dissociation constants are as follows: K Gln is 0.

GDH of E. The monomer is encoded by the gdhA gene, which translates to a polypeptide of amino acids Confusing have been presented with respect to the stability of the enzyme.

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Purified GDH of E. In other hands, purified GDH was found to lose activity within minutes at room temperature Purified GDH displayed an unusual resistance to high concentrations of the protein denaturant urea 20 and guanidine HCl The same was true for purified S.

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