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Department of Microbiology and Immunology, University of South Alabama, College of Medicine, Mobile, AL 36688, USA
Correspondence
John W. Foster
fosterj{at}sungcg.usouthal.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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-aminobutyric acid antiporter encoded by gadC. The regulatory protein GadE is the essential activator of the gadA and gadBC genes. The transcription of gadE, however, is controlled by numerous proteins. Two of these proteins, GadX and GadW, are AraC-family regulators whose sensory input signals are not known. Since Na+ and K+ play important roles in pH homeostasis, the contribution of these ions toward the regulation of this acid-resistance system was examined. The results indicated that a decrease in Na+, but not K+, concentration coincided with diminished acid resistance, and decreased expression of the gadE, gadA and gadBC genes. However, Na+-dependent regulation of these genes dissipated in the absence of GadX and GadW. Since Na+ levels did not regulate gadX or gadW transcription, it is proposed that GadX and GadW sense intracellular Na+ concentration or some consequence of altered Na+ levels.
-aminobutyric acid; HTH, helix–turn–helix |
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). To overcome this challenge, E. coli possesses four known acid-resistance systems (Foster & Moreno, 1999; Gorden & Small, 1993; Hersh et al., 1996; Iyer et al., 2003; Richard & Foster, 2003). Acid-resistance (AR) system 1 (AR1), also referred to as the oxidative system, is a stationary-phase-induced glucose-repressed system that does not require the presence of an amino acid in the challenge medium to function (Castanie-Cornet et al., 1999). The other three systems (AR2, AR3 and AR4) are all amino-acid-dependent systems that require glutamate, arginine and lysine, respectively (Castanie-Cornet et al., 1999; Gong et al., 2003; Iyer et al., 2003; Lin et al., 1995).
All four AR systems provide different levels of protection. AR1 and AR4 provide a minimal level of protection, while AR3 provides moderate protection. The glutamate-dependent (AR2) system is the most robust, and thus the most extensively studied. This system requires glutamate decarboxylase, encoded by gadA and gadB, and a glutamate/-aminobutyric acid (GABA) antiporter (GadC) (Castanie-Cornet et al., 1999; De Biase et al., 1996, 1999; Hersh et al., 1996; Malashkevich et al., 1998; Richard & Foster, 2003). GadA and GadB are isozymes of glutamate decarboxylase, and they are encoded by genes located at different sites on the chromosome (78.98 and 33.8 min, respectively). The gadB and gadC genes are transcribed as an operon (De Biase et al., 1999). As internal pH becomes acidic, GadA/B converts intracellular glutamate to GABA, with the consumption of a proton and the release of CO2. The GABA produced in the decarboxylation reaction is then transported out of the cell through GadC, with the concomitant uptake of glutamate. A continuous cycle of proton consumption through amino-acid decarboxylation raises the internal pH of acid-stressed cells (Castanie-Cornet et al., 1999; Foster & Moreno, 1999; Richard & Foster, 2004). This increase in internal pH is thought to be required for survival in extreme acid stress.
Genetic regulation of this system is complex, and involves numerous regulators. Environmental signals such as acid and osmotic stress, as well as stationary phase signals, are important in inducing gadA/BC expression (Castanie-Cornet & Foster, 2001; Castanie-Cornet et al., 1999; De Biase et al., 1999). Known transcriptional regulators include the alternative sigma factor RpoS, three AraC-family regulators (GadX, GadW and YdeO), cAMP and cAMP receptor protein, GadE (a LuxR-like regulator), TrmE (an Era-like GTPase), PhoP, EvgA/S (a two-component regulatory system) and the RcsCDB phosphorelay (Castanie-Cornet & Foster, 2001; Castanie-Cornet et al., 2006, 1999; De Biase et al., 1999; Gong et al., 2004; Hommais et al., 2001; Ma et al., 2004, 2002, 2003b; Masuda & Church, 2002, 2003; Tramonti et al., 2002; Zwir et al., 2005). The activity of each of these transcriptional regulators leads to the activation or repression of genes involved in glutamate-dependent acid resistance (Foster, 2004).
GadE is the essential activator of the gadA/BC genes. Most of the other regulators influence gadA/BC expression by controlling the expression of gadE. GadX and GadW are two AraC-like regulators that function in this regulatory circuit by controlling the expression of gadE and gadA/BC (Ma et al., 2003a; Tramonti et al., 2006; Sayed et al., 2007). These proteins are known to activate and repress gadA/BC and gadE under different growth conditions; however, the signal that influences their activity has yet to be identified (Ma et al., 2002; Tramonti et al., 2002).
Of interest to this study is the role of Na+ and K+ in regulating gadA/BC expression. We hypothesized that one or both of these ions might regulate acid resistance because they play such important roles in housekeeping pH homeostasis systems (Booth, 1985, 1999; Kroll & Booth, 1983; Lewinson et al., 2004; Padan et al., 1981, 2005; Zilberstein et al., 1982). This investigation has revealed that Na+ levels affect gadA/BC expression during growth into stationary phase. The effects of Na+ on gadA/BC expression appear to be through the modulation of GadX and GadW activity, which, in turn, controls gadE expression.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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. Media included minimal E medium containing 0.4 % glucose (EG) (Vogel & Bonner, 1956), and Na+- and K+-deficient media (modified M63 medium; Miller, 1992) containing 15 mM (NH4)SO4, 18 µM FeSO4.7H2O, 1 mM MgSO4 and 0.2 % glucose. In addition, the Na+-deficient medium (M63K) contained 100 mM KH2PO4, while the K+-deficient medium (M63N) contained 100 mM NaH2PO4. A control medium (M63N/K) containing both KH2PO4 and NaH2PO4 in equal concentrations (50 mM of each) was also used. M63N0/K0, which was used for acid challenge only, contained (NH4)SO4, FeSO4.7H2O, MgSO4 and 0.2 % glucose, with no added NaH2PO4 or KH2PO4. All Na+- and K+-deficient media were made with ultrapure chemicals and double-distilled water. Na+ and K+ measurements were made using Na+- and K+-specific combination electrodes (Orion ROSS Na+ electrode; ThermoOrion ionplus K+ electrode). For acid-resistance assays, the acid challenge medium or H2O was prepared at pH 2.5 (adjusted with HCl). Cultures were grown at 37 °C, with shaking at 220 r.p.m., overnight (18 h) to stationary phase.
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). Briefly, cells were grown overnight in EG, M63K, M63N or M63N/K at pH 5.5. Stationary-phase cultures were diluted 1 : 1000 into prewarmed pH 2.5 M63K, M63N, M63N/K or H2O, with or without 1.6 mM glutamate. To determine if Na+ or K+ was required during acid challenge, cells were grown in minimal EG medium at pH 5.5 to stationary phase. Cells were then harvested, and washed three times in an equal volume of MC buffer (10 mM MgCl2 and 5 mM CaCl2) to remove excess Na+ and K+ from the cells. After the final wash, cells were resuspended in an equal volume of MC buffer, and subsequently diluted 1 : 1000 into the pH 2.5 challenge media indicated (Fig. 1). At various time points, 10 µl aliquots were removed and serially diluted, and 10 µl of each dilution was plated on Luria–Bertani (LB) agar. The numbers of c.f.u. were determined, and percentage survival was calculated relative to time zero.
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) at pH 5.5. Cells were then harvested by centrifugation at 4500 g for 5 min (4 °C), and resuspended in 50 µl 0.1 % SDS. Protein concentrations were measured using the Bio-Rad protein assay reagent. Protein (5 µg) was separated on 10 % polyacrylamide-SDS gels (Bio-Rad), and then transferred to Immobilon-P (PVDF) membranes with a Semiphore transfer cell (Hoefer Scientific) at 100 mA for 2 h. Membranes were blocked with 5 % nonfat milk in Tris-buffered saline (10 mM Tris, pH 8, 150 mM NaCl) containing Tween 20, and incubated with rat (GadA/B) or rabbit (GadC) primary antibodies for 1 h, followed by incubation with anti-rat or -rabbit secondary antibodies for 1 h at room temperature. The blot was developed with ECL detection reagents (Amersham Pharmacia Biotech).
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. Cells were cultured in the indicated medium to stationary phase, and 100 µl of the stationary phase culture was used in the assay. |
RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Consequently, potential roles for these ions in surviving extreme acid stress were investigated. Cells were grown to stationary phase in M63K, M63N or M63N/K at pH 5.5, and subsequently challenged in the same medium at pH 2.5. When cells were grown and acid challenged in M63N (a high-Na+, low-K+ condition), survival was 84 % after 2 h (Fig. 1a
). A similar result was observed when cells were both grown and acid challenged in M63N/K (containing an intermediate level of both Na+ and K+) (Fig. 1a). However, when cells were grown and challenged in M63K (a low-Na+, high-K+ condition), survival was only 3 % after 2 h at pH 2.5 (Fig. 1a). The data suggest that Na+ is important to acid resistance. However, it was unclear whether Na+ was more important during cell growth (i.e. during the induction of acid resistance), or during acid challenge (i.e. via the actual mechanism of acid resistance).
As noted above, Na+ can function as a counter-ion in antiport mechanisms that directly remove H+ from the cytoplasm (Karpel et al., 1991; Kroll & Booth, 1983; Zilberstein et al., 1982). Alternatively, Na+ could act at the gene level by influencing the induction of key system components (Rahav-Manor et al., 1992). We first determined whether Na+ or K+ played a physiological role in the mechanism of acid survival. The gadA/BC genes were induced by growth to stationary phase in pH 5.5 minimal EG medium, which is a high-Na+, high-K+ medium. The induced cells were then extensively washed to remove excess Na+ and K+, and subsequently challenged in M63N, M63N0/K0 (containing no added Na+ or K+) or H2O, at pH 2.5, in the presence or absence of glutamic acid (Fig. 1b). Remarkably, cells survived equally well under all challenge conditions when glutamic acid was present. This result indicates that neither Na+ nor K+ plays a major physiological role during pH 2.5 acid stress.
Na+ levels affect gadA/BC expression
Glutamate decarboxylase and the GadC antiporter are critical components of AR2. To determine whether Na+ or K+ regulates gadA/BC expression, Western blot analyses were performed to examine the levels of GadA/BC proteins. Cells grown to stationary phase in M63K, M63N and M63N/K were harvested, and solubilized in 0.1 % SDS. Cells cultured in media containing high levels of Na+ (either M63N or M63N/K) expressed GadA/BC proteins at high levels (Fig. 2, lanes 2 and 3). In contrast, Fig. 2 (lane 1) shows that cells grown in M63K (low Na+, high K+) poorly expressed the GadA/B decarboxylases and GadC antiporter. This corresponds to the lower level of acid resistance seen under these conditions in Fig. 1(a). These findings suggest that high Na+ levels are involved in inducing gadA/BC expression.
The expressions of gadA and gadBC are controlled at the transcriptional, as well as the translational, level (Castanie-Cornet & Foster, 2001; De Biase et al., 1999; Gong et al., 2004). We next examined which of these levels was influenced by high Na+ by using gadA : : lacZ transcriptional and translational fusions. The results shown in Fig. 3(a, b) indicate that cells grown under high-Na+ (low-K+) conditions (M63N) exhibit a 5.8-fold higher β-galactosidase activity compared with cells cultured in a high-K+ (low-Na+) condition (M63K). Cells grown at intermediate Na+/K+ concentrations (M63N/K) induced gadA at a level that was 3.4-fold above the expression seen with cells grown in low-Na+ M63K medium (Fig. 3a, b). Because similar fold differences were obtained when a gadA : : lacZ translational fusion was examined, it appears that Na+ levels affected gadA/BC transcription, not translation, during growth to stationary phase (Fig. 3b).
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The expression of GadE, the essential activator of gadA/BC, is also regulated by Na+ levels
Of the known activators of gadA and gadBC, GadE appears to be the most important. Thus, we wondered whether the effect of Na+ levels on gadA/BC expression might really be due to an influence of these ions on gadE expression. This question was addressed by examining the influence of Na+ and K+ on the expression of a gadE : : lacZ transcriptional fusion strain. When cells containing a gadE : : lacZ fusion were cultured in M63N (high Na+), gadE expression was threefold higher than that produced when the cells were grown in M63K (low Na+), and 1.75-fold higher than levels made during growth in M63N/K (Fig. 3c). The results indicate that gadE transcription is regulated by Na+ levels. Since GadE is a required activator of gadA and gadBC, the Na+ dependence of gadA/BC is likely to be due to Na+-dependent regulation of gadE.
GadX and GadW affect the Na+-dependent regulation of gadE and gadA
GadX and GadW are two AraC-family regulators that activate the expression of gadA, gadB/C and gadE (Ma et al., 2002; Tramonti et al., 2002; Sayed et al., 2007). Therefore, we questioned whether GadX and/or GadW play a role in the Na+-dependent regulation of gadE, as well as that of gadA. Wild-type (WT) and 
gadX/W strains carrying the gadA : : lacZ reporter were cultured in M63K, M63N and M63N/K. The results presented in Fig. 4(a) indicate that the Na+-dependent induction of gadA exhibited by the WT is lost in the XW mutant. A similar pattern was observed when we examined the gadE : : lacZ reporter strain (Fig. 4b). The gadX/W strain again failed to induce gadE in the high-Na+/low-K+ medium (Fig. 4b).
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). Thus, these data suggest that GadX and GadW affect Na+-dependent gadA expression indirectly through the Na+-dependent regulation of gadE.
GadX and GadW differentially affect gadE : : lacZ expression
The individual effects of GadX and GadW were then analysed to determine whether distinct roles exist for each of these two proteins in gadE expression. In WT cells possessing both gadX+ and gadW+, gadE was induced in high Na+/low K+ (Fig. 5, bar 1 versus bar 5). Either GadX or GadW alone could carry out this activation (Fig. 5, bars 2 and 3 versus bar 4).
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gadX gadW+), actually increased low Na+ expression of gadE compared with WT cells (Fig. 5, bar 5 versus bar 6). This suggests that GadW can activate gadE in low Na+, and that GadX normally prevents or inhibits this. In contrast, when GadX was retained, and GadW was removed (gadX+ gadW), there was little effect on low Na+ expression of gadE (Fig. 5, bars 5 and 7). However, GadX was still needed to activate gadE in low Na+, as seen when comparing the gadW and gadXW results (Fig. 5, compare bars 7 and 8). These data can be explained as GadX repressing the activity of GadW, while also directly activating gadE, under low-Na+ conditions. Under high-Na+ conditions, however, GadX and W had an additive effect on the expression of gadE (Fig. 5, bars 1 versus bars 2 and 3). As for the effect of these mutations on acid resistance, mutants individually defective in gadX or gadW remained acid resistant following growth in high Na+ because of the redundant effects of GadX and GadW on gadE induction (50–60 % survival after 4 h at pH 2.5). In low Na+, however, gadX mutants were actually more acid resistant than the WT, exhibiting 10 % survival versus 1 % survival, respectively, after 4 h at pH 2.5. This occurs because, as shown in Fig. 5, GadW is better at activating gadE when GadX is absent. As noted above, one might argue that the ion-dependent expression of this system is due to low K+ rather than high Na+ levels. That is, high K+ levels repress the system rather than high Na+ levels induce it. However, the effects are probably not due to K+. When both K+ and Na+ were high (as in NK medium), the gadX and gadW phenotypes were similar to those seen using the high-Na+/low-K+ medium, i.e. both GadX and GadW were needed for maximal expression of gadA and gadE (data not shown). If high K+ was the sensed condition, one would have expected that the gadX/gadW phenotypes observed in M63N/K medium would be similar to those seen in M63K medium. They were not.
Na+/K+ levels do not regulate expression of gadX and gadW
We next examined whether the Na+ effect on gadE and gadA expression was due to Na+/K+ effects on gadX or gadW expression. Strains containing gadX : : lacZ or gadW : : lacZ fusions were grown in high-Na+ (M63N), low-Na+ (M63K) and intermediate-Na+ (M63N/K) media, and the effects on expression were determined. The results shown in Fig. 6 reveal that Na+ levels had no significant effect on the transcription of either gadX : : lacZ or gadW : : lacZ, suggesting that Na+-dependent regulation of gadA and gadE is due to the post-transcriptional modulation of GadX and GadW activity, and not to their levels of expression.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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; Small, 1998). AR2, the glutamate-dependent system, is the most robust of the four systems that protect E. coli from acid stresses encountered in the environment and in the stomach of the host (Castanie-Cornet et al., 1999; Iyer et al., 2003; Price et al., 2004). A complex web of regulation controls AR2 expression, and this allows cells to anticipate future exposures to acid stress when growing under a variety of conditions (Castanie-Cornet & Foster, 2001; Castanie-Cornet et al., 1999; De Biase et al., 1999; Gong et al., 2004; Hommais et al., 2001; Ma et al., 2003a, 2004, 2002; Masuda & Church, 2002, 2003; Tramonti et al., 2002). Production of GadE is the focus of much of this regulatory network. Numerous regulatory proteins are known to control gadE expression, including GadE itself, GadX, GadW, CRP, RpoS, YdeO, EvgAS, PhoP and RcsCDB. Despite knowledge of these many regulators, little is known regarding what small molecules influence their activities.
Previous work has shown that cAMP levels affect induction of acid resistance by controlling RpoS production, which, in turn, activates expression of a small RNA (GadY) needed to stabilize gadX mRNA (Jung & Kim, 2003; Ma et al., 2003a; Opdyke et al., 2004). In addition to cAMP, microarray studies have implicated PhoP, which senses Mg+, as a regulator of gadE (Zwir et al., 2005). The current work indicates that Na+ is also involved in this extensive regulatory network. However, it is not clear whether the system senses internal or external Na+ levels, since altering external Na+ concentration will also influence internal Na+ concentration. For instance, it has been shown that changing external Na+ levels from 1 mM to 85 mM will change internal Na+ levels from 5 mM to 14 mM (Lo et al., 2006).
Since GadE is the central activator of gadA and gadBC, it would seem reasonable that the effect of Na+ on gadA/BC expression would be indirect via an effect on GadE activity or expression. GadE belongs to the LuxR family of transcriptional regulators, with homology in the helix–turn–helix (HTH) DNA-binding domain (Fuqua et al., 1994). The LuxR family of regulators is separated into two classes, both of which depend on a chemical or environmental signal to activate or inactivate them (Nasser & Reverchon, 2007; Withers et al., 2001). However, Na+ does not appear to be a signal sensed directly by GadE; instead, Na+ appears to affect the expression of gadE via influences over GadX and GadW.
GadX and GadW are two AraC-like regulators that have been shown to regulate gadA/BC expression (Ma et al., 2002; Tramonti et al., 2002), and have more recently been established as regulators of gadE expression (Sayed et al., 2007). Members of the AraC/XylS family of regulators possess a DNA-binding domain (HTH motif), as well as a dimerization domain (Gallegos et al., 1997). Many of these proteins are also capable of binding ligands, such as arabinose in the case of AraC, that modulate their activity (Gallegos et al., 1997). The data presented indicate that the Na+ level during growth can modulate the activities of GadX and GadW. However, it is not certain whether GadX and/or GadW actually bind Na+, or if external Na+ somehow alters their activities.
The working model fitting the current data suggests that GadW can activate gadE regardless of Na+ levels. GadX, on the other hand, will activate transcription of gadE when Na+ levels are high. However, when Na+ levels are low, GadX appears to inhibit GadW activity. Because Na+ levels did not affect the expression of gadX and gadW operon fusions (Fig. 6), it seems that Na+ post-transcriptionally modulates the activity of these two regulators.
The mechanism by which Na+ modulates GadX and GadW activities is not known. There is some evidence that GadX and GadW can form both homodimers and heterodimers (Ma et al., 2002). Therefore, assuming that the Na+ effect is post-translational and intracellular, the level of Na+ inside the cell may change the effectiveness of these interactions, thereby changing the activity of the proteins. It is also possible that this ion does not affect protein–protein interaction, but affects the activity of the protein directly via ion binding. Alternatively, Na+ may cause some other unknown physiological effect inside the cell that then modulates the activity of GadX and GadW.
It is known that changing external Na+ levels from 1 mM to 85 mM changes internal Na+ levels from 5 mM to 14 mM (Lo et al., 2006). Other published measurements indicate that growth pH also alters intracellular Na+ levels, changing them from approximately 0.1 µmol (mg protein)–1 to 0.4 µmol (mg protein)–1 during growth at pH 8.3 and 6, respectively (Shijuku et al., 2001). Thus, even though we cannot rule out the possibility that external Na+ levels are responsible for the effects seen, the evidence that external Na+ levels and pH affect internal Na+ levels is consistent with the idea that an acid-associated increase in internal Na+ levels could contribute to the acid induction of the GAD system.
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ACKNOWLEDGEMENTS |
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Edited by: D. J. Jamieson
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Received 2 March 2007;
revised 16 May 2007;
accepted 28 May 2007.
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