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Chapter 14 : Dual Sensors and Dual Response Regulators Interact to Control Nitrate- and Nitrite-Responsive Gene Expression in

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Abstract:

Nitrate and nitrite control is mediated by the Nar (nitrate reductase) dual interacting two-component regulatory systems, which consist of homologous membrane-bound sensors (the NarX and NarQ proteins) and homologous DNA binding response regulators (the NarL and NarP proteins). This chapter emphasizes that the Nar system controls nitrate and nitrite metabolism strictly in response to the needs of anaerobic respiration and has nothing to do with the use of nitrate or nitrite as nitrogen sources for biosynthesis. Identification of dual nitrate-responsive sensors led to the notion that dual response regulators may also be involved in the Nar regulatory circuit. Analysis of target operon expression in and null mutants has revealed a diversity of regulatory patterns. The and genes have only recently been recognized, whereas the and genes have been studied for many years. Sequence comparisons strongly suggest that the NarX/NarQ and NarL/NarP proteins function in phosphoryl transfer reactions. Studies with purified proteins have examined some of the interactions in vitro. The Asp-59 residue in the NarL protein corresponds to the site of phosphorylation in all response regulators studied. A specific equilibrium state produces a regulatory outcome based on the net effect of the positive and negative sensor activities, which, in turn, controls the phosphorylation state of the NarL response regulator. The control regions of several nitrate- and nitrite-regulated operons have now been studied in detail. Most studies have used batch cultures grown with excess nitrate or nitrite.

Citation: Stewart V, Rabin R. 1995. Dual Sensors and Dual Response Regulators Interact to Control Nitrate- and Nitrite-Responsive Gene Expression in , p 233-252. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch14

Key Concept Ranking

IHF Protein
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NarK Protein
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Figures

Image of FIGURE 1
FIGURE 1

Model for nitrate- and nitrite-regulated gene expression. Activation and repression of target operon expression are indicated by + and —, respectively; question marks denote situations that have not yet been tested. Strong interactions (10-fold or greater regulation) are boxed, whereas weaker interactions (less than 10-fold regulation) are circled. The NarL and NarP proteins are represented by circled L and circled P, respectively; the phosphorylated forms are represented by the same letters boxed. The NarX and NarQ proteins are represented by the letters X and Q, respectively. In the presence of nitrite, a relatively small proportion of NarL molecules is phosphorylated. Target operon designations are listed in Table 1 . The operon is denoted as “-” in this figure. Modified from ).

Citation: Stewart V, Rabin R. 1995. Dual Sensors and Dual Response Regulators Interact to Control Nitrate- and Nitrite-Responsive Gene Expression in , p 233-252. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch14
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Image of FIGURE 2
FIGURE 2

Linker regions of MCPs (Tsr, serine chemoreceptor; Tar, aspartate chemoreceptor; Tap, peptide chemoreceptor; Trg, ribose chemoreceptor) and sensors (EnvZ, osmolarity sensor; NarX and NarQ, nitrate/nitrite sensors). The segments immediately following the second transmembrane region are shown. Residues that are identical in all seven sequences are boxed. Mutational changes in tsr ( ) and ( ) are indicated.

Citation: Stewart V, Rabin R. 1995. Dual Sensors and Dual Response Regulators Interact to Control Nitrate- and Nitrite-Responsive Gene Expression in , p 233-252. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch14
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Image of FIGURE 3
FIGURE 3

Equilibrium model of NarX and NarQ protein functions in the presence of (A) nitrate or (B) nitrite. See text for details. The NarX and NarQ sensor proteins are shown in equilibria between their negative (rounded) and positive (rectangular) forms. The relative sizes of the equilibrium arrows indicate qualitatively how much of a given sensor population is found in each of the two forms. Positive interactions with the NarL response regulator are designated + (i.e., NarL kinase), and negative interactions are designated − (i.e., phospho-NarL phosphatase). A solid or dashed line (at 45° angle to the sensor protein) emphasizes whether a large or small proportion respectively, of a given sensor population is responsible for a specific influence on the NarL protein.

Citation: Stewart V, Rabin R. 1995. Dual Sensors and Dual Response Regulators Interact to Control Nitrate- and Nitrite-Responsive Gene Expression in , p 233-252. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch14
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Image of FIGURE 4
FIGURE 4

Promoter-regulatory regions for nitrate-regulated operons. Scale is in base pairs. Thin arrows denote transcription initiation sites; the dashed arrow for the control region denotes a minor constitutive transcript. Fnr protein binding sites are shown as dark hatched inverted arrows. NarL heptamer sequences are indicated by their position with respect to the transcription initiation site. Heptamers denoted by black arrows have been identified by both mutational analysis and by DNase I footprinting. Heptamers denoted by gray arrows have been identified by DNase I footprinting only. Heptamers denoted by light hatched arrows have been identified by mutational analysis only. Heptamers denoted by white arrows have been identified by sequence inspection only. The IHF protein binding sites in the and the control regions are denoted by striped boxes. The aeg-46.5 operon is denoted as in this figure. Modified from ) and ).

Citation: Stewart V, Rabin R. 1995. Dual Sensors and Dual Response Regulators Interact to Control Nitrate- and Nitrite-Responsive Gene Expression in , p 233-252. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch14
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References

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Tables

Generic image for table
TABLE 1

Known NarL- and NarP-regulated operons

Citation: Stewart V, Rabin R. 1995. Dual Sensors and Dual Response Regulators Interact to Control Nitrate- and Nitrite-Responsive Gene Expression in , p 233-252. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch14
Generic image for table
TABLE 2

Effects of narX mutations on nitrate and nitrite regulation

Citation: Stewart V, Rabin R. 1995. Dual Sensors and Dual Response Regulators Interact to Control Nitrate- and Nitrite-Responsive Gene Expression in , p 233-252. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch14

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