- Research article
- Open Access
Stationary phase expression of the arginine biosynthetic operon argCBH in Escherichia coli
- Jeevaka P Weerasinghe†1,
- Tao Dong†1,
- Michael R Schertzberg1,
- Mark G Kirchhof1,
- Yuan Sun1 and
- Herb E Schellhorn1Email author
© Weerasinghe et al; licensee BioMed Central Ltd. 2006
- Received: 25 August 2005
- Accepted: 22 February 2006
- Published: 22 February 2006
Arginine biosynthesis in Escherichia coli is elevated in response to nutrient limitation, stress or arginine restriction. Though control of the pathway in response to arginine limitation is largely modulated by the ArgR repressor, other factors may be involved in increased stationary phase and stress expression.
In this study, we report that expression of the argCBH operon is induced in stationary phase cultures and is reduced in strains possessing a mutation in rpoS, which encodes an alternative sigma factor. Using strains carrying defined argR, and rpoS mutations, we evaluated the relative contributions of these two regulators to the expression of argH using operon-lacZ fusions. While ArgR was the main factor responsible for modulating expression of argCBH, RpoS was also required for full expression of this biosynthetic operon at low arginine concentrations (below 60 μM L-arginine), a level at which growth of an arginine auxotroph was limited by arginine. When the argCBH operon was fully de-repressed (arginine limited), levels of expression were only one third of those observed in ΔargR mutants, indicating that the argCBH operon is partially repressed by ArgR even in the absence of arginine. In addition, argCBH expression was 30-fold higher in ΔargR mutants relative to levels found in wild type, fully-repressed strains, and this expression was independent of RpoS.
The results of this study indicate that both derepression and positive control by RpoS are required for full control of arginine biosynthesis in stationary phase cultures of E. coli.
- Stationary Phase Culture
- Arginine Concentration
- Arginine Biosynthesis
The biosynthesis and/or scavenging of arginine are important during host colonization by uropathogenic Escherichia coli. In urine, expression of the E. coli argCBH operon and artJ, encoding a periplasmic transporter, increases more than 10 fold  and 18 fold , respectively. Synthesis of arginine is likely required during infection as the concentration of arginine found in urine is below that necessary to support maximal growth of E. coli . Consistent with these data, infection challenge in a murine model with E. coli strains carrying mutations in the argC gene results in impaired proliferation in the kidney . In enteropathogenic E. coli  arginine synthesis and transport, together with arginine decarboxylase (encoded by adiA), are important components of the cell's acid resistance repertoire [3–5].
Under nutrient-limiting conditions, E. coli can potentially utilize arginine as both a carbon and a nitrogen source . Arginine is a precursor for the synthesis of polyamines, putrescine and spermidine, which may reduce oxidative damage to proteins and DNA [7, 9]. In addition, in phosphate-starved cells, aerobic metabolism of arginine may be an important physiological adaptation that is intimately associated with cell survival . Since arginine contains 11% of the cell's nitrogen in stationary phase , biosynthesis of this amino acid is likely important under sub-optimal conditions.
Arginine is synthesized by a complex biosynthetic pathway consisting of several operons and unlinked genes that are controlled by ArgR  which represses by binding to a conserved ARG box [13, 14] to overlap with RNA polymerase binding sites. Maximum derepression occurs in the absence of arginine . In contrast to most amino acid biosynthetic genes, the expression of the arg biosynthetic genes increases briefly during diauxic growth arrest . As this stress is similar to that imposed by nutrient limitation, it is plausible that stationary phase regulators participate in control of arginine biosynthesis. Several enzymes required for arginine catabolism are controlled by RpoS, an alternative stationary phase sigma factor , including those encoded by astD [11, 17], and cstC (astC) [11, 18]. Many of the members of the large RpoS regulon are specifically expressed during the transition to stationary phase growth [19, 20]. Although clearly required for virulence in Salmonella , the role of RpoS in the pathogenesis of E. coli is equivocal. RpoS controls many functions that contribute to host adaptation, including osmotic stress  and acid challenge . In E. coli, however, RpoS mutants are not impaired in colonization of the urinary tract  or gastrointestinal tract  in animal models. There are several different alleles of RpoS found in natural populations of E. coli , and it is thus possible that RpoS regulation may be strain specific.
In a previous study, we identified many independent RpoS-dependent operon fusions . Two of these mapped to the argCBH operon and were of particular interest because, unlike other RpoS-regulated functions that we identified, this operon, when mutated, rendered the cell auxotrophic. In this study, we have employed these fusions as probes to examine regulatory controls on transcription of the argCBH operon to identify how this key biosynthetic pathway is activated.
Characterization of argCBH operon fusions
Since ArgR is a known regulator of argCBH , we constructed combinatorial argR and rpoS mutants to determine the relative contributions of each regulator to the expression of the operon. Introduction of a deletion of argR into a strain with an argCBH-lacZ fusion resulted in high expression with or without RpoS (Fig. 2). It is likely that RpoS-dependent expression of argCBH in the ΔargR strains may be masked by strong derepression as a consequence of loss of ArgR.
Growth phase dependence of argCBH expression
Expression of the argCBH operon in rich media. Wildtype, ΔrpoS and ΔargR strains harboring the rsd1066 operon lacZ-fusion to the argCBH operon were grown in LB media and assayed for β-galactosidase activity in exponential phase (OD600 = 0.3) and stationary phase (OD600 = 1.5) as described in Methods. All reported activities are the average of three independent determinations.
β-Galactosidase (Miller Units)
5.6 ± 0.34
38.4 ± 0.97
6.1 ± 0.26
18.8 ± 0.15
469 ± 18
553 ± 33
486 ± 32
712 ± 35
Effect of exogenous arginine on argCBH expression
Effect of exogenous supplemented pyrimidines on growth of ΔargR strains. Overnight cultures were grown in minimal media with exogenously-supplemented L-arginine (230 μM). Cultures were washed in arginine-free minimal media and replica-plated onto minimal plates supplemented with exogenous cytosine, thymine and uracil. Growth was scored after overnight incubation at 37°C. "-" no growth on the plates after 24 hours incubation
M9 + G
M9 + G + P
Effect of ΔargR on culture growth in minimal media. Overnight cultures in LB were washed in minimal salts 3 times and subcultured at 1:1000 dilution into minimal media and grown at 37°C, 200 rpm, and samples were plated on minimal media to determine the average colony size.
Generation Time (h)
Average Colony (mm)
1.31 ± 0.12
1.21 ± 0.02
2.14 ± 0.28
0.74 ± 0.02
M9 + P
1.21 ± 0.07
1.30 ± 0.03
M9 + P
1.27 ± 0.23
0.73 ± 0.02
We further examined the pyrimidine requirement by transforming an argR deletion mutant with an argR-containing plasmid clone from the ASKA collection . Colony size of the ArgR-complemented argR deletion mutant was more than twice that of the control strain after two days growth on minimal media (0.76 ± 0.03 mm vs. 0.34 ± 0.03 mm).
Effect of an astCADBE operon deletion on expression of argCBH
The effect of exogenous arginine on growth
Northern analysis of argH expression
Expression of Argininosuccinate lyase, the product of argH
To determine if RpoS and ArgR modulation of argH expression results in changes in the level of the encoded enzyme, we assayed exponential phase cultures of strains deficient in the expression of these regulators for argininosuccinate lyase activity. This was tested by growing cultures in minimal media at suboptimal levels since the RpoS effect was most pronounced when cells were slightly starved for arginine (Fig. 3).
Specific argininosuccinate lyase (ASL) activity in exponential culture of WT, rpoS-, and ΔargR strains. Cultures were grown in M9 minimal media supplemented with 30 μM L-arginine and harvested at OD600 nm = 0.3. Cell extracts were assayed as described in the Methods section. ASL enzyme assay values were corrected for the low background levels of non-specific activity in the argH- mutant.
Argininosuccinate lyase (U/mg protein)
Per cent of wild type
6.50 ± 0.083
1.53 ± 0.86
159.6 ± 22.0
In this study, we examined RpoS-dependent control of argCBH expression, and its modulation by ArgR and external arginine in Escherichia coli. Using independently-isolated mutants carrying operon fusions in different positions within the argCBH region, we conducted expression studies of this biosynthetic operon by assaying reporter gene fusions and by examining argH transcript levels in both a wild type strain and an rpoS mutant by Northern analysis. Since ArgR also regulates this operon , we evaluated the relative contributions of both ArgR and RpoS to its expression by constructing appropriate double and single null mutants.
RpoS regulates many genes that play important roles in stress resistance and energy metabolism , but a subset of these RpoS-dependent genes including gabP , proP , proU , gadAB  and ldcC  aid in amino acid transport and utilization. In a previous genetic screen for RpoS-dependent genes , we identified one mutant that was auxotrophic for arginine and carried a mutation that mapped to the terminal gene member of the argCBH operon. To the best of our knowledge, this is the only RpoS-modulated gene known which, when mutated, renders the cell auxotrophic. As such, examining the regulation of this operon may offer unique insight into RpoS-controlled stationary phase physiology.
Our data showing that stationary phase expression of the argCBH operon is affected by RpoS does not reveal whether this effect is direct or indirect. In fact for many members of the RpoS regulon such information has not been established. Indirect regulation is known to be operant for at least some members, including gadA and gadB, two glutamate decarboxylases that are among the most highly RpoS-dependent genes based on microarray analysis . The expression of these genes depends on GadX, a regulator whose growth phase dependent increase expression requires RpoS .
RpoS can regulate its operon members directly (e.g. osmY ) or indirectly (e.g. gadW by the RpoS-dependent GadX regulator ). As RpoS dependence of argCBH was not observed in ΔargR mutants, ArgR appears to be necessary for RpoS-modulated expression of the operon. There are at least two mechanisms that could explain the increase in expression in stationary phase. In the first, as RpoS activates expression of its large regulon, depletion of intracellular arginine may result as a consequence of de novo synthesis of stationary phase proteins. This may derepress the arginine biosynthetic pathway, resulting in an increase in argCBH expression. Alternatively, increased catabolism through the RpoS-dependent AST pathway lower intracellular arginine and might also result in de-repression of the operon. The latter explanation, however, seems unlikely in view of the fact that RpoS modulation of argCBH is not affected by deletion of the AST operon (this study).
Using the arginine auxotroph (HS1072), we found that E. coli becomes growth limited at arginine concentrations below 60 μM. As derepression also occurs at these concentrations (this study), it appears that expression of the biosynthetic pathway is closely coupled to the biosynthetic need for arginine. As the concentration of arginine in LB media is about 60 μM , it is possible that our results could be partially explained by depletion of arginine during growth in late exponential phase. However, as supplementation with exogenous arginine did not markedly reduce stationary phase induction of the argCBH operon, it is likely that other mechanisms, including control by RpoS, ensure that this operon continues to be expressed under nutrient limited conditions.
Surprisingly, maximum levels of argCBH expression in the wild type strain were only one third of those found in an isogenic ΔargR mutant suggesting that ArgR can be an active repressor even in the absence of exogenous arginine. This may be due to the fact that, even under starvation conditions, synthesized endogenous arginine can be an effective co-repressor. Such control may be physiologically necessary as carbamoylphosphate, an arginine precursor, is also required for pyrimidine biosynthesis. Balancing these two pathways, arginine and pyrimidine biosynthesis, under nutrient-limited conditions, is likely an important physiological imperative, as complete derepression of arginine biosynthesis, by deletion of argR, causes cells to develop a partial requirement for exogenous pyrimidine (this study). The need for de novo arginine synthesis therefore appears to be balanced against other biosynthetic requirements of the cell. he multiple controls on carAB, including availability of arginine, pyrimidines as well purines  ensure that the synthesis of these macromolecule precursors is balanced in actively growing cells.
Why might arginine biosynthesis be stationary phase dependent? It is well established that nutrient scavenging is an important survival mechanism in starved cultures . Arginine in particular is likely to be an important metabolite in stationary phase cultures for several reasons. As arginine represents 11 percent of the cells total nitrogen , it is potentially an important nitrogen reservoir for starving populations. Arginine is also a potential precursor for the biosynthesis of polyamines which stabilize and condense DNA during senescence  and protect it against oxidative damage [7, 8, 42]. Finally, as de novo protein synthesis in non-growing stationary phase cells is required for the expression of stationary phase adaptive proteins, this may impose a significant biosynthetic demand upon the cell both because there are many such proteins produced (see  for review) and because some of these are expressed to extraordinarily high levels. For example, Dps, a highly RpoS-dependent DNA binding protein , is almost undetectable in exponential phase, but accumulates to 200,000 molecules per cell in stationary phase (approx. 5% of total cellular protein) . Many genes are induced upon entry into stationary phase and it is likely that this creates a high demand for amino acids for de novo protein synthesis. The up-regulation of amino acid biosynthetic operons such as argCBH may provide a means to satisfy this demand in addition to nutrient scavenging mechanisms including arginine transport which is also a key factor in maintaining high arginine levels in stationary phase cultures .
While our studies employed a non-pathogenic E. coli K-12 strain, the results of this study may have relevance for E. coli pathogenesis. For example, though urine is a good growth media for uropathogenic E. coli , low concentration of several key nutrients, including arginine  and iron , can be limiting. As both transport  and biosynthesis  of arginine are required for maximum growth in urine and in minimal media containing restrictive levels of arginine, control of the functions for the metabolism of this amino acid are likely critical for urovirulence. As RpoS has now been implicated in both control of biosynthesis (this study) and catabolism of arginine , it will be useful, in future studies, to establish the relative importance of these metabolic functions in pathogenesis.
In summary, argCBH expression is clearly controlled by a finely balanced mechanism mediated by two signals: 1) a general nutrient stress signal mediated, in part, by RpoS and, 2) well known specific control through arginine-dependent modulation of the ArgR repressor.
Bacterial strains, phage, and plasmids
E. coli strains and bacteriophage used in this study.
Prototrophic E. coli K-12, F- λ-rph
CGSC, Yale University
as GC4468 but rpoS13::Tn10
as GC4468 but argH+-λplac Mu53[Φ(argH-lacZ)66](rsd 1066)
as HS1066 but rpoS13:: Tn10
as GC4468 but argH--λplac Mu53[Φ(argH-lacZ)72](rsd 1072)
as HS1072 but rpoS13:: Tn10
as MG1655 but ΔargR:: cat
as GC4468 but ΔargR:: cat
as GC122 but ΔargR:: cat
as HS1066 but ΔargR:: cat
as HS1066p but ΔargR:: cat
as HS1072 but ΔargR:: cat
as HS1072p but ΔargR:: cat
As HS1066 but ΔastCADBE::cat
As HS3006 but rpoS13:: Tn10
generalized transducing phage
Template plasmid for gene disruption, cat is flanked by FRT sites.
λ Red recombinase expression plasmid under control of an araC-P araB inducible promoter.
Derivative of pCA24N
H. Mori 
Media and chemicals
All chemicals were supplied by either Sigma Chemical or Gibco BRL. Cultures were routinely grown in Luria-Bertani (LB) media and in M9 minimal media . The antibiotics used were ampicillin (100 μg ml-1), chloramphenicol (25 μg ml-1), kanamycin (50 μg ml-1), tetracycline (15 μg ml-1), and streptomycin (100 μg ml-1).
All cultures were grown in triplicate from independently isolated colonies. Cell growth was monitored spectrophotometrically (Novaspec® II spectrophotometer, Pharmacia LKB Biochrom Ltd., Cambridge, England) by measuring optical density at 600 nm (OD600). Expression studies in rich media were conducted using cultures maintained in early exponential phase (OD600 of < 0.3) in antibiotic-free LB media for at least 8 generations, prior to the start of the experiment. Sub-cultures with a starting OD600 of 0.01 were grown in LB at 37°C and agitated at 200 rpm.
To quantify the RpoS dependence of argCBH expression in relation to exogenous arginine concentration in minimal media, overnight minimal media cultures (0.4% glucose) were inoculated from well-isolated colonies on minimal media plates (0.2% glucose) and grown with appropriate antibiotics. To ensure complete repression of arginine biosynthesis, the overnight cultures were supplemented with 230 μM L-arginine. The cultures were diluted (1 in 1000) and maintained in early exponential phase (as described above) prior to the start of experiments in antibiotic-free minimal media supplemented with 230 μM L-arginine. At an OD600 of 0.3, cultures were placed on ice for 2 min and then centrifuged for 10 min at 4000 × g at room temperature. The supernatant was decanted and the resulting cell pellets washed twice with arginine-free minimal media to remove remaining exogenous arginine. The arginine-free cell pellets were re-suspended in minimal media to the same optical density as collected. A series of sub-cultures with a starting OD600 of 0.05 were made into minimal media supplemented with various concentrations of exogenous L-arginine. The sub-cultures were incubated at 37°C and agitated at 200 rpm. For each concentration of L-arginine, samples were taken in mid-exponential phase (OD600 of 0.3) and assayed for β-galactosidase activity
β-galactosidase activity was assayed as previously described by Miller . ONPG was used as the substrate, and activity was expressed in Miller units . All cultures were grown in triplicate from independent colony isolates (biological replicates) and all assays were performed in duplicate.
Argininosuccinate lyase (ASL) activity was determined by measuring the absorbance of fumarate hydrolyzed from argininosuccinate at OD240 nm . Cell extracts were prepared by sonication . The reaction mixtures containing 10 ug/ml protein, 1.0 mM argininosuccinate in 50 mM potassium phosphate buffer (pH7.5) were monitored photometrically at OD240 nm. One unit of ASL activity corresponds to 1 nmole L-argininosuccinate hydrolysized per min at pH 7.5 and 37°C.
Construction of ΔargR and ΔastCADBE deletion mutants
The one-step chromosomal gene inactivation procedure of Datsenko and Wanner  was used to generate precise ΔargR and ΔastCADBE deletion mutations. The mutation was transduced  into other strains using P1vir transduction (see Table 5).
The pKD3 plasmid was used as a template to amplify the PCR fragments used for replacement of the argR and astCADBE target genes. Primers were designed such that the resulting PCR product includes the Cmr cassette from pKD3 flanked by sequences adjacent to the target reading frame in the MG1655 chromosome. The PCR primers used for argR were: forward 5'-CAATAATGTTG TATCAACCACCATATCGGGTGACTT GTGTAGGCTGAAGCTGCTTC-3' and reverse 5'-ACATTTTCCCCGCCGTCAGAAACGACGGGGCAGAGA CATATGA ATATCCTCCTTAG-3'; primers used for creating astCADBE deletion were: forward 5'-ACTTAATACCCGCAGAATGATTTCTGCGGGTAAGTA GTGTAGG CTGGAGCTGCTTC-3' and reverse 5'-CATATAAATAACGAATTATTTACTGTA GAGGTCGCT CATATGAATATCCTCCTTAG-3'. The bold text corresponds to target gene flanking sequences, and normal text represents DNA sequences of the Cmr cassette. The deletion generated the entire target coding sequence.
Incorporation of the Cmr cassette into the MG1655 chromosome was confirmed by PCR using genomic DNA as a template and confirmational primers. The confirmational forward primers used were the forward primers (as described above). The reverse confirmational primer for argR was 5'-TGTCGCA GTAAAACGCACTA-3', for astCADBE was 5'-TTATACGCAAGGCGACAAGG-3'.
All primers were synthesized by MOBIXLab, McMaster University (Hamilton, ON).
RNA Isolation and Northern Analyses
RNA was isolated from cultures grown in LB using the hot phenol method . Primers to the argH gene (5'-CGGTTCAAACAATTCAACGA-3' and 5'-GCAGCTTTTTGCCTAACTGG-3') were used to PCR-amplify a DNA probe for hybridization studies to examine stationary phase and RpoS dependence of argH expression. RNA samples were prepared, separated by electrophoresis and hybridized as previously described . Probes were prepared and radioactively labeled by PCR as described in . Densitometric analysis of the bands was performed using a Storm® (Amersham Biosciences, Inc., Baie d'Urfe, QC) gel and blotting imaging system with ImageQuant™ v 5.2 (Amersham Biosciences, Inc.).
This work was supported by grants from the Natural Sciences and Engineering Research Council (NSERC) of Canada to H.E. Schellhorn. We thank C.M. Patten, Y.D. Li and S. Tariq for critical review of the manuscript. We also thank E. Brown for supplying strains from the Nara collection and H. Mori and co-workers for developing these collections and making them available for general use. M.R. Schertzberg was supported by an Ontario Graduate Scholarship and M.G. Kirchhof was the recipient of an NSERC undergraduate summer scholarship.
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