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J Bacteriol. Oct 2005; 187(19): 6856–6861.
PMCID: PMC1251575

Regulation of sigL Expression by the Catabolite Control Protein CcpA Involves a Roadblock Mechanism in Bacillus subtilis: Potential Connection between Carbon and Nitrogen Metabolism

Abstract

A catabolite-responsive element (CRE), a binding site for the CcpA transcription factor, was identified within the sigL structural gene encoding σL in Bacillus subtilis. We show that CcpA binds to this CRE to regulate sigL expression by a “roadblock” mechanism and that this mechanism in part accounts for catabolite repression of σL-directed levD operon expression.

RNA polymerase consists of a core structure plus a sigma factor that recognizes the promoter. While a single core complex is usually present in a bacterium, multiple sigma factors may be present. For example, Escherichia coli has 7 sigma factors, while Bacillus subtilis has at least 17, 6 for vegetative cell growth, 7 for extracytoplasmic functions, and 4 that are sporulation specific (16, 18). These sigma factors fall into two families, the sigma 70-type family, which recognizes −35, −10-type promoters, and the sigma 54-type family, which recognizes −24, −12-type promoters (27, 46). While σ70-type sigma factors can generally open the DNA by themselves, σ54-type factors require the participation of an enhancer (4, 43). Although a bacterium may possess multiple σ70-type factors, they often possess a single σ54-type factor.

σ54 RNA polymerase of E. coli is primarily concerned with transcription of nitrogen metabolic genes, although it transcribes several carbon metabolic genes as well (34, 35). One of the vegetative sigma factors in B. subtilis is σL, a σ54-type factor (10). In contrast to E. coli, relatively few genes have been shown to be transcribed by RNA polymerase containing σL (Table (Table1).1). These operons include the levanase operon, levDEFG-sac, involved in fructose and levanan metabolism (10, 26), three roc operons concerned with arginine catabolism (3, 5, 13, 14), an operon, acoABCL, encoding the acetoin dehydrogenase complex (1, 19), and the seven-cistron bkd operon (9), encoding enzymes involved in leucine and valine degradation. As indicated in Table Table1,1, several but not all of these operons contain a putative catabolite-responsive element (CRE) which binds the CcpA protein that mediates catabolite repression (39, 40). In the lev and aco operons, direct regulation by CcpA has been demonstrated (1, 25, 26, 30). Comparable regulation of the rocG operon has been proposed (2, 3). We also identified a potential CRE in the rocDEF operon.

TABLE 1.
Known constituents of the SigL regulon in Bacillus subtilisa

Little is known about the connection between nitrogen and carbon metabolism in B. subtilis (12, 45). While examining the B. subtilis genome for CRE sites using the GRASP-DNA program (42), we discovered the presence of a CRE in the middle of the sigL structural gene (Table (Table1).1). We show here that this CRE mediates catabolite repression of sigL gene expression by CcpA. The evidence presented suggests that a roadblock mechanism (11) is operative. We also show that this mechanism contributes to catabolite repression of lev operon expression.

Strains and plasmids.

Bacterial strains used in this study are listed in Table Table2.2. E. coli DH5α was used as a general cloning host. Transformation of B. subtilis was carried out by a method described elsewhere (7). Plasmids pDG1661 and pDG1664 were obtained from the Bacillus Genetics Stock Center in Ohio. To construct plasmid pDG-sigL1, the sigL1 fragment containing the sigL promoter and the CRE internal to the sigL gene was amplified by PCR with primers L1 (5′-AGTAAGCTTCCACATCCTGTCTTCTCTTC-3′) and L4 (5′-TAAGGATCCATATACACATCTTGCTCTG-3′) using Platinum Pfx DNA polymerase (Invitrogen Corp.). The product was digested with HindIII and BamHI and cloned into the corresponding sites of plasmid pDG1661. The sigL2 fragment containing only the sigL promoter was amplified by PCR with primers L1 and L2 (5′-TTTGGATCCCCAGCATTTCCGCTTGTTCA-3′), digested with HindIII and BamHI, and cloned into the corresponding sites of plasmid pDG1661 to construct pDG-sigL2. The sigLT fragment, containing the entire sigL gene, was amplified by PCR with primers L9 (5′-TTTAGTACTCCACATCCTGTCTTCTCTTC-3′) and L10 (5′-TTTGGATCCTTTTGCTGCTGCTCGTCTG-3′), digested with BamHI and ScaI, and cloned into the BamHI and blunt-ended EcoRI sites of pDG1664 to construct pDG-sigL. To construct pDG-sigLm2, the SpeI-EcoRI fragment of pDG-sigL was replaced with the SpeI-EcoRI fragment of pUC-sigL1m2 containing the sigL promoter and the mutated CRE.

TABLE 2.
Bacillus subtilis strains used in this study

Site-directed mutagenesis.

The SalI fragment containing the sigL promoter and the CRE from pDG-sigL1 was cloned into pUC19 to construct pUC-sigL1. pUC-sigL1m1 and pUC-sigL1m2, containing the mutated CRE sites (Fig. (Fig.1),1), were constructed by site-directed mutagenesis of pUC-sigL1 using a QuikChange site-directed mutagenesis kit (Stratagene Corp.) with primers L5 (5′-GCGCAAAAAAAATGGAAAAAGCTTTCAGTAGAGACGGG-3′) and L6 (5′-CCCGTCTCTACTGAAAGCTTTTTCCATTTTTTTTGCGC-3′) for pUC-sigL1m1 and primers L7 (5′-GCGCAAAAAAAATGGAA AACACTTTCAGTAGAGACGGG-3′) and L8 (5′-CCCGTCTCTACTGAAAGTGTTTTCCATTTTTTTTGCGC-3′) for pUC-sigL1m2. Mutations were confirmed by sequencing. SalI fragments of pUC-sigL1m1 and pUC-sigL1m2 containing the sigL promoter and the mutated CRE were cloned into pDG1661 to construct pDG-sigL1m1 and pDG-sigL1m2, respectively.

FIG. 1.
The wild-type sigL gene (top) and four lacZ fusion constructs (bottom) used to demonstrate the involvement of CcpA and the CRE site within the sigL structural gene in glucose-mediated catabolite repression in B. subtilis. The four constructs include (construct ...

Growth conditions and enzyme assays.

Bacillus cells were grown in LB medium or CHP minimal medium as modified from CSE medium (45) [50 mM Tris-Cl (pH 7.2), 25 mM (NH4)2SO4, 0.5 mM MgSO4, 10 μM MnSO4, 22 mg/liter ferric ammonium citrate, 6 g/liter sodium succinate, 8 g/liter potassium glutamate, 5 mM KH2PO4] supplemented with 160 μg/ml each of tryptophan, phenylalanine, and threonine. Fructose and glucose were added to CHP minimal medium to final concentrations of 0.2% and 0.5%, respectively.

For the LacZ assay of sigL expression, overnight cultures grown in 1 ml of LB medium were diluted 200-fold into fresh LB medium with or without 1% glucose and grown at 37°C with shaking at 200 rpm. For a LacZ assay of levD expression, overnight cultures of strains BCS162, BCS163, BCS172, and BCS173, grown in 1 ml of CHP minimal medium containing 0.05% yeast extract, 0.5% glucose, and 160 μg/ml each of tryptophan, phenylalanine, and threonine, were diluted 200-fold into fresh CHP minimal medium containing 0.2% fructose, 160 μg/ml each of tryptophan, phenylalanine, and threonine with or without 0.5% glucose and grown at 37°C with shaking at 200 rpm. Samples were collected at hourly intervals for the determination of the optical density at 600 nm. β-Galactosidase activity was determined as previously described (29), and the highest value recorded during a 6-h growth period was used.

RT-PCR.

Bacillus cells were cultured overnight at 37°C in 1 ml of LB medium, diluted 200-fold in 10 ml of LB medium with or without 1% glucose, and cultured at 37°C. Cell cultures (1 ml) were harvested 5 h after inoculation, and RNA was purified using the RNeasy Mini kit (QIAGEN, Inc.). Purified RNAs were treated with RNase-free DNase I (Roche Diagnostics) at 37°C for 1 h to remove any possible DNA contamination. RNAs were repurified using the RNeasy Mini kit. Ten nanograms of RNA was present by reverse transcription-PCR (RT-PCR) using the SuperScript III one-step RT-PCR system (Invitrogen Corp.) with either primers L11 (5′-ACAAGTATTAAAGCCTCAAC-3′) and L2 or primers L11 and L4. Following RT-PCR, 3-μl aliquots were electrophoresed in a 1.5% agarose gel.

Control of sigL expression by CcpA.

Figure Figure11 shows the constructs made to study expression of the sigL gene. The wild-type gene (sigL) was fused to lacZ downstream of the intragenic CRE site (sigL1). We also constructed an internal deletion mutant lacking the CRE site (sigL2) as well as two point mutants (sigL1m1 and sigL1m2) that are defective in the CRE site. In the first of these two point mutants, a threonine residue in SigL is changed to a lysine residue, but in the second mutant, the wild-type SigL protein is produced.

Table Table33 presents the data obtained using these strains. In the wild-type genetic background, a threefold repression was observed upon inclusion of glucose in the growth medium. No repression was observed in a ccpA mutant. When the CRE inside the sigL gene was either deleted or mutated in the wild-type genetic background, glucose catabolite repression was completely abolished (Table (Table3).3). We conclude that CcpA binds to this intragenic CRE site to mediate catabolite repression.

TABLE 3.
β-Galactosidase expression from lacZ fusions in wild-type and ccpA mutant strainsa

Evidence for a roadblock mechanism.

In order to investigate the mechanism of repression, reverse transcription-PCR was used to determine the level of sigL mRNA production in front of and behind the intragenic CRE site (Fig. (Fig.2A).2A). The results (Fig. 2B and C) showed that in the presence of glucose, but not in its absence, there was a substantial decrease in mRNA production, with a much greater decrease behind the CRE site than in front of it. This effect was abolished by the sigL1m2 mutation (Fig. (Fig.22).

FIG. 2.
Demonstration of the roadblock mechanism regulating sigL expression by CcpA using RT-PCR. (A) The wild-type sigL gene is shown in the top figure. The positions of the primers used for the RT-PCR experiments (L11, L2, and L4) are shown below this diagram. ...

Consequence of sigL regulation to levD operon expression.

The levD operon is known to be transcribed by σL RNA polymerase (Table (Table1).1). In order to establish the physiological significance of the regulation of sigL gene expression by CcpA, we examined catabolite repression of the levD operon. Cells were grown either in fructose-containing medium (weakly catabolite-repressing conditions) or in fructose plus glucose-containing medium (strongly catabolite-repressing conditions). The presence of glucose caused catabolite repression to an extent more than 10-fold of that in the wild-type background. Mutation of the CRE site in sigL (sigL1m2) partially, but not fully, relieved the glucose effect, as expected (Table (Table4).4). Moreover, mutation of the CRE site upstream of levD similarly resulted in partial relief of catabolite repression. The combined effects of the two mutations were essentially additive (Table (Table4).4). These observations clearly show that regulation of sigL gene expression by CcpA contributes to catabolite repression of the levD operon.

TABLE 4.
Effects of the sigL1m2 mutation on the expression of levDa

Conclusions and perspectives.

Bacteria live in harsh environments that often lack or contain low concentrations of a specific nutrient, even when other nutrients are present in excess. To deal with such problems, microorganisms have evolved multiple mechanisms to sense and respond to the availability of specific nutrient types (37-39, 41). However, in order to optimize growth, microorganisms must not only sense the availability of a nutrient type (e.g., carbon and energy), but they must also adjust their uptake or production of other nutrient types (e.g., nitrogen-, phosphorus-, and sulfur-containing compounds) according to the availability of carbon. Only in a few cases have such interactions been investigated (28, 32, 33).

Bacteria have pleiotropic transcriptional regulatory factors, the actions of which define the various nutrient regulons (23, 36, 48). Thus, in Bacillus subtilis, the CcpA transcription factor plays a primary role in sensing carbon and energy availability, although several other mechanisms that allow sensing are also operative (20, 39, 44).

A few potential mechanisms by which the nitrogen and carbon regulons of B. subtilis may interact have been proposed (8, 12, 22, 45), but the relative significance of these specific interactions has in general not been evaluated. In this communication, we have investigated a previously unrecognized mechanism by which carbon and nitrogen metabolism may be interconnected. As noted in Table Table1,1, SigL is known to direct the transcription of several nitrogen catabolic operons, and there are undoubtedly many more that have not been examined. For this reason, our demonstration that CcpA, the central transcriptional sensor of carbon availability in B. subtilis, dramatically regulates expression of the sigL gene may be of considerable physiological significance. This mechanism might allow the coordinated regulation of carbon and nitrogen metabolic pathways in response to carbon availability. The fact that SigL controls several key carbon operons as well as important nitrogen operons emphasizes the probable significance of this complex interaction. In fact, we have demonstrated the physiological relevance of glucose repression of sigL expression to catabolite repression of the lev operon. Further studies will be required to demonstrate the importance of this type of regulation to the coordination of nitrogen metabolism with carbon metabolism.

The results reported here represent one of a few well-studied examples in which the binding of a transcription factor to a site within a structural gene can affect regulation of gene expression (15, 17, 21, 31, 49). We demonstrate that the binding of CcpA to the CRE site within the sigL structural gene blocks mRNA synthesis far more effectively downstream of this site than upstream of it (Fig. (Fig.2).2). Such a mechanism, termed a “roadblock” mechanism, has been demonstrated in only a few cases (15, 21, 47). Based on unpublished genome-wide binding site analyses using the GRASP-DNA program (42), we anticipate that such mechanisms will prove to be far more common than is currently appreciated.

Acknowledgments

We are grateful to Michel Debarbouille for strains QB5505, QB5081, and QB7000. We thank Mary Beth Hiller for her assistance in the preparation of the manuscript.

This work was supported by NIH grant GM55434.

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