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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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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). However, Escherichia coli survives this acidity nearly as well as the stomach pathogen Helicobacter pylori (Gorden & Small, 1993; Lin et al., 1996). Acid resistance (AR) appears to contribute to the low infectious dose of pathogenic E. coli and aids the gastric passage of commensal strains (Giannella et al., 1973; Price et al., 2004).
Four E. coli AR systems have been described, three of which, the glutamate-, arginine- and lysine-dependent systems, are based on amino acid decarboxylation reactions (Castanie-Cornet et al., 1999; Lin et al., 1995; Richard & Foster, 2003). The decarboxylases consume an intracellular proton while removing CO2 from their amino acid substrates. Decarboxylation products are then expelled by specific antiporters in exchange for new substrate (Gong et al., 2003; Iyer et al., 2003). This process changes internal pH and electrical charge in ways that enable the cell to survive extreme acid stress (Richard & Foster, 2004).
Glutamate-dependent AR (GDAR) is the most effective system. It is composed of two isoforms of glutamate decarboxylase, GadA and GadB (Smith et al., 1992), and the membrane-bound antiporter GadC that exchanges glutamate for the decarboxylation product 
-aminobutyric acid (GABA) (Richard & Foster, 2004). Induction of GadABC is multifactorial and includes the AraC-like regulator GadX, formerly YhiX (Hommais et al., 2001; Ma et al., 2002; Shin et al., 2001; Tramonti et al., 2003; Tucker et al., 2002, 2003), the AraC-family proteins GadW (Ma et al., 2002; Tramonti et al., 2006) and YdeO (Masuda & Church, 2003), the LuxR-family regulator GadE (Hommais et al., 2004; Ma et al., 2003b), the EvgSA two-component regulatory system (Masuda & Church, 2002), the alternative sigma factor RpoS (Castanie-Cornet et al., 1999), the signal GTPase MnmE (Gong et al., 2004), as well as RcsF, TorR, Crp and H-NS (Bordi et al., 2003; Castanie-Cornet et al., 2006; De Biase et al., 1999; Ma et al., 2002; Tramonti et al., 2002). This large number of regulators probably reflects a need to connect induction of GDAR to many facets of cell physiology, but makes the definition of regulatory circuits difficult.
GadE is required to induce gadA and gadBC under all circumstances (Ma et al., 2003b). Most of the other regulators influence the system by controlling gadE. However, which regulators are used differs depending on growth phase and medium. For instance, EvgA, YdeO and GadE itself form a branched regulatory loop that activates gadE during exponential growth in pH 5.5 minimal medium (Ma et al., 2004). However, neither EvgA nor YdeO is required for gadE expression in stationary phase. A second circuit involving MnmE activates gadE during stationary-phase growth in Luria–Bertani (LB) medium containing glucose. However, in LB lacking glucose, another, unknown circuit takes over (Gong et al., 2004). It was suspected that this alternative gadE control circuit might involve RpoS, GadX and GadW – three regulators required to induce GadABC during growth in LB (Ma et al., 2002; Tramonti et al., 2002, 2006).
RpoS activates gadY, a gene located downstream of gadX, whose small-RNA (sRNA) product stabilizes gadX mRNA (Opdyke et al., 2004). The resulting increase in GadX somehow activates gadA and gadBC (Giangrossi et al., 2005; Ma et al., 2002; Shin et al., 2001; Tramonti et al., 2002, 2006). GadX and GadW bind and activate the gadA and gadBC promoters in vitro (Tramonti et al., 2006). However, overexpression of GadX in vivo does not induce gadA or gadB in the absence of a gadE+ allele, suggesting that the in vitro results may not reflect in vivo function (Gong et al., 2004). Microarray studies indicate that GadX may actually activate gadE, which, in turn, would activate gadA and gadBC (Hommais et al., 2004; Tucker et al., 2003; Weber et al., 2005). The current study uses in vivo approaches to reexamine the roles of GadX, GadW and RpoS in controlling AR.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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. Constructions of merodiploid chromosomal gadE–lacZ and gadA–lacZ transcriptional fusions have been described previously (Ma et al., 2002, 2003b, 2004).
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AR was tested by diluting an overnight culture (LB or LBG, pH 5.5 or pH 8) to 2x106 c.f.u. ml–1 into pH 2.5 minimal E salts glucose medium (EG medium) containing 1 mM glutamic acid, and percentage survival over time was determined by viable counting (Lin et al., 1995).
Molecular procedures.
P1 transduction, β-galactosidase assays, DNA manipulations, CaCl2 transformation and electroporation were performed by standard methods (Miller, 1992; Sambrook et al., 1989). Results are means of triplicate experiments and fell within 10 % of the stated values.
Transfer of lacZ fusions from E. coli to Salmonella enterica serovar Typhimurium was accomplished by conjugally transferring a plasmid containing P22 phage from TE1335 (EK297) into EF1285 and EF1286 (Elliott, 1992). The resulting phage lysates were used to transduce restrictionless S. Typhimurium SF586 (JR501; Bullas & Ryu, 1983). The resulting constructs (JF4971 and JF1502) contained the gadE–lacZ fusions inserted into the put locus. P22HT105-int was subsequently used to transfer the fusions into the wild-type strain UK1 to make JF4972 and JF5003 (Curtiss et al., 1991).
MBP-GadX was purified, and electrophoretic mobility shift assays (EMSAs) were performed as described previously (Ma et al., 2004; Shin et al., 2001). EMSA was conducted with the gadE sequence between –682 and –355 generated by PCR with oligo-598 (5'-CTAGTGATTTCAACCTACT-3') and oligo-601 (5'-ATGTAATCCGATTTAAATATCGAG-3'). A lacP control sequence [oligo-507 (5'-CCATACGCAAACCGCCTCTCC-3'), oligo-508 (5'-AGTGAATCCGTAATCATGGTCATA-3')] was run in parallel.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). A previous study found that MnmE is required for optimal expression of gadE during growth in LBG (Gong et al., 2004). The effect of RpoS on AR paralleled its effect on gadE–lacZ (Fig. 1b). Thus, RpoS may affect AR primarily by influencing GadE production. RpoS does not affect AR through any gadE-independent mechanism, since overexpressing GadE in an RpoS mutant still activates AR.
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GadX and GadW activate gadE
Individual mutations in gadX or gadW had little effect on gadE–lacZ expression during growth in LB (no glucose). However, a 
gadXW mutation dramatically reduced expression (Fig. 2a, wild-type vs gadXW). Thus, GadX and GadW had redundant effects. However, during growth in glucose (pH 5.5), GadX and GadW activation of gadE was additive (Fig. 2b).
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also reveals that gadE–804to+331–lacZ is acid-induced during growth in LBG but not in the absence of glucose (Fig. 2a, b, wild-type cells). Part of that acid induction appears to involve GadX and GadW acting as partial negative regulators of gadE at pH 8 in glucose. This may be due to the previously demonstrated cross-repression of gadX and gadW on each other (Ma et al., 2003b). Since gadE expression is RpoS-independent during growth on glucose (Fig. 1a), but remains dependent on GadX and/or GadW (Fig. 2b), factors other than RpoS must activate GadX during growth in LBG.
RpoS does not appear to activate gadE through a GadXW-independent pathway, since rpoS, gadXW and rpoS gadXW mutants are equally acid sensitive, and the overexpression of RpoS does not induce gadE in a gadXW mutant (data not shown)
The –360 to –804 region is required for GadX and GadW activation of gadE
The intergenic region controlling gadE expression is large (798 bp). Deletions removing sequences from –804 to –360, or to –195 nt upstream of the translation start, were used to determine where GadX and GadW had effects. Sequences between –360 and –804 were required for maximal gadE expression in LB with or without glucose (Fig. 3, a vs b, d vs e). GadX or GadW alone activated this expression (Fig. 3a, d, fourth bars).
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). However, it will be shown below that this dependence is indirect due to GadE autoinduction from the wild-type gadE+ allele also present in these strains. The results indicate that the major target for GadX and GadW lies between –804 and –360 nt.
The –360 to –804 region inhibits GadE autoactivation
GadE can autoactivate by binding to three GAD box sequences between –233 and –42 nt, shown in Fig. 4(a). Autoinduction was previously seen during exponential growth in minimal glucose media, but not during growth in LB (Ma et al., 2004). Fig. 4 illustrates that in LB at pH 5.5 (black bars) gadE did not autoactivate unless the –360 to –804 region was removed, at which point gadE caused a 10-fold decrease in expression (Fig. 4b, c, filled bars, set 1 vs 4, set 2 vs 5). At pH 8 (open bars) without glucose, some GadE-dependence was noted even in the full-length fusion (Fig. 4b, open bars, set 1 vs 4). However, GadE-dependence was still enhanced by removing the –360 and –804 bp region (open bars, set 2 vs 5).
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). In the merodiploid strain, GadX and GadW stimulate the wild-type gadE+ allele, and the resulting GadE protein activates the –360 and –195 gadE–lacZ fusions. The gadXW mutant no longer makes GadE, so induction of the shorter gadE–lacZ fusions will not occur. This was confirmed when the plasmid pQE-GadE did not activate the full-length gadE–804 to +331–lacZ fusion, even in a gadXW mutant, but did activate the –360 to +331 fusion in the gadXW mutant (data not shown). Thus, an unknown regulatory protein may limit gadE autoactivation by binding between –360 and –804 nt, creating a need for GadX or GadW.
GadX binds to the gadE control region
Regulators EvgA, YdeO and GadE bind to subfragments of the 798 bp gadE upstream control region (Ma et al., 2004). Since GadX control over gadE appeared to require the region upstream of –360 bp, we tested whether GadX, purified as a maltose-binding fusion, could bind to this region. The gadE fragment between –682 and –355 bp was used along with the unrelated lacP fragment as a negative control. The results shown in Fig. 5 reveal that MBP-GadX binds to this region, supporting the hypothesis that GadX can act directly on gadE. The binding is specific, since the reaction mix contains poly-dIC as a nonspecific competitor and because GadX did not shift the lacP promoter (Fig. 5, left-hand panel). Similar attempts to purify active GadW-MBP were not successful.
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reveal that plasmid pQE-gadX increased the expression of gadE–lacZ almost 10-fold in exponential-phase cultures supplemented with 0.1 mM IPTG. Higher concentrations of IPTG decreased growth of the culture, suggesting that GadX overexpression may have an effect on other S. Typhimurium genes (data not shown). GadW, though less effective than GadX, still activated gadE–lacZ between four- and fivefold. These results support the hypothesis that GadX and GadW activate gadE in vivo. The fact that activation was less than expected (based on the E. coli results) suggests that factors in addition to GadX and GadW are important to maximize gadE expression. We also found that neither GadX nor GadW activated expression of the –360 to +331 fusion, confirming that sequences upstream of –360 are important for activation by these proteins (data not shown).
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; Gong et al., 2004). These in vivo results could be explained as an indirect effect of GadX and GadW activating gadE. However, in vitro EMSAs and DNA footprint analysis using GadX and GadW indicate that both proteins can bind to the gadA and gadBC promoters (Ma et al., 2003a, 2002, 2003b; Shin et al., 2001; Tramonti et al., 2002, 2006). More recently, an in vitro effect of GadX on the transcription of gadA and gadB promoters has been demonstrated (Giangrossi et al., 2005). Nevertheless, since the in vivo data presented indicate that GadX and GadW activate gadE, and that GadE is essential for gadA and gadBC induction, it seemed possible that the in vivo roles of GadX and GadW in inducing gadA and gadBC may have more to do with their triggering the expression of GadE. Previous in vivo support for this hypothesis was reported when overexpression of GadX failed to induce gadA or gadB in a gadE mutant strain (Gong et al., 2004).
This hypothesis was further tested using the S. Typhimurium model. A gadB–lacZ fusion was introduced into the Salmonella chromosome, and then plasmids expressing GadX, GadW or GadE were introduced. The results shown in Fig. 6(b) indicate that GadX and GadW had little or no effect on gadB expression, although they did activate gadE (Fig. 6a). In contrast, introducing GadE had a tremendous effect on in vivo gadB activation.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Several induction circuits are evident. First, the response regulator EvgA and the AraC-family activator YdeO create a feed-forward gadE activation circuit that functions in minimal glucose medium (Ma et al., 2004; Masuda & Church, 2003). The second pathway involves GadE autoinduction, also evident in cultures grown in minimal glucose (Ma et al., 2004). A third pathway requires the MnmE (TrmE) molecular switch GTPase and is most evident when cells are grown in LBG (Gong et al., 2004). The current report describes two other regulatory pathways that can activate gadE expression, primarily in rich media. One pathway is GadX-dependent while the other is GadW-dependent. The GadX and GadW pathways activate gadE in stationary-phase LB at any growth pH. Thus, E. coli has developed at least five iterative regulatory circuits that assure activation of gadE and AR under diverse physiological situations.
GadX and GadW appear to play a role in gadE induction regardless of whether glucose is present in the growth medium. During growth in glucose, the two AraC-family regulators collaborate with the MnmE-dependent pathway to effect maximum gadE expresion. However, GadX and GadW appear to be independent of the MnmE-modulated pathway, since an mnmE mutation did not affect the expression of either gadX–lacZ or gadW–lacZ fusions (data not shown). The results presented also indicate that the alternative sigma factor RpoS indirectly activates gadE by first activating gadX. However, the fact that RpoS is not needed for gadE expression in glucose, yet GadX and GadW remain important, suggests the presence of an RpoS-independent route for gadX induction.
The finding that GadX and GadW do not appear to directly activate gadA/BC promoters in vivo, but do so indirectly by activating gadE, contradicts earlier models, including our own. However, based on microarray reports, this result was not totally unexpected (Tucker et al., 2002, 2003). It is certainly possible, even probable based on the in vitro findings, that under some growth condition(s) these regulators will directly bind gadA/BC in vivo and modulate GadE-dependent activation, but that growth condition does not seem to be growth in LB.
The discovery that several additional regulatory layers govern the expression of the E. coli gadE gene underscores the importance that this organism places on becoming acid resistant. Growth to different cell densities in different media clearly results in different physiological states, some of which may presage encounters with extreme acid stress. The AR regulatory network described here appears to be configured in a way that senses dramatic, and perhaps nuanced, changes in chemical signals that coincide with changing physiology. GadX, GadW and YdeO are all AraC-family regulators with potential sensing modules that likely sense different physiological signal molecules in the cell. Each signal molecule could alter the abilities of these proteins to act as activators of gadE or of gadA/BC.
It is also important to recognize that the relevance of this system extends beyond GDAR, since GadE is in fact a global regulator that activates numerous genes in addition to gadA/BC, and negatively regulates biofilm formation in K12 as well as epithelial attachment in enterohaemorrhagic E. coli (EHEC) (Dahan et al., 2004; Hommais et al., 2004; Tatsuno et al., 2003; J. W. Foster, unpublished observation). It is important to learn what signals these regulators sense and then integrate that knowledge into a global view of cell physiology under acid stress.
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ACKNOWLEDGEMENTS |
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Edited by: D. J. Jamieson
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Received 16 February 2007;
revised 4 May 2007;
accepted 10 May 2007.
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